CONTRIBUTIONS FROM THE SYMPOSIUMHUMAN EVOLUTION: PAST, PRESENT & FUTURE London 8–10th May 2013

PART 1 – 2013

Letter from EditorIntroduction

Peter Rhys-Evans

1. Human’s Association with Water Bodies: The ‘Exaggerated Diving Reflex’ and its Relationship with the Evolutionary Allometry of Human Pelvic and Brain Sizes

Oppenheimer S

2. Human Ecological Breadth: Why Neither Savanna nor Aquatic Hypotheses Can Hold Water

Langdon JH

3. Endurance Running Versus Underwater Foraging: An Anatomical and Palaeoecological Perspective

Munro S

4. Wading Hypotheses of the Origin of Human Bipedalism Kuliukas A

5. The Aquatic Ape Evolves: Common Misconceptions and Unproven Assumptions about the So-Called Aquatic Ape Hypothesis

Verhaegen M (see below)

6. The Epigenetic Emergence of Culture at the Coastline: Interaction of Genes, Nutrition, Environment and Demography

Broadhurst CL & Crawford MA

PART 2 – 2014

7. Man's Place Among the Diving Mammals Fahlman A & Schagatay E

8. The Origin of Articulate Language Revisited: The Potential of a Semi-Aquatic Past of Human Ancestors to Explain the Origin of Human Musicality and Articulate Language

Vaneechoutte M

9. The Darwinian-Like Evolution of Language From Near Incipient Vernaculars to Modern Idioms

Bichakjian BH

10. Surfer’s Ear (Aural Exostoses) Provides Hard Evidence of Man’s Aquatic Past Rhys Evans PH & Cameron M

11. Human Brain Changes Resulting from an Aquatic Phase in Hominid Evolution Chiarelli B

12. Dental Microwear and Diet: As Indicators of Geographic and Cultural Contexts in Human Evolution

Puech P-F & Pinilla B

13. Aquatic Adapting of Human Newborns Meijers DJW

14. A Living Based on Breath-Hold Diving in the Bajau Laut Abrahamsson E & Schagatay E

15. Human Breath-Hold Diving Ability Schagatay E

16. Sara Campbell, World Champion in Deep Diving After 9 Months of Training – How Is This Possible?

Johansson O & Schagatay E

17. The Global Crisis in Brain Nutrition and the Rise in Mental-Ill Health Crawford MA, Hussein I, Nyuar KB & Broadhurst CL

18. What About the Future of Homo sapiens? Odent M

Book ReviewsChart Summarizing Aquatic Adaptations

Chan WC

Marc Verhaegen Human Evolution

The Aquatic Ape evolves: Common Misconceptions and Unproven Assumptions about the so-called Aquatc Ape Hypothesis

2013 Human Evolution 28: 237-266 Morphological Distance between Australopithecine, Human and Ape Skulls

1996 Human Evolution 11: 35-41 Australopithecines: Ancestors of the African Apes?

1994 Human Evolution 9: 121-139 Did Robust Australopithecines Partly Feed on Hard Parts of Gramineae?

1992 Human Evolution 7: 63-64 African Ape Ancestry

1990 Human Evolution 5: 295-297 Letter to the Editor

1987 Human Evolution 2: 381 Possible Preadaptations to Speech: A Preliminary Comparative Approach

2004 Human Evolution 19: 53-70 + Stephen MunroHominid Lifestyle reconsidered: Paleo-environmental and Comparative Data

2000 Human Evolution 15: 151-162 + Pierre-François Puech

THE AQUATIC APE EVOLVES: COMMON MISCONCEPTIONS AND UNPROVEN ASSUMPTIONS ABOUT THE SO-CALLED AQUATC APE HYPOTHESIS

Human Evolution 28: 237-266, 2013

AbstractWhile some paleo-anthropologists remain skeptical, data

from diverse biological and anthropological disciplines leave little doubt that human ancestors were at some point in our past semi-aquatic: wading, swimming and/or diving in shallow waters in search of waterside or aquatic foods. However, the exact scenario—how, where and when these semi-aquatic adaptations happened, how profound they were, and how they fitinto the hominid fossil record—is still disputed, even among anthropologists who assume some semi-aquatic adaptations.

Here, I argue that the most intense phase(s) of semi-aquatic adaptation in human ancestry occurred when populationsbelonging to the genus Homo adapted to slow and shallow

littoral diving for sessile foods such as shellfish during part(s) of the Pleistocene epoch (Ice Ages), presumably along African or South-Asian coasts.

Keywords :Human evolution, Littoral theory, Aquarboreal theory, Aquatic ape, AAT, Archaic Homo, Homo erectus, Neanderthal, Bipedalism, Speech origins, Alister Hardy, Elaine Morgan, Comparative biology, Pachyosteosclerosis

Contents

IntroductionWikipedia: a reliable source?What is AAH—and what is it not?Analytical comparative approachBipedalismSpeech Early hominoids: peri-Tethys dispersal in coastal forests? Homo: from diving to wading? Conclusions

Introduction

The term aquatic ape gives an incorrect impression of our semi-aquatic ancestors. Better terms are in my opinion the coastal dispersal model (Munro 2010) or the littoral theory of human evolution, but although littoral seems to be a more appropriate biological term here than aquatic, throughout this paper I will use the well-known and commonly used term AAH (Aquatic Ape Hypotheses) as shorthand for all sorts of waterside and semi-aquatic hypotheses (note paleoanthropologists sometimes use AAH for African-Ape-Human clade).

Popular and semi-scientific websites about AAH (e.g. Wikipedia) and even some supposedly scientific papers (e.g. Langdon 1997) appear to contain several biased or outdated views on AAH, giving lay-people and new students of AAH wrong impressions of our ancestors’ likely waterside past. Many of these unproven prejudices are widespread, not only among AAH opponents, but also among proponents. Some of these misconceptions find their origin in the original writings of the ‘father of AAH’ Sir Alister Hardy (e.g. on the timing of our aquatic past, and on the transition towards it), in the books of Elaine Morgan (who has done most to promote AAH) or

in common interpretations of AAH proponents (e.g. on bipedalism, and on laryngeal descent). Others derive from wide-spread interpretations and unproven assumptions in popular writings on human evolution, or even in more scientific papers, for instance, on savanna adaptations, on running, hunting and meat-eating, and on australopiths being human ancestors.

This paper first briefly discusses the AAH website in Wikipedia. Then it lists a number of popular misconceptions onAAH by opponents as well as proponents. Thereafter it discusses a few important aspects of AAH, such as bipedalism and speech origins. Finally, it briefly provides a possible scenario of ape and human evolution.

Wikipedia: a reliable source?

While Wikipedia is generally a fantastic instrument, usually providing recent and reliable information to lay-people, this is perhaps not always the case in highly controversial topics like human evolution. In spite of the efforts of AAH enthusiasts to update the Wikipedia website Aquatic Ape Hypothesis, the editors of the website appear to take aconservative approach (which in other instances might be a safe strategy). As a result, the AAH website is considerably biased and outdated, relying chiefly on the 1987 Valkenburg conference (Roede et al. 1991), while overlooking most recent literature on AAH.

For example in the first paragraph, instead of referring to a few dozen recent peer-reviewed and detailed publications on different aspects of AAH, Wikipedia refers solely to the only anti-AAH peer-reviewed paper, now sixteen years old: “An extensive criticism appeared in a peer reviewed paper by John H. Langdon in 1997. Langdon states that the AAH is one of manyhypotheses attempting to explain human evolution through a single causal mechanism, and that the evolutionary fossil record does not support such a proposal; that the hypothesis is internally inconsistent, has less explanatory power than its proponents claim, and that alternative terrestrial hypotheses are much better supported. AAH is popular among laypeople and has continued support by a minority of scholars.Langdon attributes this to the attraction of simplistic single-cause theories over the much more complex, but better-

supported models with multiple causality.” However, the article fails to mention that Langdon’s

paper has been thoroughly answered in peer-reviewed publications not mentioned by the Wikipedia article. Suffice it to say that Langdon merely gives his personal thoughts without scientific argumentation. AAH is no simplistic, single-cause theory. On the contrary, waterside hypotheses provide an extra viewpoint to human evolution, not discussed by conventional anthropologists: AAH not only considers forest- and open plain dwelling, but also the possibility that human ancestors at some time lived along coasts, rivers, swamps etc.AAH is internally consistent, and, compared to purely terrestrial hypotheses (forests vs. plains, tropical vs. cold,scavenging vs. hunting, etc.), it offers incomparably greater explanatory power, as shown below as well as in the many recent publications not consulted by Langdon.

The Wikipedia AAH article bluntly declares: “There is no fossil evidence to support the AAH”, but fails to refer to relevant publications (e.g. Walter et al. 2000, Gutierrez et al. 2001, Joordens et al. 2009, Munro 2010). In fact, our extensive reviews of the literature as well as the malacological (mollusc) and other paleo-environmental evidence suggest that virtually all archaic Homo sites are connected with abundant edible shellfish (Verhaegen et al. 2007, Munro 2010, Table 5 in Munro & Verhaegen 2011).

The Wikipedia article also states without argument: “Several theoretical problems have been found with the AAH.” In our opinion, the littoral theory instead offers theoreticalas well as practical solutions to several problems in conventional paleo-anthropology, as shown below.

The site continues: “some claims made by the AAH have been challenged as having explanations aside from a period of aquatic adaptation … most of these traits have an explanation within conventional theories of human evolution.” But the older and more conventional ideas suggest that human ancestorsevolved from forests or trees to more open plains, without considering alternatives. These open plain ideas are anthropocentric just-so interpretations: uniquely-human (not seen in non-human animals) constructions attempting to fit thehuman condition. For instance, they ‘explain’ fur loss by heat, and subcutaneous fat by cold, not considering the possibility that human ancestors, like all mammals that are

both furless and fat, could have spent a lot of time in the water. All the purported objections by conservative anthropologists have been addressed and answered in recent publications on AAH, not cited in Wikipedia’s entry (e.g. Verhaegen et al. 2007, Munro & Verhaegen 2011).

The Wikipedia article claims that human traits such as bipedalism and laryngeal descent have been considered by proponents to be pro AAH arguments. However, this is not the general AAH opinion, currently. According to Hardy’s method (comparative biology), neither bipedalism nor laryngeal descent can be considered as pro AAH arguments. There are no bipedal (semi)aquatic animals apart from (wading) birds, and even the semi-aquatic penguins are only bipedal when outside thewater. The same holds for laryngeal descent. For instance, Cetacea have ascended (intra-narial) larynges, not descended. These matters have been discussed (see also below) in several publications not mentioned in the Wikipedia article (e.g. Verhaegen 1993, Verhaegen & Munro 2007).

The article is also biased in citing anti-AAH comments, while failing to mention the obvious responses. One opponent claims that AAH “explains all of these features … twice. Everyone of the features encompassed by the theory still requires areason for it to be maintained after hominids left the aquaticenvironment”, yet seems to be unaware of the existence of phylogenetic inertia as well as of rudiments in evolution, and has apparently not heard of the title of Elaine Morgan’s book The Scars of Evolution: as Morgan explained repeatedly, AAH is based onembryological, anatomical, physiological etc. remnant traits of our past that are not typically seen in terrestrial mammals. She quoted Stephen Gould: “the remnants of the past that don’t make sense in present terms—the useless, the odd, the peculiar, the incongruous—are the signs of history.”

Equally selective is the Wikipedia article’s mentioning Greg Laden’s anti-AAH comments in 2009, yet omitting Laden’s more recent and positive blog on AAH (Laden 2013).

The Wikipedia article mentions the recent eBook on AAH (Vaneechoutte et al. eds 2011), but then cites from Langdon’s review of that book, instead of discussing the fifteen actual contributions in the eBook. The site verbosely writes about Langdon’s opinion (outdated and no longer relevant, see above), yet not about recent peer-reviewed critiques of Langdon’s publications (Kuliukas 2011, Vaneechoutte et al. 2012).

It also does not mention many intriguing contributions in the eBook on different aspects of AAH, and it misrepresents or omits our own chapters on Miocene ape and australopith evolution, on Pleistocene Homo, and on speech origins.

These are only a few examples, but they support the idea that the Wikipedia article is prejudiced toward outdated and ill-informed opinions on what AAH is as defined and misunderstood by its critics rather than on the recent publications exploring the theory itself.

Of course, the same can be said about some similarly unscientific blogs and websites on the Internet mentioning AAH.

What is AAH—and what is it not?

In popular discussions, it is often incorrectly assumed by opponents, and even by some proponents, that AAH proposes that our most-aquatic phase happened before the time of the australopiths. Such an early phase (late Miocene), however, isunlikely. I provide a number of possible (often overlapping) pitfalls on ideas on AAH.

In my opinion, * AAH is not about becoming aquatically adapted by gradually wading deeper

on two legs at the beach. Hardy (1960) imagined that human ancestors might have

become more aquatic by wading deeper and deeper at the beach. But since early Primates were arboreal, and since Darwinian evolution generally does not make great leaps, a transition towards a more aquatic lifestyle likely happened in a milieu where both trees and water were present, rather than on open rocky or sandy shores. Flooded, swamp and mangrove forests andlater wetlands are indeed where virtually all fossils of Mio-Pliocene hominoids are found: as we discuss elsewhere (e.g. Verhaegen & Puech 2000, Verhaegen et al. 2002, Verhaegen et al. 2011), the transition towards more aquaticness therefore did not start at the beach as Hardy and other AAH advocates have suggested, but rather in densely vegetated mangrove or swamp forests—wet forests were more abundant in the Mio-Pliocene (23–5.3–2.59 Ma, million years ago) than in the Pleistocene epoch (2588–12 ka, kilo-years ago)—by descending into the water below the branches, and by spending less and less time in the trees and more in the water, for instance, collecting

easily obtainable foods they found near the water surface, possibly not unlike lowland gorillas collecting aquatic herbaceousvegetation (AHV) in forest bais (Doran & McNeilage 1998). Such semi-arboreal semi-aquatic lifestyles have been called aquarboreal byWilliams (2006). Typical hominoid features (as opposed to monkeys) such as below-branch climbing, a broad thorax with dorsal scapulae and arms aside, complete tail loss, and a morevertical and central spine (Schultz 1969) are parsimoniously explained by vertical aquarborealism (Verhaegen et al. 2011). The remarkably humanlike lumbar vertebra of Morotopithecus (e.g. MacLatchy et al. 2000, Filler 2007) suggests that (at least some)Miocene hominoids were already orthograde ~18 Ma (the exact datesdo not affect my proposed scenario), i.e. with habitually-vertical lumbar spines in as well as outside the water. Since the early great hominoids acquired thick cheekteeth enamel (e.g. Afropithecus–Morotopithecus, Griphopithecus etc.) and since all extant great apes use and even make stone tools (Breuer et al. 2005), the diet of the great hominoid last common ancestors might have been durophagous, partially feeding on hard objects,for instance, nuts or hard-shelled invertebrates (HSI). Note the thick-enameled capuchin monkeys Cebus apella also use hard tools to open palm nuts and mangrove oysters (Fernandes 1991, Martin et al. 2003).

* AAH is not about why Homo and Pan split, or about what happened at the split, but about what happened during the million years after the split.

Elaine Morgan (personal communications, Internet discussions) suggested that our ancestors becoming more aquatic caused the Homo/Pan split. But at the time of the Homo/Pan split (~5 Ma?) chimpanzee and human ancestors were identical, so the differences between them and us arose (possibly mosaic-like) after that time, i.e. at some time(s) between the split and today, in the Pan branch or in the Homo branch. Evolutionary turn-overs are indeed frequent with drastic climatic changes such as during the Pleistocene through alternation of glacials and interglacials (Ice Ages). Humans are obviously a very special kind of primate: they musthave walked a special or complicated evolutionary path. Indeed, most or all possibly-aquatic traits in the human fossil record (see below the huge brain, POS, ear exostoses, external nose, platycephaly, platymeria, finds in association with marine molluscs, dispersal to islands, etc.) seem to haveappeared after ~2 Ma, at some time in the Pleistocene.

* AAH is not about ‘aquatic apes’ or even australopiths, but about archaic Homo.

Most or all traits that can possibly be explained by a (semi)aquatic past seem to be absent in apes and australopiths, and appear in the fossil record mostly or exclusively in the genus Homo: the spectacular brain enlargement (arguably through the abundant DHA in aquatic foods, see Crawford et al. 2002), an external nose (strongly projecting nasal bones, as in some semi-aquatic mammals), pachy-osteo-sclerosis (POS, very thick and dense bones, as in slow and shallow diving tetrapod species), platycephaly (flattened skull-caps, as in semi-aquatic Carnivora, presumably for hydrodynamic streamlining, see Curtis et al. 2012), platymeria (dorso-ventrally flattened femora, as in Pinnipedia), wide and deep thoraxes (as in most shallow-divingendotherms), ear exostoses (as in human divers in cold water),etc. In the malacological record, marine mollusc species in combination with hominid fossils are not seen with australopiths, but appear together with Homo erectus and relatives (Munro 2010). This does not mean that our ancestors’littoral adaptations could not have begun prior to that time, only that to date we have no evidence of littoral adaptations before the Pleistocene (this absence of Pliocene evidence might or might not be due to the fluctuating sea levels of theIce Ages). Since littoral adaptations seem to be more prominent in Homo erectus than in Neanderthals, later Homo populations might gradually have ventured more and more inlandalong the rivers, where their remains have been found in oxbowlakes at the time (e.g. Mauer in Germany, Lynford in the UK), frequently in paleo-landscapes with reeds and beavers. The Neanderthal diet seems to have been remarkably varied (Hardy &Moncel 2011) and probably included salmon (Bocherens et al. 2013). How aquatic the non-archaic Homo fossils were, is less clear. Which of the different so-called Homo habilis fossils wereclose relatives of archaic Homo (e.g. many O.H. fossils?) and whether some of them might have belonged to the australopiths (e.g. KNM ER-1813?) might be difficult to answer with the present knowledge. In any case, Sahelanthropus, Orrorin, Ardipithecus and australopith fossils have to be studied on their own, apart from Homo’s littoral past: even if they can provide information on how our ancestors before their most-aquatic phase might have looked and lived, they have in my opinion

little bearing on AAH in the strict sense.* AAH is not about what happened 10 or 5 Ma, as Hardy and Morgan thought,

but rather about what happened after ~2 Ma.In 1960, when Hardy wrote his famous paper, it was

generally thought that humans and apes split more than 10 Ma, and since it was commonly believed then (without firm evidence) that australopiths were precursors of humans and hadlived on the open plains, Hardy supposed that the most-aquaticphase must have happened before that time. If that had been the case, most (semi)aquatic traits might have disappeared since then, but the abundance of these traits in humans suggests that our ancestors’ most-aquatic phase happened more recently. Indeed, the first known occurrences of fossil hominids in coastal sediments are probably ~1.8 Ma (Mojokerto), as well as the first hominid fossils or tools outside Africa, so the diaspora of Homo to tropical, subtropical and temperate regions of the Old World (as far as England, Angola, the Cape, China and Flores, between at least 0°E and 120°E, and 52°N and 34°S) might have happened at the beginning of the Pleistocene along the coasts (coastal dispersal model, see Munro 2010), and afterwards from the coasts inland along rivers.

* AAH is less about how modern humans behave in water than about erectus’ differences with sapiens.

In popular AAH discussions, proponents as well as opponents often assume that Homo erectus moved more or less likeus (e.g. the endurance running model), and that if there was evera semi-aquatic episode, this was followed by a more cursorial phase in human evolution (on savannas or elsewhere). This thinking not only underestimates the differences between erectusand sapiens, but is also based on the unproven assumption that when hominid fossils bear humanlike locomotor traits, these traits are adaptations for humanlike locomotion (‘bipedalism’). For instance, the human plantar arch is believed to be an adaptation to running, whereas it should be noted in the first place that cursorial mammals are not plantigrade, but unguli- or digitigrade. Extant humans are in fact very atypical runners: we are relatively slow, on short as well on long distances, we are fully plantigrade, have remarkably short toes, a wide body build, archaic Homo had very heavy skeletons (ballast in running), etc. Virtually all purportedly ‘running’ features of Homo (i.e. where humans

locomotorically differ from chimps) can more parsimoniously beexplained by non-running adaptations (Table 4 in Verhaegen et al.2007): by diving and/or wading locomotions and/or vertical climbing. Conservative views often suppose that there was a more or less straight evolutionary line from apelike towards human locomotion, and that most locomotor differences between humans and apes are adaptations to bipedal walking or running.But primates that evolve from forests to more open terrain typically become more pronograde and quadrupedal, not less. This contradiction has been called the baboon paradox (Bender 1999). On the other hand, many AAH proponents assume that wading led to bipedalism, although bipedalism did not evolve in non-primate wading mammals such as tapirs, hippos or capibaras. Obviously, the different erectus-like fossils should be studied on their own. My quantitative comparative study of extant and fossil hominioid cranio-dental traits showed that the sum of differences between Australopithecus africanus and Homo erectus was only marginally higher than those between H. sapiens and H. erectus (Verhaegen 1996). There were indeed a lot of differences between Homo sapiens and archaic Homo, and even between different fossils of archaic Homo. The following list is not exhaustive. Some archaic Homo specimens were very heavycreatures (e.g. heidelbergensis), and archaic men weighed in some populations much more than the women (e.g. georgicus). The brainsize was initially (already in modjokertensis ~1.8 Ma, which exceeded georgicus) intermediate between australopiths and laterHomo. In archaic Homo skulls, the frontal brain-case was placed behind the eyes rather than above as in sapiens, and the inferior part of the brain skull was relative wider (notably in neanderthalensis). The skull-cap was remarkably flattened and ventrodorsally long (platycephaly), with a heavy eye-protecting ridge (torus) above the orbits (in neanderthalensis largely filled by frontal air sinuses, though not in erectus), and sometimes with parasagittal ‘keeling’ (especially in erectus). Homo erectus s.s. had smaller, but some other archaics (e.g. heidelbergensis) had larger paranasal sinuses than sapiens (see also below Table 2). The dorsal skull (occiput) and many other skeletal parts such as most long limb bones had typically extraordinarily thick cortices (often more than twice as in gorillas), dense bone and narrow medullary canals (POS). Some Javanase erectus specimens had canine diastemata in the maxilla of ~4 mm, about as large as in female orangutans

(G.H.R. von Koenigswald in Puech 1983). Tooth enamel was generally thicker than in sapiens, although some archaic specimens showed enamel dysplasias and even tooth loss (e.g. Margvelashvili et al. 2013). Teeth from Atapuerca (cf. heidelbergensis) were strongly worn as by plant foods such as roots, stems and seeds (Pérez-Pérez et al. 1999). Postcranially, the palms of the hands and soles of the feet were generally wide, the fingers and toes were relatively short, but the fifth digital rays were relatively long compared to the other rays (neanderthalensis). In the shoulder, the glenoid fossae were directed more upwards (possibly for climbing arms-overhead) inthe early-Pleistocene georgicus and ergaster. In most archaics, the femur was dorsoventrally flattened (platymeria). The vertebrae were craniocaudally ‘low’ (platyspondyly) in ergaster (Walker & Leakey 1993). The femoral neck, as in australopiths,was relatively longer than in humans and certainly apes, whichfits the iliac flaring and wide pelvis (platypelloidy) as wellas the more valgus knees than in sapiens and certainly apes. Thelong leg bones and especially the tibiae were relatively shorter than in sapiens. Etcetera. For possible explanations of these differences with sapiens, see below, but it is clear that archaic skeletons (too heavy and too wide) were even less adapted to cursorialism than sapiens.

* AAH is less about bipedal wading (except in later phases <200 ka?) than about slow and shallow diving.

As explained in the previous paragraphs, but not commonlyacknowledged by AAH opponents and some proponents, archaic Homo fossils displayed a number of features that are often seen in shallow-diving mammals: brain expansion, ear exostoses(in some erectus and many neanderthalensis), POS, platymeria, platycephaly and keeling, relatively wide bodies and extremities, midfacial prognathism with projecting nose, etc.,whereas in H. sapiens (in the fossil record after ~200 ka) these possibly-littoral features disappear or become reduced. This does not imply that most or all archaic Homo populations did not frequently wade or walk bipedally, only that we do not have enough evidence to make firm conclusions about how often they waded. Although archaic Homo had relatively larger femoral heads than apes and australopithecines, which suggestsmore frequent bipedalism (standing, wading or walking), they had very heavy skeletons, and at least some of them (e.g. heidelbergensis and neanderthalensis, especially the males) seem to

have had larger bodies than most extant humans. Thick and dense skulls (POS), on the other hand, are exclusively seen inslow and shallow diving tetrapods (e.g. Laurin et al. 2011): there is no reason—apart from conservatism—why archaic Homo should be unlike other animals with POS (Munro & Verhaegen 2011, Verhaegen & Munro 2011). POS, ear exostoses, abundant edible shellfish, human slow-diving skills (Schagatay 2010) etc. all independently point into the same direction: our Pleistocene ancestors were no cursorial runners, but—at least parttime—littoral divers.

* AAH is not about surface-swimming, but about shallow bottom-diving, where Homo’s foods such as shellfish could be found.

Many AAH proponents do not discern clearly between surface-dwelling (which can be called a terrestrial—keeping the head outside the water—rather than an aquatic adaptation) and underwater foraging, and among the latter, between fast swimming (e.g. in open or even oceanic waters) and littoral diving (e.g. in search of sessile foods). In all endotherms that spend time inthe water, hydrostatic adaptations are essential. Buoyancy, especially of the airway entrances, is very important: terrestrial ungulates that live in wetlands, or even only twice a year have to cross dangerous rivers, typically have very large paranasal air sinuses; elephants have huge paranasal sinusus around the trunk origin, and swine around the snout origin, as opposed to hippos (who usually stand and walk on the bottom); and salt water dwellers such as most marine mammals (sea water is ~2.4 % heavier than fresh water) also have reduced or absent air sinuses (Farke 2010, Curtis et al. 2012, and refs in Verhaegen 1991). Homo erectus’ dense and thick skeletons (POS) and small paranasal sinuses are typical of salt-water littoral bottom-diving mammals, and erectus-like fossils are indeed the first hominid fossils that are sometimes found in association with marine molluscs (Munro 2010). In this respect, the East African australopiths Australopithecus afarensis, aethiopicus and boisei were the opposite of Homo. Their more lightly built skull bones with large basicranial air sinuses of as well as their large laryngeal airsacs (as still seen in extant gorillas) are not unexpected in surface-feeders in fresh water habitats such as papyrus swamps, where indeed their fossils have been found (Conroy 1990, Reed 1997): a wetland diet with a lot of papyrus sedges (AHV), possibly supplemented by hard-shelled invertebrates

(HSI) found in reedbeds etc. (Shabel 2010), is confirmed by their dentitional molarization (with superthick enamel protecting against HSI), glossy polished micro-wear (Puech 1992), and isotopic data (van der Merwe et al. 2008).

* AAH is less about what happened in Africa or even the Rift Valley than about what happened on the Indian Ocean or Mediterranean shores.

As opposed to the presence of australopiths in Africa, Homo fossils and tools are found at (sub)tropical and temperatecoasts all over the Old World throughout the Pleistocene, and indeed most of the earliest known archaic Homo fossils come from Java and Georgia (~1.8 Ma), both outside Africa. During the Ice Ages, sea levels dropped, and vast territories, presumably tree-poor and shellfish-rich, became accessible forhandy tool-using omnivores, and since Pleistocene Homo fossilsare found in coastal sediments from different latitudes and longitudes (Indonesia, the Cape, England), the most parsimonious solution is that Homo populations dispersed alongthe coasts between those sites, possibly during the glacial periods on the then exposed continental shelves (Verhaegen & Munro 2002). From the coasts, different populations in parallel followed the rivers inland, arguably at first seasonally (e.g. following anadromous species such as salmon),later sometimes permanently. Joordens et al. (2013) “propose thatthe Indian Ocean coastal strip should be considered as a possible source area for one or more of the multiple Homo species in the Turkana Basin from over 2 Ma onwards.” Since glacial coasts are now far below the present sea level, fossilization of Homo might be biased towards inland lakes or riverbeds such as Lake Turkana in the East African Rift Valley.

* AAH is less about out of or into Africa or Asia scenarios than about coastal diaspora.

Paleo-anthropologists often discuss when early Homo left Africa, but if Pleistocene Homo was originally littoral, the question whether they lived, for instance, on the African or the Asian side of the Red Sea is not very relevant. If Pleistocene Homo dispersed along the coasts, it should be noted that the East-African coasts do not have extensive continental shelves, as opposed to Sunda in Southeast Asia. Some of the oldest archaic fossils (~1.8 Ma) come from coastaland deltaic sediments in Indonesia (Mojokerto, amid shellfish and barnacles) and from a site in Georgia “rich in lacustrine

resources” (Dmanisi, at a confluence of rivers, not so far from the Black–Caspian Sea connection at the time). Both sitesare Asian. Yohn et al. (2005) provide DNA evidence (retroviral data) that human ancestors (this does not necessarily mean allHomo populations then) were outside Africa at least between ~4and 3 Ma. If this is correct, they might have been in southernAsia then, but it does not say where they lived after ~3 Ma. (In fact, theoretically, part of our genome might even have been in Africa at the same time when another part was perhaps in Asia.)

* AAH is less about a riverine evolution in fresh-water than about a coastal lifepossibly followed by a riverine life.

Homo erectus’ POS suggests that they, as all other pachyosteosclerotic tetrapods, collected a considerable part of their food in near-shore salt-water habitats. Two ontological data might confirm this. The human newborn’s vernix caseosa has only been observed among other species in newborn common seals (Don Bowen, personal communication, and Odent 2011). And newborn humans have renculated kidneys (each kidney consisting of numerous small kidneys, from Latin reniculus or renculus, the diminutive of ren), a trait that is most often seenin marine mammals (Williams 2006), but this renculization disappears during childhood, when human kidneys and renal concentration powers become more like those of mammals with free access to fresh water, such as pigs (Verhaegen 1991b). This seems to suggest that a littoral phase in the early Pleistocene (with frequent diving apparently) might have been followed by a more freshwater phase in the late Pleistocene (with more frequent wading presumably).

* AAH is not in the first place about an isolated evolution on an island.LaLumiere (1981) suggested that the semi-aquatic phase

happened on an isolated island (he proposed Danakil, a Mioceneisland in the southern Red Sea). Islandization, however, generally leads to drastic brain reduction in mammals. More likely, AAH is about a littoral and estuarine evolution on African and Eurasian coasts (possibly including near-shore, but not isolated, islands) during most of the Pleistocene. Near-shore islands may have been involved, but a long isolation on one island, such as Danakil, seems unlikely.

* AAH is not about unique anthropocentric explanations, but about universally valid biological correlations.

Hardy (1960) based this theory on comparative anatomy. As

an illustration, the combination of fur loss and abundant subcutaneous fat is only seen in (semi)aquatic mammals. (The reverse is not true. Some illogical opponents reject AAH saying that not all (semi)aquatic mammals are fat and furless.) Some AAH proponents and many opponents, however, usejust-so purportedly-functional explanations for ‘unique’ humanfeatures. For instance, bipedalism is believed to have evolvedfor running over open plains (opponents) or for wading (proponents), subcutaneous fat for thermo-isolation during cold savanna nights in furless mammals (opponents) or for buoyancy in surface-swimming (proponents), laryngeal descent for breathing large amounts of air for open plain running (opponents) or for diving (proponents). But when we use comparative data, and if necessary and possible, analyse thesefeatures into more elementary traits, we discover more realistic and fool-proof, although at first sight sometimes unexpected, correlations. Human locomotion includes, for instance, orthogrady (e.g. seen in gibbons hanging from branches, and in penguins on land), full plantigrady (e.g. as in sealions and ducks on land), very long and straight legs (e.g. in herons and flamingoes more than ostriches) etc. Humanlaryngeal descent also is composed of at least two different elements (Nishimura 2003, 2006, 2008, Nishimura et al. 2003, 2006, 2008): laryngeal descent against the hyoid bone (also inother hominoids, and extremely in e.g. hammerhead bats Hypsignathus monstrosus), and the typically human hyoidal descent against the mandible (whereas Cetacea have ascended larynges). Below I discuss bipedalism and laryngeal descent in somewhat more detail.

* AAH is not about sudden mutations, macro-evolution, saltations or evolutionary jumps from ape- to human-like, but about a mosaic-like evolution in numerous small steps.

AAH is not about a sudden evolutionary shift as thought by many opponents (some even reason: humans are unike aquatic Cetacea and Pinnipedia, hence AAH is wrong) and some proponents (Wescott 1995). Our ancestors’ evolution is not a straight line, for instance, from forest to open plain dwellers. Rather, there were a lot of small (mosaic-like) steps in different directions, as discussed below: in my opinion schematically from pronograde arborealism (above-branch) to pronograde and later orthograde aquarborealism (below-branch) to slow and shallow littoral diving (archaic

Homo) to bipedal wading in very shallow waters (early sapiens) and to walking on terra firma (Table 1).

* AAH is even less about the hominid fossil record than about our own rudiments.

Some opponents criticize AAH for being untestable, as most of the evolutionary adaptations described by AAH proponents would not have fossilized. But AAH is in the first place a biological hypothesis, based on comparisons of extant humans with other animals (parallels) and with chimpanzees (differences): “the remnants of the past that don’t make sensein present terms—the useless, the odd, the peculiar, the incongruous—are the signs of history” (Gould 1977). Although the hominid fossil record can provide relevant information on African ape (australopith) and human (Homo) evolution that would otherwise be unknown (e.g. that most archaic Homo displayed POS, or that many early great hominoids had thick enamel), AAH is based on the anatomy, embryology, physiology, biochemistry and DNA of extant humans compared to our close relatives (chimpanzees and other primates) as well as to animals of different lifestyles (including arboreal, terrestrial, littoral, pelagic, and freshwater). Human ‘odd’ traits—ill-adapted to our present way of life (fur loss, fatness, low speed etc. are unexpected in terrestrial mammals)—give clues to how our ancestors lived.

Analytical comparative approach

AAH is in the first place based on comparative biology, but not all features can easily be compared to comparable features in other animals. Moreover, human features such as language and bipedal locomotion are considered to be unique. Consequently, paleo-anthropologists tend to rely on functionalinterpretations rather than on comparative arguments. However,functional interpretations are often subjective. For instance,since quadrupedal non-human primates live in forests, and bipedal humans live on terra firma, it is easily concluded that the transition from forest to open plain resulted in the adoption of bipedalism. This logical mistake, confusing since and because, is know as post hoc ergo propter hoc ‘after this, therefore because of this’. Once this seemingly-logical interpretation is considered a fact, other misinterpretations follow: since we ‘know’ our ancestors lived on the open

plains, it is easy to conclude that in humans, unlike typical open plain mammals, the function of subcutaneous fat was, for instance, thermal insulation in the cool savanna night, or energy depot during endurance running, or for the dry season. And because it is ‘known’ that human ancestors were living on the open plains, there is no need to consider that subcutaneous fat tissues (often seen in (semi)aquatic but not open plain mammals) could have been a (semi)aquatic adaptation(no matter for what reason: energy storage in the water, thermo-insulation, streamlining, buoyancy, sexual selection, or some other reason). In the same way, conventional paleo-anthropologists who find fossil hominid footbones or footprints automatically assume that such feet evolved ‘for’ running bipedally over open plains, without considering that ostriches (cursorial bipeds) have feet that are higher and shorter than ours, with only two toes, which are spread widelyapart and are unequal in length. In still the same way, since we ‘know’ that we lived on the open plains and that our brainsneed high-quality nutrients (e.g. DHA), and since these nutrients are scarce on the open plain and almost exclusively obtainable from animal food there, it was concluded that our ancestors must have eaten a lot of meat, bone marrow or brainsfrom ‘prey’. This conclusion was corroborated by discoveries of ‘butchering sites’—without considering that all these siteswere lake- or riverside, that archaeological materials could have been washed together there, that stones and bones conserve incomparably better than fish or plant foods (biasingthe archaeological record), and that virtually all sites wherearchaic Homo tools or fossils have been discovered were near abundant (and sometimes marine) edible shellfish. Also, the fact that some humans can successfully throw spears at ungulates, in combination with the idea that archaic Homo regularly scavenged or even hunted, recently led to the conclusion that all human features that allow throwing were developed ‘for’ throwing (Roach et al. 2013)—without considering that (part of) our throwing skills could have evolved stepwise(preadaptations) over long periods in different contexts (e.g.‘arms overhead’ movements in vertical climbing and/or surface-swimming), and that throwing-skills could at least as easily have evolved for throwing harpoons or nets when wading in shallow water.

Just because some of our features (e.g. human locomotion,language) can appear to be unique, it does not mean that comparisons with other animals cannot be made at all. What is required is to separate these features into as many individual(more elementary) components as possible (ideally these components should be independent from each other). The finer the distinctions, the more detailed reconstructions can be obtained. Since biological features are inherited largely independently of each other (Mendel’s Laws, due to chromosomalrecombination and crossing-over during meiosis), there is no reason not to use an analytic approach.

I provide two illustrations, already discussed elsewhere:bipedalism (e.g. Verhaegen & Munro 2007) and speech (e.g. Vaneechoutte et al. 2011).

Bipedalism

It is often stated that human locomotion was an adaptation to running on the open plains, which is illustratedby expressions such as ‘Savannahstan’, ‘endurance running’, ‘born to run’, ‘le singe coureur’ etc., even on the cover of the most influential scientific journals. Verhaegen et al. (2007) disproved in detail all endurance running arguments (Bramble & Lieberman 2004) that our Homo ancestors during mostof the Pleistocene were adapted to running over open plains. When we analyse human locomotion into more elementary components, the running ‘explanation’ appears to be a just-so interpretation (cherry-picking): Bramble & Lieberman (2004) interpret every locomotor trait in humans as having evolved ‘for’ running, without even considering possible wading or swimming scenarios. A comparative approach shows that, for each trait, semi-aquatic scenarios provide more parsimonious explanations (Table 4 in Verhaegen et al. 2007), and that extant human running is a secondary and conspicuouslyimperfect adaptation which evolved late in the human past, forinstance, we run maximally 32 km/hr over short and 20 km/hr over long distances, about half as fast as typical open plain mammals.

Typical for human locomotion, as opposed to chimpanzee and other primate locomotion, is not only our habitual two-leggedness (bipedalism s.s.), but also our long and flat foot soles, our very long and habitually stretched legs, our

vertical trunk, etc., which we now discuss in somewhat greaterdetail. The list overlaps, but is not exhaustive:a) Two-leggedness is seen in birds (including ostriches, flamingoes, and penguins on land), many dinosaurs, and diversemammals, including kangaroos and hopping-mice on the savanna, tarsiers, indris and gibbons upon branches, and lowland gorillas and proboscis monkeys Nasalis larvatus while wading. Largepangolins Smutsia temminckii regularly walk on their hindlimbs with horizontal (pronograde) bodies (McCormick 2007). Most mammals that frequently or occasionally wade, however, are quadrupedal, such as tapirs, hippos and many suids, wetland antelopes or ungulates that seasonally have to cross rivers: they wade into the rivers on four legs, and when the water deepens, they swim pronogradely. This suggests that human bipedal wading did not cause our bipedal locomotion. Instead, it might have resulted from earlier orthogrady, see (b) and (c).b) A more or less aligned body (with head, trunk and hindlimbsin one line) is typically seen in animals that have to swim regularly, probably as a hydrodynamic adaptation. Atelids (e.g. spider monkey) and hylobatids (e.g. gibbons), however, also frequently have more or less elongated bodies when hanging or swinging vertically from branches, and I will arguebelow that early sapiens might possibly have evolved very long and straight legs and a fully upright posture to spot prey from above in very shallow water, for instance, wading with harpoons or nets.c) Orthogrady (‘upright’ truncal erectnes, with a vertical lumbar spine) is rare in tetrapods, but is regularly seen in some arboreal species (especially tarsiers, sifakas, atelids and gibbons), meerkats on the look-out, gerunuks eating leavesfrom branches, gorillas, giant anteaters and kangaroos intimidating or threatening rivals, penguins on land, partly in herons in search for prey in shallow water, etc. Orthogradyis very atypical of running tetrapods, for instance, ostricheshave horizontal spines. It is not independent from the two previous ones, (a) and (b): walking bipedally with spine and head in the extension of the legs (as in humans and penguins on land, as opposed to ostriches) implies orthogrady.d) Very long hind-limbs in tetrapods relative to forelimb and/or trunk length are typical of frogs, kangaroos, indris and tarsiers (which are hopping, with hips and knees bent in rest, not striding), giraffes, ostriches, and especially

flamingoes and other wading-birds, to name a few typical examples. Many swimming tetrapods have short (penguins on landwalk orthogradely) or even absent legs.e) Straight legs (as opposed to bent-knees-bent-hips in rest) are seen from wading-birds to giraffes, and especially in large and heavily-built species.f) A striding gait (i.e. with alternating limbs, as opposed tohopping or jumping), bi- or quadrupedally, is more frequent inlarge tetrapods than in smaller ones, more in ground-dwelling than in arboreal species, and possibly more in slow species than in fast ones.g) Valgus knees are very atypical for cursorial mammals: most or all cursorials have the hindlimb joints in a vertical sagittal plane (Hildebrand 1974). Among anthropoid primates (reviewed in Verhaegen 1991a), knees are more valgus in 3–4-year old human children (~165°) than in adults (~170°), in smaller (~165°) than in larger (~170°) Hadar specimens (afarensis), and in orangutans and spider-monkeys (~175°) than inmost monkeys and apes (~180°).h) A medio-laterally wide trunk is typically seen in beavers and platypuses, and to a lesser degree in hippopotami, river dolphins as well as suspensory and/or brachiating primates (apes and atelids). Fossil hominids (australopiths as well as archaic Homo) typically show iliac flaring, which broadens thepelvis and hence the trunk. Iliac flaring and long femoral necks facilitate femoral abduction through the action of the gluteus medius and gluteus minimus muscles (Aiellao & Dean 1990), an adaptation which is not seen in cursorial mammals. The longer and more horizontal the femoral neck, the more effective femoral abduction is, but also the more valgus the knees have to be in order to have the hip, knee and ankle joints in one line, which might be required in a standing position for a stronger stance. If this is the case, the valgus knee might suggest an often vertical leg stance (possibly for wading) and/or a relatively very heavy body weight. (Note archaic and modern Homo have relatively larger femoral heads than apes and australopiths. This too might suggest more bipedalism (with the body weight on two instead of four legs) and/or relatively heavier body weights.)i) Relatively long and strong outer pedal digital rays, resulting in subequal toe-lengths, are seen in pinnipeds and wading and swimming birds. Cursorial mammals typically have

long and strong central digital rays (ray 3, or rays 3–4), never the first or last digital rays.j) Toe shortening together with hindfoot lengthening as seen in humans is rare or absent in nonhuman animals, cursorial as well as swimming ones. Cursorial tetrapods typically show drastic lengthening of distal hindlimb parts, especially the central digital rays (Hildebrand 1974). k) Very flat feet and full plantigrady (i.e. with the heels usually touching the ground or branch) is, for instance, seen in sealions, water opossums, and wading and swimming birds. Cursorial mammals, however, run on their toes or hooves (digiti- or unguligrady). l) Non-grasping feet (with loss of the typical primate grasping) are seen in most non-arboreal mammals. This feature is not independent from the previous ones.

These comparisons are often based on subjective resemblances, sometimes do not seem to allow clear conclusions(j, f), and are preliminary and limited, nevertheless they indicate that humans partly resemble cursorials in leg length (d), less than humans resemble arboreals (a, c, d, g), waders (d, e, i, k) and swimmers (b, h, i, k). One group of adaptations alone (either climbing, or wading, or swimming) cannot alone explain all the different elements of human (‘unique’) locomotion, which suggests that human ancestors underwent a rather complex evolution. Taken together, this seems to corroborate our scenario (based on the convergence ofother lines of evidence) that human ancestors were originally tree climbers who gradually learned to swim and dive, wade, walk and run.

Speech [Figure 1]

This exercise can be repeated with all other features in which humans differ from our closest relatives the chimpanzees, such as the human skin (fur loss, subcutaneous fat, superficial venes, sebaceous glands, sweat glands etc.), nose (poor olfaction, external nose, protruding midface, conchal cavernous tissue, paranasal sinuses etc.) and mouth (philtrum, red lips, small mouth opening, closed parabolic tooth row, masticatory reduction, incisiform canines, vaulted palate, globular tongue etc.).

Even human speech can be analysed into smaller elements. In short, we argue (Verhaegen & Munro 2004, Vaneechoutte et al. 2011): m) that musical elements of human speech (e.g. melodic, rhythmic and prosodic sounds, in different voices) originated in the territorial song of the early hominoids (>18 Ma?), comparable to the duetting of hylobatids and some other monogamous animals living in dense vegetation, such as Indri, Tarsius and Callicebus primates, and many bird species (Geissmann 2000), n) that our voluntary breathing musculature and breath-holdingoriginated in littoral frequently-diving ancestors (<2 Ma?) who had to hyperventilate just before they wanted to dive, as well as between dives, and to hold their breath at free will during dives, o) that the typically-human fine control of lips, tongue, velum and throat (now used e.g. in pronouncing labial, dental,palatal, velar etc. consonants) originally evolved for the swallowing (not impossibly also underwater) of soft, wet and/or slippery foods such as molluscs without much biting or chewing,p) and that our huge brain (possibly indispensable at some time for the development of language, e.g. for attributing an arbitrary meaning to a morpheme or ‘word’) was facilitated by the brain-specific nutrients that are abundant in aquatic foods (e.g. docosahexaenoic acid or DHA, see Crawford et al. 2002).

Laryngeal descent in adult humans has sometimes been interpreted as an adaptation for inhaling large quantities of air—for running (Geoffrey Laitman, personal communication), orto the contrary for diving in human ancestors (Morgan & Verhaegen 1986)—but both these interpretations are contradicted by comparative data. Once more, we have to analyse human laryngeal descent into smaller elements. Nishimura (2003) described two components of laryngeal descent: hominoids, as opposed to monkeys, have the larynx descended in relation to the hyoid bone, but only in Homo (andpossibly partly in chimpanzees, see Nishimura et al. 2006) is thehyoid descended in relation to the mandible, so that the larynx in adult humans (Adam’s apple) is lower in the neck than in apes, and much lower than in monkeys. Vaneechoutte et al. (2011) argued, based on comparative data, that,

schematically, the first descent was for fine and varied and/or loud phonation in territorial singing (m), whereas the second descent might have been part of a group of adaptations for suction or deglutition of littoral foods that could be swallowed whole without biting or chewing, possibly also underwater (o), such as the small mouth with fleshy lips (red mucosa), shorter mandible, short and globular tongue, vaulted and smooth palate with few transverse palatal ridges, closed parabolic tooth row with incisiform canine teeth, and myosin heavy-chain 16 (MYH16) inactivation in the masticatory musculature (Figure 1).

By using all these comparative results, in combination with the fossil and archeological data, we can try to reconstruct ancient diets and locomotions, as well as possiblescenarios of African ape and human evolution (Table 1).

Early hominoids: peri-Tethys dispersal in coastal forests? [Figure 2]

Although Mio-Pliocene hominoids were quite diverse, theirfossils typically lay in coastal, flooded or gallery forests, lagoons or wetlands (surveyed in Verhaegen et al. 2011). Monkeysdominate extant African primate communities while apes are species-poor, but in the early Miocene, when catarrhine monkeys and apes appeared, the climate was hotter and wetter than today, apes were very diverse, and monkeys were not speciose (Grossman 2013), which suggests that the flooded and mangrove forests were occupied by early hominoids rather than early cercopithecoid monkeys. The hottest and wettest forests today still have the highest densities of lowland gorillas (Blom et al. 1995), who feed parttime with erect bodies on floating vegetation in the swamp or bai today (Doran & McNeilage 1998, Nishihara 1995). In a comparable way, Miocene hominoids in flooded forests could have fed on floating herbs and aquatic herbaceous vegetation (AHV), cane, sedges or papyrus, eggs or frogs, crabs, snails, bivalves or other hard-shelled invertebrates (HSI) between reeds or mangroves etc. Such aquarboreal lifestyles (aqua=water, arbor=tree, see Figure 2) could have included climbing and hanging vertically (all exant apes), grasping branches above the water (lowland gorillas and orangutans in forest swamps), wading on two legs (lowland gorillas in forest bais) and possibly floating

vertically for AHV and/or HSI collection (Verhaegen et al. 2011).

Spending a lot of time in the swamp helps explain hominoid body enlargement (as in most mammals becoming more aquatic), tail loss (discarding a superfluous organ), verticaland centrally-placed spine (for vertical wading, hanging and possibly floating), dorsal scapulae with the arms aside (for collecting floating AHV around the body, or grasping branches above the head), and wide thorax and pelvis (as in other shallow water dwelling animals). Some paleo-anthropologists argue that medio-laterally broad thoraxes might be a suspensory or brachiating adaptation (Esteban Sarmiento, personal communication), but New World brachiators such as atelids (e.g. spider monkeys) have relatively less broad thoraxes than the about equally-large hominoid gibbons (although broader than in most monkeys). Tail loss is even more difficult to explain by pure arborealism, although the hopping indris have very short tails. Even the slow sloths as well as sloth bears and pottos still have short, not absent, tails. Tail shortening is frequently seen in primates that spend some time in the water, for instance, the simakobu Simias concolor and three species of Macaca that reached the island of Sulawesi. The uniquely-hominoid complete tail loss (incorporating the diminutive caudal vertebrae into the pelvicbottom), however, is not unexpected if they spent a lot of time vertically in forest swamps or wetlands: in an orthogradeposture, the tail has no locomotor function, it was hydrodynamically (drag) and possibly thermoregulatorily (heat loss) disadvantageous in water, and could be infected by different sorts of water-born parasites, or bitten by fishes or turtles. It is easy to imagine that an early hominoid wading or floating in a swamp gradually evolved a shorter tail, which it most of the time held between the legs, protecting the body openings and/or supporting the viscera in a habitually erect posture, so that eventually it grew into the pelvic bottom. Note that the vertically brachiating atelids have lengthened, not shortened, tails. Several ‘reasons’ can theoretically be found to explain hominoid tail reduction (e.g. body enlargement, very slow locomotion, loss of arboreality, cold ambient temperatures, higher latitudes, and need to conserve energy in homeotherms with slow metabolism), but, as far as I know, these have not been able

to cause complete tail loss in any other mammals, and, apart from body enlargement, are unlikely to have been present in hominoid ancestors. Aquatic mammals such as beavers, otters, manatees, cetaceans, water shrews etc. have kept the tail or evolved a new one, but they are pronograde swimmers (unlike orthograde hominoids), and most of them live in presumably much more open waters (requiring faster swimming speeds) than the early hominoids.

Did this aquarboreal phase begin before or after the split (~18 Ma?) with the hylobatids (the lesser apes gibbons and siamang)? The hylobatids, as all hominoids, have complete tail loss as well as broad thoraxes, habitually upright postures (for hanging from or walking over branches), and gestation times unexpectedly long for their body size, and although they weigh less than other apes, body weight reduction is not unexpected if they became acrobatic brachiators after the great/lesser ape split, so arguably theytoo had orthograde aquarboreal ancestors. Later Mio-Pliocene hominoids presumably colonized different sorts of aquarboreal niches: coastal (salt water) or inland (usually fresh water), more arboreal (vertical climbing, below-branch hanging or later brachiating) or more aquatic (wading, surface-swimming or/and floating), feeding on softer (AHV) or harder foods (HSI) in the water or the trees, etc.

In this view, the Homo-Pan last common ancestor (6 or 5 Ma?), like the australopiths and other fossil hominoids, was still aquarboreal, possibly somewhat resembling lowland gorillas today (Figure 2), but spending more time in the swamps. If the Mio-Pliocene hominids and pongids lived in the Tethys and para-Tethys coastal forests, different lineages including the australopiths might have followed the rivers inland (where fossilization might have been more likely than in coastal forests). In the australopiths, aquarborealism can explain the unexpected combination of curved hand phalanges (suggesting branch-hanging or climbing arms overhead), a vertical and centrally-placed spine (suggesting orthogrady), and flat foot soles and flat footprints suggesting wading and/or swimming (instead of digitigrady): Pliocene australopiths “existed in fairly wooded, well-watered regions”and Pleistocene robust australopiths “in similar environs and also in more open regions, but always in habitats that includewetlands” (Reed 1997) such as swamp and riverine forests,

papyrus swamps, lagoons and wetlands with sedges or cattails (e.g. Shabel 2010, Stewart 2010, Munro 2010, Verhaegen & Puech2000). The South-African australopiths seem to have been more omnivorous generally, the East-African australopiths more herbivorous. Paleo-environmental, dento-gnathic, micro-wear and isotopic data independently suggest that East-African australopiths, not unlike extant lowland gorillas in forest bais, might frequently have fed partly or largely on papyrus sedges in the swamps where their fossils lay (Puech et al. 1986, Conroy 1990, Puech 1992, van der Merwe et al. 2008, Stewart 2010,Sponheimer et al. 2013).

Homo: from diving to wading?

According to retroviral data, our direct human ancestors between about 4 and 3 Ma (at least) might not have been in Africa (Yohn et al. 2005). If early Homo populations already before ~4 Ma followed the southern Eurasian littoral forests, this could help explain that by ~1.8 Ma archaic Homo fossils were found at places as far apart as Java (Mojokerto, amid barnacles and shellfish in a river delta), Georgia (Dmanisi, amid “rich lacustrine resources” David Lordkipanidze informed me), Algeria (Aïn-Hanech, at a coastal floodplain) and Kenya (Lake Turkana, where erectus appeared at about the time stingrays did, suggesting a marine connection, possibly already ~2 Ma, see Feibel 1993, Joordens et al. 2013). A coastal dispersal (likely followed by riverine dispersals) easily explains this longitudinally and latitudinally diverse distribution ~1.8 Ma, as well as the subsequent finds of Pleistocene Homo fossils and tools as far as the Cape, Angola,England, China, Flores etc.

However, one very knowledgeable correspondent wrote, and this may reflect a general opinion among conservative paleo-anthropologists: “... we can travel inland to go from Dmanisi to Mojokerto. At least when it came to movement between Dmanisi and Africa, humans could have followed the same routesgiraffes, ostriches and hyenas did. There is no direct evidence either the animals or humans followed coastal routes.” But giraffes, ostriches and hyenas do not need as much water as humans do (Verhaegen 1987, 1991b), they are not typically found next to marine molluscs (Munro 2010), and an inland route cannot explain the Flores remains (>800 ka?), nor

the numerous human traits (fossil, anatomical, embryological, physiological, nutritional, behavioral etc.) that are easier or even exclusively to understand within a waterside dispersal. That mid-Pleistocene Homo reached Flores (>18 km overseas) is not unexpected in the littoral theory (Tobias 2011), and does not need two hardly credible assumptions, which are moreover mutually hardly compatible: that ancient people were ‘born to run’ yet built sea-worthy rafts or boats ~800 ka. As a correspondent wrote from his own experiences: “…the savannas are not the best place for two feet, the gopher holes and pits and boulders are pretty treacherous, four legs would be a distinct advantage [whereas] in the Caribbean, tourists throw coins into the ocean, and the young guys dive from the rocks to catch the coins as they fall through the water. Their ability to see underwater, to control their breath, to maneuver and dive and to nimbly and delicately grasp a tiny object falling through the warm water: how on earth does an animal have the ability to develop such subtle skills from evolving as a creature running around on the grasslands?”

Sea-levels repeatedly dropped more than one hundred metres during glacials, and on the continental shelves, vast territories (~15 % of today’s land surface)—arguably tree-poorand shellfish-rich—became available for intelligent, dexterous, tool-using, thick-enameled, coastal forest-dwellinghominoids, who could open mangrove oysters (like capuchin monkeys do) and coconuts (containing fresh water) and beach-comb for turtles and their eggs, mussels and crabs. Pleistocene Homo fossils (but no other hominoid fossils) are often found in association with marine molluscs (e.g. Munro 2010, Joordens et al. 2009, Choi & Driwantoro 2007, Gutierrez et al. 2001), and virtually all known archaic Homo sites, including those in savannas, were associated with permanent water and edible shellfish (Munro 2010). Not unexpectedly, these handy beach-combers on their diaspora to different continents and islands learned to dip and later dive, deeper and deeper, for molluscs and presumably seaweeds. We called this the continental shelf hypothesis (Verhaegen & Munro 2002).

Frequent diving biologically explains archaic Homo’s POS,the extraordinary thickness and density of many cranial and postcranial bones of most erectus-like and other archaic Homo fossils (Munro & Verhaegen 2011, Verhaegen & Munro 2011). In

tetrapods, generalized POS of both cranial and postcranial bones is exclusively seen in littoral, slow and shallow divingspecies (e.g. dugong and manatee, walrus, Kolponomos, pakicetids, Odobenocetops, and some Thalassocnus spp), and marine biologists agree POS has a hydrostatic ballast function (Taylor 2000, Madar 2007, Laurin et al. 2011). The calcium makes the skeleton heavier, but too much calcium as in osteosclerosis renders it brittle and prone to fracture, as insirenians (Leismer 2007) and the human disease of Albers-Schonberg.

Some conservative paleo-anthropologists, however, deny this and believe that archaic Homo must be an exception among heavy-boned animals and cannot have been littoral. They say that some archaic Homo fossils are found far inland, and they sometimes bring far-fetched ‘explanations’ for POS, such as head-banging (Knuckey 1992) although POS bones are in fact more brittle, and flat skull-caps are more vulnerable to blowsthan vaulted ones. We discussed these non-aquatic hypotheses for POS at length in Munro & Verhaegen (2011).

KNM-LO 45500, an erectus-like fossil found in freshwater wetlands, had thin cranial bones (Potts et al. 2004), and many heavy-boned Homo finds throughout most of the Pleistocene weredeltaic or littoral (e.g. Mojokerto ~1.8 Ma, Gibraltar ~40 ka), but other heavy-boned Homo fossils were probably found farfrom the sea. How to explain the archaic features, especially POS, in inland fossils?

There might be fossilization biases. The sea level today is lower than some interglacial Pleistocene sea levels (possibly explaining some ‘inland’ coastal finds, or marine connections at the time, see Joordens et al. 2013), and is generally much higher than during glacial periods (presumably hiding many archaic littoral fossils). The possibility should be considered that the major part of our ancestors’ semi-aquatic adaptations might have happened during the glacials, far below the sea level today, and that during warmer periods they more often followed the rivers inland, but we do not knowhow fast POS can appear or disappear evolutionarily when moving from salt to fresh water or vice versa (phylogenetic inertia). Some archaic populations could have been littoral during certain seasons (explaining their POS), and during other seasons trekked inland along the rivers (e.g. following

anadromous fish), where their fossilization chances might havebeen higher.

Although the fully marine sea otters use stone tools, thelate-Pleistocene composite tools suggest their manufacturers spent at least part of their time outside the water, but what about the early Pleistocene? Although many traditional paleo-anthropologists (e.g. Will et al. 2013) assume without argumentation that the Middle Stone Age shellfish collection in South Africa was a late-Pleistocene innovation (~130 ka), all available data concur to suggest that this ‘coastal colonization’ was only a left-over of a much more pronounced littoral phase earlier in the Pleistocene, or possibly a recent re-colonization of the coasts. In any case, although there are still numerous uncertainties, there is no reason whyPOS in archaic Homo should be explained in a unique way, different from POS in other mammals. [Table 2]

Regular slow and shallow littoral diving parsimoniously explains many other ‘odd’ features seen in Homo—fossil (e.g. ear exostoses, projecting nasals and mid-face, low and long braincases with pronounced frontal ridges, flattened femora, huge brain size) and living (e.g. fur loss, SC fat, head–spine–legs in one line, and in human newborns vernix caseosa and reniculi). The fossil Homo traits that are more typical ofdiving species (e.g. POS, platycephaly, platymeria, ear exostoses, external nose) apparently did not appear before thePleistocene epoch: arguably, our ancestors’ most-littoral phase began with the Ice Ages, when Homo during glacials couldcolonize the drying continental shelves (Table 2). It is to beexpected that these dextrous primates intensified their handedness (like clawless otters Aonyx capensis, who seek prey inreedbeds and under rocks) and stone tool use (in parellel withsea-otters Enhydra lutris in kelp beds), and that this superior handedness, together with the growing brain, led to the beginning of technological skills (stone and later wooden tooluse and manufacture) which preadapted these littoral creaturesto following the rivers inland. The abundant brain-specific nutrients in aquatic foods (DHA, iodine etc.) presumably facilitated brain growth. (In Homo sapiens, the ‘poorer’ post-aquatic diet might have required a longer youth to grow the same brain size.) From the coasts and estuaries, different Homo populations gradually (presumably seasonally, and later more permanently) ventured inland along rivers, and many late-

Pleistocene Homo populations might have been more freshwaterside than littoral. Neanderthals and pre-neanderthals generally had less POS but larger paranasal sinuses than erectus (Table 2), their bones had been washed intothe caves according to the discoverers of the Neanderthal fossils of Engis and Neanderthal (Huxley 1863), their fossils often lay just above those of beavers (Castor as well as Trogontherium), their dental calculus sometimes contained tracesof waterlilies (Henry et al. 2011), and some of their tools bore traces of cattails (Paunovic & Smith 2002, Shreeve 1996), so perhaps (if their C and N isotopic values are to be explained by meat-eating, as paleo-anthropologists traditionally propose) they hunted or scavenged ungulates in shallow water, reedbeds, mud or amid water(side) vegetation in beaver ponds or oxbow lakes, whereas at the coast they still collected shellfish and butchered whales and seals (e.g. at Gibraltar, see Stringer et al. 2008).

Homo sapiens’ gracile skulls (with higher and shorter vaults, and reduced POS) appeared in the fossil record at Omo and Herto in East Africa after 0.2 Ma, and humans developed longer tibias and presumably straighter legs, they got shorterand less horizontal femoral necks, a narrower pelvis, and relatively long and more vertical spinous processes of the mid-thoracal vertebrae (stabilising the orthograde spine). This suggests our ancestors (~0.2 Ma?) abandoned regular diving, but more frequently waded upright and beach-combed on two legs, possibly to spot edible foods in very shallow water such as cray- and shellfish and/or to spear fishes from above or perhaps to use nets. The remarkably high frequency of varicose veins on the hindlimbs but not arms in humans (a veryvariable trait) suggests that this wading-adaptation (superficial veins are ideal to discharge superfluous body heat to the surrounding water, and the water pressure prevented varices) is disappearing. Not impossibly, these modern-looking people might usually have slept in some primitive sort of floating reed huts (far more primitive than what is seen in Marsh Arabs) above the water (safer from predators), used reed boats or dugouts, and possibly nets, andspent more and more time outside the water, walking on land plantigradely as they did in very shallow water. Maps of humanpopulation densities show that, although we have become fully terrestrial today, we are still a waterside species, and

perhaps half of human dietary calories still come from the water: fish, shell- and crayfish, rice, aquaculture, etc.

The nowadays popular ideas about Pleistocene human ancestors running in open plains (‘endurance running’, ‘doggedpursuit of swifter animals’, ‘born to run’, ‘le singe coureur’, ‘Savannahstan’) are among the worst scientific hypotheses ever proposed. The susprising frequency and diversity of foot problems (e.g. hammertoes, hallux valgus andbunions, ingrown nails, heelspurs, athlete’s feet, corns and calluses—some of these due to wearing shoes) and the need to protect our feet with shoes prove that human feet are not madein the first place for running. Moreover, humans are physiologically ill-adapted to dry open milieus: “We have a water- and sodium-wasting cooling system of abundant sweat glands, totally unfit for a dry environment. Our maximal urineconcentration is much too low for a savanna-dwelling mammal. We need much more water than other primates, and have to drinkmore often than savanna inhabitants, yet we cannot drink largequantities at a time” (Verhaegen 1987). This does not imply tosay that human ancestors or relatives never lived on savannas,only that if they did, it was at the wetlands and rivers there. Apparently we evolved running—only lately, and only about half as fast as equids, bovids, felids or canids, and even slower than arboreal primates—in spite of our broad build, short toes and plantigrade feet, profuse sweating, and large subcutaneous fat tissues (a burden of ~10 kg in most people). Of course, healthy adult men can sometimes outrun ungulates (the usual ‘argument’ of conventional paleo-anthropologists) and provide a limited part of the calories for the group, but this dogged pursuit is largely confined to a few inland populations in East Africa today, is derived and probably veryrecent (less than a few thousands of years), and it requires arather specialized technology with water bags, weapons and poisons. Quadrupedal chimps can hunt colobus monkeys and even eat them raw, but archaic Homo with their heavy bones (POS), very broad pelves and valgus knees, shorter legs and flat feetwere much too slow on land. Humans have a remarkably poor olfaction (Gilad et al. 2003) and low muscularity, which make regular scavenging, and a fortiori hunting, unlikely. In fact,our small mouth, spatulated canines and closed tooth-row, short tongue and smoothly vaulted palate are ill-designed for meat-eating, but ideal for consumption of slippery foods (and

preadaptive to the evolution of human speech).

Conclusions

Many scientific as well as popular publications on the so-called aquatic ape theory or aquatic ape hypothesis give incorrect impressions of how, when and where our semi-aquatic ancestors could have evolved. This paper provides arguments from diversebiological subdisciplines for the following three hypotheses, which to conservative anthropologists might seem unexpected atfirst sight, but are based on what is known from other animals: the comparative evidence.

(1) The aquarboreal theory of Mio-Pliocene hominoids suggeststhat our Miocene and Pliocene more apelike ancestors and relatives, including the australopiths, led an aquarboreal life, living in wet forests such as flooded, mangrove or swampforests and later in more open wetlands, and fed on hard-shelled and other plant and animal foods at the water surface and the waterside as well as in the trees.

(2) The littoral theory of Pleistocene Homo (AAH sensu stricto) suggests that early-Pleistocene archaic Homo populations dispersed along the coasts, where they reduced climbing adaptations, but frequently dived and used stone and other tools for feeding on shallow-water and water-side foods including shellfish.

(3) The wading hypothesis of early Homo sapiens suggests that, later in the Pleistocene, Homo populations gradually ventured inland along the rivers, reduced diving skills, and frequently waded with very long and stretched legs and fully upright body to spot prey in very shallow water and used complex tools to collect different sorts of aquatic and waterside foods.

Acknowledgements – I wish to thank Charles Smith, Greg Jones, Johnny Weyand, Stephen Munro, Pierre-françois Puech, Mario Vaneechoutte, Bert Chan Wang Chak, Roger Crinion and Daud Deden for corrections, help and ideas.

Figure 1 – Mid-sagittal view of mouth and throat of chimpanzeeand human (schematically). After Laitman (1977), Aiello& Dean (1990), and Vaneechoutte et al. (2011).

Figure 2 – Gorilla in forest swamp, feeding on floating vegetation (AHV).The silverback gorilla “soaks in a swamp for hours, methodically stripping and rinsing dirt from herb roots beforemunching.” Note its laryngeal airsac (covered with naked skin, visible inthe neck) is partly inflated. Photo by Ian Nichols, National Geographic Societyhttp://blog.al.com/spotnews/2010/09/malaria_jumped_from_gorillas_t.html

References

Aiello L & Dean C 1990 An Introduction to Human Evolutionary Anatomy, Academic Press London

Bender R 1999 Die evolutionsbiologische Grundlage des menschlichen Schwimmens, Tauchens und Watens: Konvergenzforschung in den Terrestrisierungshypothesen und in der Aquatic Ape Theory, DiplomarbeitTurn- und Sportlehrer II, Institut für Sport und Sportwissenschaft, Universität Bern

Blom A, Almaši A, Heitkönig IMA, Kpanou JB & Prins HHT 1995 A survey of the apes in the Dzanga-Ndoki National Park, Central African Republic: a comparison between the censusand survey methods of estimating the gorilla (Gorilla gorilla gorilla) and chimpanzee (Pan troglodytes) nest group density, African Journal of Ecology 39:98-105

Breuer T, Ndoundou-Hockemba M & Fishlock V 2005. First observation of tool use in wild gorillas, PLoS Biology 3(11):e380

Bocherens H, Baryshnikov G & Van Neer W 2013 Were bears or lions involved in salmon accumulation in the Middle Palaeolithic of the Caucasus? An isotopic investigation in Kudaro 3 cave, Quaternary International in press

Bramble DM & Lieberman DE 2004 Endurance running and the evolution of Homo, Nature 432:345-352

Choi K & Driwantoro D 2007 Shell tool use by early members of Homo erectus in Sangiran, central Java, Indonesia: Cut mark evidence, Journal of Archaeological Science 34:48-58

Conroy GC 1990 Primate Evolution, Norton & Company New YorkCrawford MA, Wang Y, Cunnane SC, Parkington JE, Broadhurst CL

& Schmidt WF 2002 Brain-specific lipids from marine, lacustrine, or terrestrial food resources: Potential impact on early African Homo sapiens, Comparative Biochemistry 131:653-673

Curtis A, Lai G & van Valkenburgh B 2012 Frontal Sinus Morphology in Arctoid Carnivorans, Society for Integrative & Comparative Biology 2012 Annual Meeting abstract P1.94

Doran DM & McNeilage A 1998 Gorilla ecology and behavior, Evolutionary Anthropology 6:120-130

Farke AA 2010 Evolution and functional morphology of the frontal sinuses in Bovidae (Mammalia: Artiodactyla), and implications for the evolution of cranial pneumaticity, Zoological Journal of the Linnean Society 159:988-1014

Feibel CS 1993 Freshwater stingrays from the Plio-Pleistocene of the Turkana Basin, Kenya and Ethiopia, Lethaia 26:359-366

Fernandes M 1991 Tool use and predation of oysters (Crassotrea rhizophorae) by the tufted capuchin, Cebus apella apella, in brackish water mangrove swamps, Primates 32:529-531

Filler AG 2007 The Upright Ape, Career Press Franklin Lakes New Jersey

Geissmann T 2000 Gibbon songs and human music from an evolutionary perspective :103-123 in Wallin NL, Merker B & Brown S eds. The Origins of Music, MIT Press Cambridge Massachusetts

Gilad Y, Man O, Pääbo S & Lancet D 2003 Human specific loss ofolfactory receptor genes, Proceedings of the National Academy of Sciences USA 100:3324-7

Gould SJ 1977 Ontogeny and Phylogeny, Harvard University PressGutierrez M, Guerin C, Lena M & Piedade da Jesus M 2001

Exploitation d’un grand cétacé au Paléolithique ancien: Le site de Dungo V à Baia Farta (Benguela, Angola), Comptes Rendus Academical Sciences 332:357-362

Hardy BL & Moncel M-H 2011 Neanderthal use of fish, mammals, birds, starchy plants and wood 125-250,000 years ago, PLoS ONE 6(8):e23768 doi

Henry AG, Brooks AS & Piperno DR 2011 Microfossils in calculusdemonstrate consumption of plants and cooked foods in Neanderthal diets (Shanidar III, Iraq; Spy I and II, Belgium), Proceedings of the National Academy of Sciences USA 108:486-491

Hildebrand M 1974 Analysis of Vertebrate Structure, John Wiley & sons New York

Huxley TH 1863 Man’s Place in Nature, Appleton & Company New YorkJoordens JC, Wesselingh FP, de Vos J, Vonhof HB & Kroon D 2009

Relevance of aquatic environments for hominins: A case study from Trinil (Java, Indonesia), Journal of Human Evolution57:656-671

Improved age control on early Homo fossils from the upper Burgi Member atKoobi Fora, Kenya2013 Joordens JC, Dupont-Nivet G, Feibel CS, Spoor F, Sier MJ, van der Lubbe JHJL,Kellberg Nielsen T, Knul MV, Davies GR & Vonhof HB 2013, Journal of Human Evolution in press

Knuckey G 1992 Patterns of fracture upon Aboriginal crania from the recent past: 47-58 in Bruce NW ed. Living with

civilization, Centre for Human Biology, University Western Australia Perth

Kuliukas AV 2011 Langdon's Critique of the Aquatic Ape Hypothesis: Its Final Refutation, or Just Another Misunderstanding? :213-226 in Vaneechoutte M, Kuliukas A & Verhaegen M eds. Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham Science Publications eBook

Laden G 2013 blog guest post Verhaegen M Common misconceptions andunproven assumptions about the aquatic ape theory http://scienceblogs.com/gregladen/2013/01/30/common-misconceptions-and-unproven-assumptions-about-the-aquatic-ape-theory/ (google: Laden Verhaegen)

Laitman JT 1977 The Ontogenetic and Phylogenetic Development of the Upper Respiratory System and Basicranium in Man, PhD dissertation,Yale University

LaLumiere LP 1981 The evolution of human bipedalism: where it happened – a new hypothesis, Philosophical Transactions of the RoyalSociety of Lonon .B 292:103-7

Langdon JH 1997 Umbrella hypotheses and parsimony in human evolution: A critique of the aquatic ape hypothesis, Journal of Human Evolution 33:479-494

Laurin M, Canoville A & Germain D 2011 Bone microanatomy and lifestyle: A descriptive approach, Comptes Rendus Palévol 10:381-402

Leismer JM 2007 Numerical Investigation of the Fracture Properties of Manatee Rib Bone using Experimentally Determined Anisotropic Elastic Constants, PhD dissertation University of Florida

MacLatchy L, Gebo D, Kityo R & Pilbeam D 2000 Postcranial functional morphology of Morotopithecus bishopi, with implications for the evolution of modern ape locomotion, Journal of Human Evolution 39:159-183

Madar SI 2007 The postcranial skeleton of early Eocene pakicetid cetaceans, Journal of Paleontology 81:176-200

Margvelashvili A, Zollikofer CPE, Lordkipanidze D, Timo Peltomäki T & Ponce de León MC 2013 Tooth wear and dentoalveolar remodeling are key factors of morphologicalvariation in the Dmanisi mandibles, Proceedings of the National Academy of Sciences USA in press  doi 10.1073/pnas.1316052110

Martin LB, Olejniczak AJ & Maas MC 2003 Enamel thickness and microstructure in pitheciin primates, with comments on dietary adaptations of the middle Miocene hominoid

Kenyapithecus, Journal of Human Evolution 45:351-367McCormick C 2007 Unexpected Bipedalism

http://cameronmccormick.blogspot.be/2007/11/unexpected-bipedalism.html

Morgan E 1990 The Scars of Evolution, Souvenir LondonMorgan E & Verhaegen M 1986 In the beginning was the water, New

Scientist 1498:62-63Munro S 2010 Molluscs as Ecological Indicators in Palaeoanthropological

Contexts, PhD thesis Australian National University Canberra

Munro S & Verhaegen M 2011 Pachyosteosclerosis in archaic Homo:Heavy skulls for diving, heavy legs for wading? :82-105 in Vaneechoutte M, Kuliukas A & Verhaegen M eds. Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham SciencePublications eBook

Nishihara T 1995 Feeding ecology of western lowland gorillas in the Nouabalé-Ndoki National Park, Congo, Primates 36:151-68

Nishimura T 2003 Comparative morphology of the hyo-laryngeal complex in anthropoids: Two steps in the evolution of thedescent of the larynx, Primates 44:41-49

Nishimura T 2006 Descent of the larynx in chimpanzees: Mosaic and multiple-step evolution of the foundations for human speech :75-95 in Matsuzawa T, Tomonaga M & Tanaka M eds. Cognitive Development in Chimpanzees, Springer Tokyo

Nishimura T 2008 Understanding the dynamics of primate vocalization and its implications for the evolution of human speech :111-130 in Masataka N ed. The Origin of Language, Springer Tokyo

Nishimura T, Mikami A, Suzuki J & Matsuzawa T 2003 Descent of the larynx in chimpanzee infants, Proceedings of the National Academy of Sciences USA 100: 6930-3

Nishimura T, Mikami A, Suzuki J & Matsuzawa T 2006 Descent of the hyoid in chimpanzees: Evolution of face flattening and speech, Journal of Human Evolution 51:244-254

Nishimura T, Oishi T, Suzuki J, Matsuda K & Takahash T 2008 Development of the supralaryngeal vocal tract in Japanesemacaques: Implications for the evolution of the descent of the larynx, American Journal of Physycal Anthropology 135:182-194

Odent M 2011 Obstetrical implications of the aquatic ape hypothesis :156-163 in Vaneechoutte M et al. eds. Was Man

More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham SciencePublications eBook

Paunovic M & Smith FH 2002 Taphonomy of lower vertebrates fromVindija Cave (Croatia): Delicacy on the Neandertal table or animal prey? Journal of Human Evolution 42:A27

Shreeve J 1996 The Neandertal enigma: Solving the mystery of modern human origins, Viking London

Pérez-Pérez A, Bermúdez De Castro JM & Arsuaga JL 1999 Nonocclusal dental microwear analysis of 300,000-year-oldHomo heidelbergensis teeth from Sima de los Huesos (Sierra deAtapuerca, Spain), American Journal of Physical Anthropology 108:433-457

Potts R, Behrensmeyer AK, Deino A, Ditchfield P & Clark J 2004Small mid-Pleistocene hominin associated with East African Acheulean technology, Science 305:75-78

Puech P-F 1983 Tooth wear, diet, and the artifacts of Java Man, Current Anthropology 24:381-2

Puech P-F 1992 Microwear studies of early African hominid teeth, Scanning Microscopy 6:1083-8

Reed KE 1997 Early hominid evolution and ecological change through the African Plio-Pleistocene, Journal of Human Evolution 32:289-322

Roach NT, Venkadesan M, Rainbow MJ & Lieberman DE 2013 Elasticenergy storage in the shoulder and the evolution of high-speed throwing in Homo, Nature 498:483-6

Roede M, Wind J, Patrick J & Reynolds V eds. The Aquatic Ape: Fact orFiction? Souvenir London

Schagatay E 2011 Human breath-hold diving ability suggests a selective pressure for diving during human evolution:120-173 in Vaneechoutte M, Kuliukas A & Verhaegen M eds.Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham Science Publications eBook

Schultz AH 1969 The Life of Primates, Universe Books New YorkShabel AB 2010 Brain size in carnivoran mammals that forage at

the land–water ecotone, with implications for robust australopithecine paleobiology :173-188 in Cunnane SC & Stewart KM eds. Human Brain Evolution: The Influence of Freshwater andMarine Food Resources, John Wiley & Sons New Jersey

Stringer CB, Finlayson JC, Barton RNE, Fernández-Jalvo Y, Cáceres I, Sabin RC, Rhodes EJ, Currant AP, Rodríguez-Vidal J, Giles-Pacheco F & Riquelme-Cantal JA 2008

Neanderthal exploitation of marine mammals in Gibraltar, Proceedings of the National Academy of Sciences USA 105:14319-24

Stewart KM 2010 The case for exploitation of wetlands environments and foods by pre-sapiens hominins :137-173 in Cunnane SC & Stewart KM eds. Human Brain Evolution: The Influence of Freshwater and Marine Food Resources, John Wiley & Sons New Jersey

Taylor MA 2000 Functional significance of bone ballast in the evolution of buoyancy controls trategies by aquatic tetrapods, Historical Biology 14:15-31

Tobias PV 2011 Revisiting water and hominin evolution :3-15 inVaneechoutte M, Kuliukas A & Verhaegen M eds. Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham Science Publications eBook

van der Merwe NJ, Masao FT & Bamford MK 2008 Isotopic evidencefor contrasting diets of early hominins Homo habilis and Australopithecus boisei of Tanzania, South African Journal of Science 104:53-55

Vaneechoutte M, Munro S & Verhaegen M 2011 Seafood, diving, song and speech :181-189 in Vaneechoutte M, Kuliukas A & Verhaegen M eds. Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham Science Publications eBook

Vaneechoutte M, Munro S & Verhaegen M 2012 Reply to John Langdon’s review of the eBook: Was Man more aquatic in the past? Fifty years after Alister Hardy, Waterside Hypotheses of Human Evolution, Mario Vaneechoutte, Algis Kuliukas, Marc Verhaegen (Eds.). Bentham eBooks (2011). 244 pp., eISBN: 9781608052448, HOMO Journal of Comparative Human Biology 63:496-503

Verhaegen M 1987 Origin of hominid bipedalism, Nature 325:305-6 Verhaegen M 1991a Aquatic features in fossil hominids? :75-112

in Roede M, Wind J, Patrick J & Reynolds V eds. The Aquatic Ape: Fact or Fiction? Souvenir London

Verhaegen M 1991b Human regulation of body temperature and water balance :182-192 in M Roede, J Wind, J Patrick, V Reynolds eds. The Aquatic Ape: Fact or Fiction? Souvenir London

Verhaegen M 1993 Aquatic versus savanna: comparative and paleo-environmental evidence, Nutrition & Health 9:165-191

Verhaegen M 1996 Morphological distance between australopithecine, human and ape skulls, Human Evolution 11:35-41

Verhaegen M & Munro S 2002 The continental shelf hypothesis,

Nutrition & Health 16:25-27Verhaegen M, Puech P-F & Munro S 2002 Aquarboreal ancestors?

Trends in Ecology & Evolution 17:212-7Verhaegen M & Munro S 2007 New directions in

palaeoanthropology :1-4 in Muñoz SI ed. Ecology Research Progress. Nova New York

Verhaegen M & Munro S 2011 Pachyosteosclerosis suggests archaic Homo frequently collected sessile littoral foods,HOMO Journal of Comparative Human Biology 62:237-247

Verhaegen M, Munro S, Vaneechoutte M, Bender R & Oser N 2007 The original econiche of the genus Homo: Open plain or waterside? :155-186 in Muñoz SI ed. Ecology Research Progress. Nova New York (google: Homo econiche)

Verhaegen M, Munro S, Puech P-F & Vaneechoutte M 2011 Early hominoids: Orthograde aquarboreals in flooded forests? :67-81 in Vaneechoutte M, Kuliukas A & VerhaegenM eds. Was Man More Aquatic in the Past? Fifty Years after Alister Hardy, Bentham Science Publications eBook

Verhaegen M & Puech P-F 2000 Hominid lifestyle and diet reconsidered: Paleo-environmental and comparative data, Human Evolution 15:175-186

Walker A & Leakey R 1993 The Nariokotome Homo erectus skeleton, Harvard University Press

Walter RC, Buffler RT, Bruggemann JH, Guillaume MMM, Berhe SM, Negassi B, Libseka Y, Cheng H, Edwards RL, von Cosel R, Néraudeau D & Gagnon M 2000 Early human occupation of the Red Sea coast of Eritrea during the last interglacial, Nature 405:65-69

Wescott R 1995 Aquaticism and quantalism: two overlapping theories of evolutionay discontinuity, ReVision 18:40-43

Will M, JE Parkington, AW Kandel & NJ Conard 2013 Coastal adaptations and the Middle Stone Age lithic assemblages from Hoedjiespunt 1 in the Western Cape, South Africa, Journal of Human Evolution 64:518-537

Williams MF 2006. Morphological evidence of marine adaptationsin human kidneys, Medical Hypotheses 66:247-257

Yohn CT, Jiang Z, McGrath SD, Hayden KE, Khaitovich P, JohnsonME, Eichler MY, McPherson JD, Shaying Zhao S, Pääbo S & Eichler EE 2005 Lineage-specific expansions of retroviralinsertions within the genomes of African great apes but not humans and orangutans, PLoS Biol 3(4):e110

MORPHOLOGICAL DISTANCE BETWEEN AUSTRALOPITHECINE, HUMAN AND APE SKULLS

Human Evolution 11: 35-41, 1996

This paper attempts to quantify the morphological difference between fossil and living species of hominoids. The comparisonis based upon a balanced list of craniodental characters corrected for size (Wood & Chamberlain, 1986). The conclusionsare: craniodentally the australopithecine species are a uniqueand rather uniform group, much nearer to the great apes than to humans; overall, their skull and dentition do not resemble the human more than the chimpanzee’s do.

Key words: human evolution, hominids, apes, skull, Australopithecus, Homo erectus, chimpanzee, gorilla

Introduction

The australopithecine species are commonly considered to be “hominids” beeause they lack some of the features that characterize the living apes, and display certain humanlike characters. Yet it has often been argued that their humanlike characters might be primitive - and indeed many of these characters are found in premature African apes - and that the australopiths should not be included in the evolutionary branch towards humans, but instead are a unique group of apes or might even be closer phylogenetically to the African apes than to humans (e.g., Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Oxnard, 1984; Hasegawa et al., 1985; Edelstein, 1987; Verhaegen, 1990; 1994).

The aim of this paper is to objectivate morphological resemblances of australopithecine species with living hominoidspecies. (To establish phylogenetic relationships, biomolecular comparisons of nucleic acids or proteins are preferable to morphological comparisons, but it does not seem very probable that extraction of enough DNA or protein from fossil bone willever become possible.)

Methods

I have used the comparative data of Wood and Chamberlain (1986) because: Their data are likely to be comparable since they stem from

the same source. They use a balanced list of 39 characters, i.e., "selected to

provide a relatively comprehensive coverage of the head" without much functional or morphological overlapping. The 39 characters stem from: cranial vault and endocranium (11 V), face (7 F), palate and maxilla plus dentition (7 P), cranial base (5 B), and mandible plus dentition (9 M).

Wood and Chamberlain do not use the "raw" metrical data, butratios, which "help to reduce, if not actually eliminate, differences due to absolute size".

Postcranial data (more scarce and difficult to attribute to a certain species) are not included in their list.

Since the data for the 39 characters were not available for all species, I selected two (overlapping) Character Groups(only characters V9 and B5 were not used at all):

I. one of 32 characters (82 %) that were available for 8 species: Hylobates, Pongo, Pan troglodytes, Gorilla, A. africanus, A. boisei, H.erectus and H. sapiens (characters V1-8,10- 11, F1-7, P1-3,5-6, B1,4, M-6,8-9);

II. one of 27 characters (69 %) that were available for 7 species: Pongo, Gorilla, Pan troglodytes, Homo sapiens, Australopithecus africanus, A. robustus and A. boisei (characters V1,7-8, F1-7, P1-7, B1-3, M1,4-9). This second Group was added since it included datafrom a third australopithecine species, A. robustus.

The data for Pan paniscus, A. afarensis and H. neanderthalensis could not be used, since they were available for too few characters.The data for “H. habilis” (which included ER-1470, ER-1813, and OH material) were not used since they might belong to more than one species.

A simple method measured the relative overall craniodentaldistance between the different (fossil as well as living) hominoid species without considering any of these species as an outgroup a priori:

Each character had to have equal weight. For each species and each character, the sum of the differences with the same character in the other species was given an arbitrary weight of 1000, i.e., each of the differences with the other species was divided by the sum of these differences and multiplied by 1000. Tables Ia and IIa show the mean results of all (32 or 27)

characters for all (8 or 7) species. These results, of course,are not directly proportional to the morphological distance, but indicate that the difference between species A and B is larger or smaller than that between A and C. As an example, Figure 1 shows the calculation of the results for Character Group II (and more in particular for A. boisei).

These results in Tables Ia and IIa for each species were made more comparable with those for the other species in the same Character Group (e.g., for interpreting the diagrams, seebelow) by multiplying them by a correction factor consisting of the sum (/1000) of the differences of the other species with that species (see Figure l). This yielded Tables Ib and IIb. (This correction exaggerates the results of the most aberrant species (e.g., H. sapiens in Table II), but does not change the order of differences.)

For illustrating which one of the living species resembled afossil species most, the diagrams of Figure 2 were constructed. Since all results are relative, the diagrams could be made clearer by equalling one of the species to zero. In this case,Pongo, which was nearest to the mean species, was taken as the reference (this choice, of course, does not influence the conclusions): in Tables Ib and IIb, the results comparing Hylobates, Gorilla, P. troglodytes and H. sapiens with the fossils were subtracted from the results of Pongo, so that a positive result(above the x-axis) means that the fossil resembles the living species more than it resembles Pongo craniodentally; a negative(below the x-axis), less.

(For comparing the diagrams between both Character Groups,the results for Group I could have been multiplied by 5198/3954, which is the quotient of the sums of the differences within Group II and I using only the species common to both Groups (i.e., omitting the results for H. erectus, A. robustus and Hylobates). This second correction factor (even less than the first) would not have influenced the conclusions.)

Discussion

The tables show that morphologically the great hominoids form three clusters: Homo, the australopithecines, and the great apes.

1) The human skull is unique and differs from that of the great apes even more than the gibbon does. Homo is about equidistant from australopithecines and chimpanzees (though evolutionarily he is probably closer to A. africanus than to Pan, only because A. africanus lived almost three million years nearer to the common ancestor). H. erectus in Group I seems to be on the way to H. sapiens. He is about equidistant from H. sapiens, P. troglodytes and A. africanus, but differs from the australopithecineseven slightly more than Pongo does.

2) The australopithecine skulls resemble each other more than they resemble the apes (even the African apes) and certainly humans; A. robustus stands somewhere between A. africanus and A. boisei, but nearer to A. boisei. In comparison with the living species(Figure 2): A. africanus in both Character Groups is closest to the chimp,

and closer to chimpanzees, gorillas and orangutans than to humans (and to gibbons in Group I);

A. robustus in Group II also is morphologically closest to the chimpanzee, and much closer to chimp, gorilla and orang thanto humans (gibbons were not included in this comparison);

A. boisei in both Groups is closer to G. gorilla than to Pan troglodytes (in contrast with the South African fossils), and very different from Homo, somewhat more different than A. africanus is from Homo.

A. boisei (who lived later) more than A. africanus (who lived earlier)resembles the living African apes compared with humans or orangs or gibbons (Figure 2). In Diagram II of Figure 2, A. robustus also resembles the African apes more than A. africanus doesin comparison with humans. This indicates that the australopithecines (from graciles to robusts) were evolving inthe African ape direction – whether in parallel with the apes (see Ferguson, 1989) or not (Verhaegen, 1994).

3) The great apes (even including Pongo) resemble each other even more than H. erectus and H. sapiens in Group I resemble each other, in spite of the evolutionary distance between the apes (cf. the African apes and Pongo split perhaps ten times earlierthan H. erectus and H. sapiens). They resemble each other more than A.boisei resembles A. africanus. This points to a remarkable degree ofconservatism and/or of parallelism in cranial evolution of these three great ape species (and to a remarkably fast

evolution of Pleistocene Homo). Yet, chimps, somewhat more thangorillas, resemble Homo more than orangs and certainly gibbons do (in accordance with the biochemical resemblances).

All this implies that the craniodental evidence provides no ground for the anthropological custom of using the living African hominoids as an outgroup when comparing australopithecines with humans or when reconstructing hominoidphylogenetic trees: if the australopithecine species are considered to be hominid, the great apes and certainly the African apes should also be called hominid, since they resemble the australopiths more than humans do, and they do not differ from humans more than the australopiths do (Figure 3).

The australopithecines are often assumed to be hominids onthe basis of their postcranial features (not included in Wood and Chamberlain’s list), but many authors argue that locomotorically australopithecines differed more from humans than from the African apes (for discussion and references, seeespecially Oxnard, 1984; and Verhaegen, 1990, 1993, 1994). In this respect too, the australopithecines could have had uniqueadaptations (Oxnard, 1984) for an environment or lifestyle that no longer exist. (For instance, there is dental as well as paleo-environmental evidence that the later australopiths fed partly on bamboo or reed or papyrus (Du Brul, 1977; F. E. Grine, pers. comm.; Puech, 1992, and pers. comm.; Verhaegen, 1992), possibly wading bipedally in the shallow waters where most fossils are discovered (discussion in Verhaegen, 1993).)

Although Gorilla and Pan skulls resemble each other morphologically (Tables Ib and IIb), both species differ biochemically (in DNA and proteins) even more than Homo and Pan (e.g., Horai et al., 1995). Since synchronous parallel evolution in related species in response to a climatic change appears to be the rule (e.g., White and Harris, 1977; Seger, 1987, Gibbs andGrant, 1987; Bown et al., 1994; theoretical considerations in Silson, 1988), some African ape features that are usually assumed to be primitive might instead have developed in parallel in gorillas and in chimpanzees. The possibility should even be considered that, if australopiths are more closely related to the African apes than to humans (be it, of course, on morphological grounds, see Figure 3), some australopithecines might evolutionarily be closer to

chimpanzees and others to gorillas (discussion in Verhaegen, 1994).

Conclusions

This comparison of 37 craniodental characters of fossil and living apes and humans yields no indication that any of the australopithecine species has evolved in the human direction. South African australopithecine skulls are morphologically closest to the chimpanzee among the living hominoids, and A. boisei is closest to the gorilla among the living hominoids. Human craniodental evolution appears to havebeen very fast the last one or two million years.

These conclusions could be verified and extended when more(including postcranial) data on living (e.g., P. paniscus) and fossil hominoids (adult and premature) will become available.

Tables

Craniodental differences between hominoid species. Tables Ia and Ib based on 32 characters (8 species).Tables IIa and IIb based on 27 characters (7 species). Tables Ib and IIb corrected (see text and Figure 1).

References

Bown T. M., Holroyd P. A. and Rose K.D., 1994. Mammal extinctions, body size, and paleotemperature. Proceedings of the National Academy of Sciences USA, 91: 10403-6.

Du Brul, E. L., 1977. Early hominid feeding mechanisms. American Journal of Physical Anthropology, 47: 305-320.

Edelstein S. J., 1987. An alternative paradigm for hominoid evolution. Human Evolution, 2: 169-174.

Ferguson W.W., 1989. A new species of the genus Australopithecus Primates-Hominidae from the Plio/Pleistocene deposits Westof Lake Turkana in Kenya. Primates, 30: 223-232.

Gibbs, H. L. and Grant P. R., 1987. Oscillating selection on Darwin's finches. Nature, 327: 511-513.

Goodman M., 1982. Biomolecular evidence on human origins from the standpoint of Darwinian theory. Human Biology, 54: 247-264.

Gribbin J. and Cherfas J., 1983. The Monkey Puzzle. London: Triad. Hasegawa M., Kishino H. and Yano T., 1985. Dating of the

human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 2: 160-174.

Horai S., Hayasaka K., Kondo R., Tsugane K. and Takahata N., 1995. Recent African origin of modern humans revealed by complete sequences of hominoid mitochondrial DNAS. Proceedings of the National Academy of Sciences USA, 92: 532-536.

Kleindienst M.R., 1975. On new perspectives on ape and human evolution. Current Anthropology, 16: 644- 646.

Oxnard C. E., 1984. The Order of Man. New Haven: Yale University Press.

Puech P.-F., 1992. Microwear studies of early African hominid teeth. Scanning Microscopy, 6: 1083-1088.

Seger J., 1987. El Nino and Darwin's finches. Nature, 327: 461.Silson R.G., 1988. Additive Genes in Evolution and Selection. Tring:

Greenfield Publications. Verhaegen M., 1990. African ape ancestry. Human Evolution, 5: 295-

297. Verhaegen M., 1992. Did robust australopithecines partly feed

on hard parts of Gramineae? Human Evolution, 7: 63-64. Verhaegen M., 1993. Aquatic versus savanna: comparative and

paleo-environmental evidence. Nutrition and Health, 9: 165-191.Verhaegen M., 1994. Australopithecines: ancestors of the

African apes? Human Evolution, 9: 121-139. White T. D. and Harris J. M., 1977. Suid evolution and

correlation of African hominid localities. Science, 198: 13-21.

Wood B. A. and Chamberlain A.T., 1986. Australopithecus: grade or clade? In (B. A. Wood, L. Martin and P. Andrews, eds). Major Topics in Primate and Human Evolution, pp. 220-248, CambridgeUniversity Press, Cambridge.

AUSTRALOPITHECINES: ANCESTORS OF THE AFRICAN APES?

Human Evolution 9: 121-139, 1994

Since australopithecines display humanlike traits such as short ilia, relatively small front teeth and thick molar enamel, they are usually assumed to be related to Homo rather than to Pan or Gorilla. However, this assumption is not supported by many other of their features.

This paper briefly surveys the literature concerning craniodental comparisons of australopith species with those ofbonobos, common chimps, humans and gorillas, adult and immature. It will be argued, albeit on fragmentary data, that the large australopiths of East Africa were in many instances anatomically and therefore possibly also evolutionarily nearerto Gorilla than to Pan or Homo, and the South African australopithsnearer to Pan and Homo than to Gorilla. An example of a possible evolutionary tree is provided. It is suggested that the evidence concerning the relation of the different australopithecines with humans, chimpanzees and gorillas should be re-evaluated.

Key words: Hominid evolution, Australopithecus, robust polyphyly, gorilla, chimpanzee, bonobo, Lucy, Taung, molecular clock.

Introduction

Biomolecular data place the Homo/Pan splitting time between 8 and 4 Myr BP (e.g. Sarich, 1977; Hasegawa et al., 1987, 1988, 1989; Caccone & Powell, 1989). This means that at the time of the earliest undoubted australopithecines (ca. 4 Myr BP), the differences between human and chimpanzee ancestors were much less than those between present-day Homo and Pan, so that it is difficult to decide whether a particular fossil of that age belonged to the Homo or to the Pan clade. No a priori reason exists therefore to reject the idea that the African apes may have had australopith ancestors. Several people had contemplated this possibility even before Sarich & Wilson (1967) initiated the drastic reduction of the estimated Homo/Pan splitting time (e.g. Woodward, 1925; Smith, 1925; Keith, 1925a, b; 1931, p.115; Schultz, 1941, p.100; A. Hrdlicka in Howells, 1985; W. Abel; W. L. Straus, S.

Zuckerman, E. H. Ashton in Reader, 1988, p. 89 and p. 124). Following the introduction of the biomolecular evidence, the idea has revived (e.g. Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Hasegawa et al., 1985; Edelstein, 1987; Verhaegen, 1990; Trevino, 1991, p. 14-15).

This approach could also explain the discrepancy between the enormous number of fossil finds and the apparent total absence of fossil African ape ancestors from a period coveringat least the last four million years (Gribbin & Cherfas, 1983;Verhaegen, 1990). The usual explanations offered are that paleontologists have not worked in the appropriate areas, or that the probability of fossilization in the tropical forests,where the ancestral apes presumably lived, is very low becauseof the relative acidity or the wetness of the soil (e.g. G. S.Krantz in Kleindienst, 1975). These explanations are hard to reconcile with the numerous discoveries of forest-dwelling bovids, suids, monkeys, dryopithecines and probable early relatives of the orang-utan (Kleindienst, 1975; Kortlandt, 1975; cf. Pilbeam, 1982; Andrews & Cronin, 1982).

When Dart (1925) discovered the skull of Taung, he believed that it was in the human lineage because it showed what he called “humanoid” features such as relatively small canines and forward situation of the foramen magnum. His proposal was promptly rejected by nearly all his colleagues (e.g. Keith, 1925a,b; Smith, 1925; Woodward, 1925; Duckworth, 1925), who saw in Taung nothing more than a sort of young chimp or perhaps gorilla. They were supported in their opinionby the Piltdown skull, which showed a rather ape-like dentition together with a big brain, almost the opposite of the Taung child. But later, when Kenneth Oakley unmasked Piltdown Man as a fraud and Robert Broom concluded from his studies of postcrania that the South African australopithecines were bipedal, opinions about Taung changed and the australopiths became accepted as being closer to man than to apes.

This paper argues that the nearly general acceptance around 1950 of W. E. Le Gros Clark’s ideas, following Dart andBroom, that the South African australopiths were closer to humans than to “pongids” (mostly based on comparisons of theirpelvis and dentition, often with male gorillas, e.g. Le Gros Clark, 1978, first edition 1955) might have been an overreaction after the unmasking of Piltdown, and that the

anthropologists’ first impressions - that Taung was a fossil species of Pan - should be reconsidered. (That Taung was closerto Homo than to Gorilla and certainly Pongo, is of course not contested in this paper).

Homo-like features in australopiths: primitive?

In imitation of Dart, Broom and Le Gros Clark, the australopithecine species are now usually considered to be closer relatives of humans than of apes. This opinion is basedespecially on their locomotor and dental features.

Ventral position of foramen magnum It is generally accepted that the australopiths were more

bipedal than present-day gorillas and common chimps, mostly because of the Laetoli footprints almost 4 Myr BP, the short ilia of Lucy and Sts.14, the broader calcaneus and the more human-like orientations (though rather ape-like anatomy) of the ankle and knee articulations of the Hadar specimens (Stern& Susman, 1983; Latimer et al., 1987), and the more ventral position of the foramen magnum in many australopiths. “Early australopithecines are linked with living humans on the basis of shared characters related to bipedalism” (Andrews, 1992), but it is often argued that the African apes’ ancestors also were more bipedal (theory of W. L. Straus; see Coon 1954; Kleindienst, 1975; Goodman, 1982; Gribbin & Cherfas, 1983; Hasegawa et al., 1985; and esp. Edelstein, 1987; cf. Schultz 1949, p. 205). Indeed, that the African apes could evolve fromdigiti-palmigrades (all other primates, including human infants) to knuckle-walkers implies that they went through a phase where the arms were barely used for pronograde locomotion (cf. Edelstein, 1987); an intermediate phase of orthograde arm-hanging or brachiation insufficiently explains knuckle-walking since neither orangutans nor hylobatids show traces of knuckle-walking. Also, most anthropoids (especially the young) occasionally walk on two legs, and bipedal tendencies are very striking in the African apes (but virtually absent in Pongo). Chimpanzee fetuses shortly before birth show humanlike feet with ventrally oriented and adductedfirst digital rays (Coon, 1954). Common chimps often walk bipedally on muddy terrain (Nishida, 1980), and bonobos are even more frequently bipedal (Zihlman et al., 1978; De Waal,

1988). “When they are on the ground, anthropoid apes... often walk erect, and the mountain gorilla's foot, indeed, is already similar to man’s” (Rensch, 1972, p. 63; see also p. 130; Schultz, 1950; Edelstein, 1987). In addition, of all primates, only the African hominoids are fully plantigrade (Gebo, 1992):

“Orangutans have further enhanced foot mobility by adapting their feet for suspension and thus similarly utilize foot positions where the heel does not touch the substrate. Chimpanzees and gorillas represent an alternative pattern (plantigrady), in which the heel contacts the surface of the support at the end of the swing phase, especially during terrestrial locomotion. Thus chimpanzees and gorillas possess feet adapted for both arboreal and terrestrial substrates. African apes also share several osteological features related to plantigrady and terrestrial locomotion with early hominids. Humans and African apes are very similar in their use of plantigrady when moving or standing upon a terrestrial substrate and this pattern of foot use is extremely different from what characterizes all other primates”.

Also, young gorillas and chimpanzees have foramina magna more ventral than adults and well within the range of A. africanus Sts.5 (e.g. Ashton & Zuckerman, 1952; Schultz, 1955). Even in adults, the foramen has the same position indices in gracile (Sts.5) and robust australopithecines (KNM-ER 406) as in bonobos (Kimbel et al., 1984, table 9). Masters et al. (1991):

“Since Taung was perhaps 3.5 years of age at death (Bromage and Dean, 1985), the position of the foramen magnum may not have achieved its adult status. This contradicts the assessment made by Dart (1925), who interpreted the position of the foramen magnum as indicating bipedal locomotion in Australopithecus africanus”.

Thick enamel Thicker molar enamel was formerly treated as a reliable

sign of affinity with the human line, so that species such as “Ramapithecus” (now included in Sivapithecus and usually considered

to have Pongo as its closest living relative, see Pilbeam, 1982; Andrews & Cronin, 1982) were designated as possible human ancestors on the strength of this evidence. But this is no argument for a closer affinity of the australopithecines with humans than with African apes, since Martin (1985) arguesthat the extant great apes have secondarily reduced enamel - slight in the case of Pongo and more marked in Gorilla and Pan (butsee also Beynon et al., 1991). It is in no way inconsistent with australopiths being ancestral to African apes (Martin, 1985):

“thick pattern 3 enamel does not identify a hominid. Moreover, the common ancestor of the great apes and man, and of the African apes and man, would have had teeth resembling those of hominids... Of the living members of the great ape and human clade, only Homo sapiens retains thecondition of enamel thickness and development from the common ancestor of the clade and can therefore be regardedas the most dentally primitive member of it”.

Smaller anterior dentition The pronounced prognathism and large incisors and very

large canines of the adult males of G. gorilla and P. troglodytes are thought to exclude australopith ancestors, since most robust australopiths had “flat” faces and (at least in comparison with their enormous back teeth) small anterior teeth. But thisevidence is not conclusive: (1) A. afarensis and A. africanus also possessed moderately projecting canines, and the robust australopiths could have been extinct side-branches specialized for extremely tough food (e.g. Verhaegen, 1992), (2) even in robust australopiths (SK 23, Natron, L.7-125), theindices of the basic rectangle of the mandible are within the range of these of common chimps but outside those of humans (Kinzey, 1970); (3) in many robust specimens, the front teeth are so much worn that it is difficult to estimate how long their unworn canines would have been (but at least the A. boisei from Chesowanja showed unworn canines which were rather short), (4) in Gorilla and Pan “with advancing age, canines tend to wear flat to the level of the incisors” (Ryan & Johanson. 1989); (5) bonobos “have relatively small and only slightly dimorphic canine teeth” (Zihlman et al., 1978); (6) “infant greatapes have flat or orthognathic faces like modern humans” (Aiello & Dean, 1990, p, 197); (7) some specimens of H. erectus

had maxillary diastemata of 6 mm, as large as an orang’s (Howells, 1959, p. 157; Rensch, 1972, p. 36), and much larger than in the robust australopiths (who lived earlier); (8) selection for larger or smaller teeth can theoretically occur in very short evolutionary periods (cf. Silson, 1988, p. 19), and is claimed to have been demonstrated in only a few thousand years in human populations (Calcagno & Gibson, 1988);(9) the marked difference in prognathism between Negroes and Whites (e.g. Howells, 1959, p.269; Kinzey, 1970, fig. IA-B) developed in a time span of only about 200,000 years (Cann et al., 1987; Vigilant et al., 1991).

Moreover, it is not very likely that the primitive Africanhominoid condition included ape-like pronounced prognathism and very long canine teeth. See, for instance, Kinzey’s (1970)comparisons of the basic rectangle of the mandible in different Haplorhini (in Kenyapithecus africanus, e.g., it resemblesHomo rather than Pan), or the anatomy of the face in infant chimpanzees (orthognathism with relatively short milk canines and vertical mandibular symphysis).

Australopiths resemble young Pan or Gorilla

At first sight, australopith skulls are more reminiscent of African apes, especially juveniles and subadults, than of humans (even Le Gros Clark calls them ape-like creatures): thegeneral morphology of the gracile crania resembles that of bonobos or common chimps, and the larger crania are more gorilla-like (e.g. Lewin, 1987, p. 260; Zihlman et al., 1978; Rensch, 1972, p. 40; Robinson, 1960; Kennedy, 1991, fig.1). This is not contradicted by a more detailed look at their anatomy. Table 1 gives a few striking quotations about ape-like features of australopith skulls in general; Table 2 provides quotations about gorilla-like cranial features in large East African fossils; Table 3, about chimpanzee-like features in africanus and robustus crania.

It is a pity that this paper has to rely so heavily upon the anthropologists’ impressions (quoted in Tables 1, 2 and 3), but extensive comparisons with enough species (including several extinct hominid species, African hominoids and humans)are rather scarce. Even in recent excellent and thorough textbooks (e.g. Conroy, 1990; Aiello & Dean, 1990), australopith fossils are often compared only with man and one

of the great apes (usually the common chimp), and detailed comparisons of the australopithecine features with humans and all three African ape species (not to mention orang-utans), preferably of different subspecies (e.g. high- vs lowland gorilla), ages and sexes, are surprisingly rare in the literature (but see e.g. Schultz, 1955; McHenry, 1983; Demes, 1988). Because of these anthropocentric viewpoints, the differences between the African ape species - like those between the different australopith species - are often underestimated. In fact, Pan is more closely related to Homo than to Gorilla biochemically (see below), and Groves & Paterson (1991) in their computer analysis of 89 anatomical features, conclude that Pan is even morphologically slightly nearer to Homo than to Gorilla.

Table 1 - Some quotations on ape-like features in australopithcrania

“The evolution of the australopithecine crania was the antithesis of the Homo line. Instead of becoming less ape-like, as in Homo, they become more ‘ape-like’. Cranial proportions and ectocranial features that were thought to beunique among pongids evolved separately [? M. V.] in the australopithecines parallel [? M. V.] with the great apes. The features of KNM-WT 17000, therefore, are not as ‘primitive’ as they look. The robust Australopithecus did not evolve from a big-toothed pongid ancestor with large cranialsuperstructures, but from a small-toothed hominid with a rounder, smoother ectocranium, like A. africanus”. Ferguson, 1989b.

“Plio-Pleistocene hominids had markedly abbreviated [enamel]growth periods relative to modern man, similar to those of the modem great apes”. Bromage & Dean, 1985.

“Enamel thickness has been secondarily reduced in the African apes and also, although at a different rare and extent, in the orang-utan. Thick enamel, previously the mostimportant characteristic in arguments about the earliest hominid, does not therefore identify a hominid”. Martin, 1985 (but Beynon et al., 1991).

In the South African fossils including Taung, “sulcal patterns of seven australopithecine encocasts appear to be ape-like rather than human-like”. Falk, 1987.

“Cranial capacity, the relationship between endocast and skull, sulcal pattern, brain shape and cranial venous sinuses, all of these features appear to be consistent with an ape-like external cortical morphology in Hadar early hominids”. Falk, 1985.

In the type specimen of A. afarensis, “the lower third premolar of ‘A. africanus afarensis’ LH-4 is completely apelike”. Ferguson,1987b.

“A. afarensis is much more similar cranially to the modern African apes than to modern humans”. Schoenemann, 1989.

“Olson's assertion that the lateral inflation of the A.L. 333-45 mastoids is greater than in any extant ape is incorrect if the fossil is compared to P. troglodytes males or some Gorilla males and females. Moreover, the pattern of pneumatization in A. afarensis is also found only in the extantapes among other hominoids”. Kimbel et al., 1984.

“Prior to the identification of A. afarensis the asterionic notch was thought to characterize only the apes among hominoids. Kimbel and Rak relate this asterionic sutural figuration to the pattern of cranial cresting and temporal bone pneumatization shared by A. afarensis and the extant apes”. Kimbel et al., 1984.

“... the fact that two presumed Paranthropus [robustus] skulls were furnished with high sagittal crests implied that they had also possessed powerful occipital crests and ape-like planum nuchale... Nuchal crests which are no more prominent - and indeed some less prominent - will be found in many adult apes”. Zuckerman, 1954b.

In Sts.5, MLD-37/38, SK-47, SK-48, SK-83, Taung, KNM-ER 406,O.H.24 and O.H.5, “craniometric analysis showed that they had marked similarities to those of extant pongids. These basicranial similarities between Plio-Pleistocene hominids and extant apes suggest that the upper respiratory systems of these groups were also alike in appearance... Markedly flexed basicrania [are] found only in modern humans after the second year...”. Laitman & Heimbuch, 1982.

“The total morphological pattern with regard to the nasal region of Australopithecus can be characterized by a flat, non-protruding nasal skeleton which does not differ qualitatively from the extant nonhuman hominoid pattern, onewhich is in marked contrast to the protruding nasal skeletonof modern H. sapiens”. Franciscus & Trinkaus, 1988.

Table 2 - Quotations on gorilla-like features in large East African australopith crania

“Incisal dental microwear in A. afarensis is most similar to that observed in Gorilla”. Ryan & Johanson, 1989.

The composite skull reconstructed mostly from A.L.333 specimens “looked very much like a small female gorilla”. Johanson & Edey, 1981, p. 351.

“Other primitive [or advanced gorilla-like? M. V.] features found in KNM-WT 17000, but not know or much discussed for A.afarensis, are: very small cranial capacity; low posterior profile of the calvaria; nasals extended far above the frontomaxillar suture and well onto an uninflated glabella; and extremely convex inferolateral margins of the orbits such as found in some gorillas”. Walker et al., 1986.

As for the maximum parietal breadth and the biauriculare in O.H.5 and KNM-ER 406 “the robust australopithecines have values near the Gorilla mean: both the pongids and the robust australopithecines have highly pneumatized bases”. Kennedy, 1991 (see also his fig. 1).

In O.H.5, “the curious and characteristic features of the Paranthropus skull... parallel some of those of the gorilla”. Robinson, 1960.

The A. boisei “lineage has been characterized by sexual dimorphism of the degree seen in modern Gorilla for the length of its known history”. Leakey & Walker, 1988.

A. boisei teeth showed “a relative absence of prism decussation”; among extant hominoids, “Gorilla enamel showed relatively little decussation ...”. Beynon & Wood, 1986 (cf.Beynon et al., 1991).

Table 3 - Quotations on chimp-like features in South African australopith crania

“Alan [Walker] has analysed a number of Australopithecus robustus teeth and they fall into the fruit-eating category. More precisely, their teeth patterns look like those of chimpanzees... Then, when be looked at some Homo erectus teeth, be found that the pattern changed”. Leakey, 1981, pp.74-75.

“The ‘keystone’ nasal bone arrangement suggested as a derived diagnostic of Paranthropus [robustus] is found in an appreciable number of pongids, particularly clearly in some chimpanzees”. Eckhardt, 1987.

“P. paniscus provides a suitable comparison for Australopithecus [Sts.5]; they are similar in body size, postcranial dimensions and... even in cranial and facial features”. Zihlman et al., 1978.

“A. africanus Sts.5, which... falls well within the range of Pan troglodytes, is markedly prognathous or hyperprognathous”". Ferguson, 1989a.

In Taung, “I see nothing in the orbits, nasal bones, and canine teeth definitely nearer to the human condition than the corresponding parts of the skull of a modern young chimpanzee”. Woodward, 1925.

“The Taung juvenile seems to resemble a young chimpanzee more closely than it resembles L338y-6”, a juvenile A. boisei.Rak & Howell, 1978.

“In addition to similarities in facial remodeling it appearsthat Taung and Australopithecus in general, had maturation periods similar to those of the extant chimpanzee”. Bromage,1985.

“I estimate an adult capacity for Taung ranging from 404-420cm2, with a mean of 412 cm2. Application of Passingham’s curve for brain development in Pan is preferable to that for humans because (a) brain size of early hominids approximates that of chimpanzees, and (b) the curves for brain volume relative to body weight are essentially parallel in pongids and australopithecines, leading Hofman to conclude that ‘as with pongids, the australopithecines probably differed only in size, not in design’”. Falk, 1987.

In Taung, “pneumatization has also extended into the zygoma and hard palate. This is intriguing because an intrapalatal extension of the maxillary sinus has only been reported in chimpanzees and robust australopithecines among higher primates”. Bromage & Dean, 1985.

“That the fossil ape Australopithecus [Taung] ‘is distinguished from all living apes by the... unfused nasal bones…’ as claimed by Dart (1940), cannot be maintained in view of the very considerable number of cases of separate nasal bones among orang-utans and chimpanzees of ages corresponding to that of Australopithecus”. Schultz, 1941.

Only a few possibly relevant data linking an australopith fossil with one of the extant African hominoids could be obtained from the literature (cf. Tables 2 and 3). Uniquely derived cranial features of A. boisei and Gorilla concern: some incisal microwear features (Ryan & Johanson, 1989; though acquired ontogenetically, tooth wear reflects phylogenetic adaptations); enamel prism decussation (Beynon & Wood, 1986; cf. Beynon et al., 1991); orbital morphology (KNM-WT 17000, see Walker et al., 1986); body size (but see also McHenry, 1991). Uniquely derived features of South African australopiths with Pan and Homo concern: mandibular premolar root morphology (Wood et al., 1988; see also below). Uniquely derived features of A. robustus and Pan concern: tooth microwear (e.g. Leakey, 1981, p.74); nasal bone arrangement (Eckhardt, 1987); maxillary sinus topology (Bromage & Dean, 1985; see also Cave & WheelerHaines, 1940). Not obtained were: uniquely derived features ofSouth African fossils with Gorilla; of A. boisei with Pan; and of any australopith with Homo (i.e. features that are absent from all African ape species, mature and immature). Jenkins (1991):

“Tobias (1988) prepared a comparative list of the cranial,mandibular, dental and endocranial traits for H. habilis, A. africanus, A. robustus, and A. boisei to determine evidence for cladogenetic relationships. His tabular summaries enumerate numerous shared derived characters of all four taxa. However, he did not include any outgroup comparisons. In this poster, data for two outgroups [? M. V.], composed of Gorilla gorilla and Pan troglodytes, were compiledand compared to Tobias’ evaluations of H. habilis, A. africanus and A. boisei. The results show that numerous traits he used are also shared with Gorilla and Pan...”

Thick molar enamel and small anterior dentition are discussed above. Orthognathism, inter- mediate position of foramen magnum, relatively “short” arms, lateral plantar process of calcaneus, longer and adducted first metatarsals, etc. are seen in bonobos or/and immature apes. Lucy’s short ilium is not a good case: overall, her pelvis is as distinct from the human as it is from the chimpanzee’s (e.g. Stern & Susman 1983), and the Sterkfontein Sts.14 pelvis (notably the ischium) is even more chimp-like (Broom & Robinson, 1950;

Oxnard, 1984, fig. 10.1); short ilia (in proportion to trunk length) as in monkeys and humans are probably the ancestral condition, so that Coon (1954) could assert that, in pelvic morphology, apes look less like monkeys than humans do (cf. Schultz, 1950, fig. 6). W. L. Straus (in Schultz, 1936, p. 431):

“The human ilium would seem most easily derived from some primitive member of a preanthropoid group, a form which was lacking many of the specializations, such as reductionof the iliac tuberosity and anteacetabular spine and modification of the articular surface, exhibited by the modern apes. I wish to emphasize here that the anthropoid-ape type of ilium is in no sense intermediate between the human and lower mammalian forms. Its peculiar specializations are quite as definite as those exhibited by man, so that it appears very unlikely that a true anthropoid-ape form of ilium could have been ancestral to the human type”.

Overall, the more human-like features of the australopith hindlimbs are less abundant than the more ape-like features (summarized in Oxnard, 1984, Nota Bene following p. 334; and in Verhaegen, 1990). Moreover, it has been argued that all these human-like features (e.g. the superhumanly broad sacrum,long femoral neck and valgus knee) could have been correlated with some sort of bipedalism in the ancestral African hominoids (see the discussion above).

With the apparent exception of the front teeth reduction and the relative orthognathism in A. boisei and A. robustus (but juvenile African apes also are orthognathic, see Schmid & Stratil, 1986; Aiello & Dean, 1990, p. 197), later large australopith skulls (KNM-WT 17000) show more gorilla features than earlier ones (from A.L.333), and later smaller ones show more chimpanzee features than earlier ones (Taung more than Sts.5, and much more than Lucy). See, for instance, the first quotation of Table l; for KNM-WT 17000, Table 2; for Taung, Table 3, and Falk et al. (1989); and for Lucy, Ferguson (1987b).

(The same could be true of the postcrania: see Verhaegen (1990) and the discussion of the distal humerus below. Nevertheless, most Kromdraai and Swartkrans remains are usually described as being intermediate between humans and

chimps but more human- than ape-like (especially the lower limb features, e.g. the adducted hallux), and more human-like than those of Hadar (Susman, 1989; Gebo, 1992). This does not necessarily contradict the evolutionary trees proposed in thispaper: (1) although most Swartkrans fossils certainly belong to A. robustus, a few probably represent Homo (Susman, 1989); (2)the earliest split is not that between humans and (African) apes, but that between Pan-Homo and Gorilla (see below), and A. robustus undoubtedly belonged to Pan-Homo rather than to Gorilla; (3) at the time of A. robustus there already existed much more humanlike fossils (e.g. KNM ER-1470 and -148l), so that A. robustus must have belonged either to Pan or to an extinct side-branch of Pan-Homo; (4) prenatal apes show adducted great toes (see above), and Pan (notably paniscus) is more bipedal than Gorilla).)

In spite of the scarcity of comparative data from single sources, a few figures regarding skulls and dentitions (the postcrania are briefly discussed in Verhaegen, 1990) are brought together in Table 4a (comparative measurements from different sources were not used), and some preliminary conclusions emerge from it (Table 4b):

(1) The figures of the large afarensis skulls from A.L.333 are rather ape-like, with more bonobo-like foramen magnum indices, chimp-like frontal bone, and rather gorilla-like dental features.

(2) Overall, A. africanus from Makapansgat and Sterkfontein resemble Pan rather than Gorilla or Homo, and in bite force and foramen magnum indices, bonobos rather than common chimps.

(3) The figures of A. robustus from Swartkrans, mostly regarding the dentition, are generally intermediate between those of common chimp and gorilla.

(4) A. boisei KNM-ER 406 and O.H.5, in spite of the differences between them, are more gorilla-like (KNM-ER 406 iseven super-gorilla in bite force).

Every australopith species in this Table thus appears morphologically nearer to at least one of the African ape species than it is to humans.

Robust polyphyly?

Biomolecular results leave no doubt that Pan is genetically closer to Homo than to Gorilla (e.g. Goodman, 1982; Hasegawa et al.,

1985, 1987, 1988; Caccone & Powell, 1989; Sibley et al., 1990; Gonzalez et al., 1990; Ruvolo et al., 1991; Begun, 1992), and contrary to the prevailing opinion this is not contradicted bythe anatomical evidence (Groves & Paterson, 1991). This implies that the African hominoids first split into Pan-Homo (smaller, relatively gracile) and Gorilla (larger, super-robust),and that many of the traits that common chimps share with gorillas but not with bonobos or humans could have developed in parallel with gorillas (e.g. very long and sexually dimorphic canines, “very” dorsal foramen magnum, ectocranial crests, arms considerably longer than legs). Convergent and parallel, even reverse or fluctuating evolution of anatomical traits are among the commonest features of biological evolution (e.g. Trinkaus, 1990; Hartman, 1989; Sheldon, 1988; Seger, 1987; Gibbs & Grant, 1987; Cartmill, 1982; White & Harris, 1977; Darwin, 1903, p.171), and the final proof that Darwinism is not a tautology. “Parallel evolution occurs when two species adopt a lifestyle that is more or less similar. Ifthe lifestyle is essentially identical, and the species from asimilar genetic background, the end result may be almost indistinguishable to other than detailed examination” (R. G. Silson, pers. comm.).

The very long canines and very dorsal foramen magnum of adult gorilla and common chimp males (but not of subadult African apes nor of adult bonobos) could well be derived and rather recent adaptations to the same environmental (e.g. in response to climatic) changes and cannot be explained by mere allometry. Even knuckle-walking of chimps and gorillas has been argued to have arisen independently (Begun, 1992), possibly in more bipedal ancestors (Kleindienst, 1975; Hasegawa et al., 1985; Edelstein, 1987). Indeed, Gorilla knuckle-walking anatomy and ontogeny are much better developed than inPan, and are different from Pan (Inouye, 1992). And the LCA (thelast common ancestor of Homo and Pan) had not yet acquired knuckle-walking since humans do not at any age show the slightest trace of knuckle-walking behaviour: (1) we lean (e.g. on a table) far more comfortably on our proximal than onour middle hand phalanges; (2) whereas in knuckle-walking apesthe middle hand phalanges are naked, in many men they are dorsally haired, and fingers III and IV (that bear most weightin knuckle-walkers) even more frequently than V and II (Harrison, 1958; Singh, 1982; Ikoma, 1986); (3) “human infants

walk or run spontaneously on all fours and this invariably with the palms flat on the ground and the fingers completely extended” (Schultz, 1936, p. 264).

Lucy’s arms were much shorter than a bonobo's (humerus 24 cm vs 29 cm; cf. 26 cm in human pygmies) and lacked knuckle-walking adaptations (Jungers, 1982; Stern & Susman, 1982), butlater the small hominid O.H.62 had more chimp- and bonobo-likeproportions (Korey, 1990; Aiello & Dean, 1990, p. 258; Wood, 1992, box 2), and the larger KNM-ER 1500 (probably a boisei female) showed some gorilla-like proportions, e.g. relatively large forelimbs (McHenry, 1978, 1992). While the early KNM-KP 271 distal humerus was “similar to that of modern man” (Senut,1980; cf. Oxnard, 1984, fig.10.12; and Aiello & Dean, 1990, p.365 and p. 368), A. robustus TM 1517 was more chimp-like, and A. boisei KNM-ER 739 more gorilla-like (Senut, 1980; Aiello & Dean, 1990, pp. 365-368). Body weight estimations for robustus and boisei based on formulae for ape postcrania fit much better with the massive jaws than estimations based on human formulae (see McHenry, 1991). The boisei ulnae O.H.36 and L.40-19 and humerus KNM-ER 739 were of gorilla robusticity and length (McHenry, 1991, 1992; Howell & Wood, 1974; Senut, 1980; Leakey, 1971; Aiello & Dean, 1990, p. 367-369), and the curvature and the cross-section of L.40-19 are reminiscent of knuckle-walkers (Howell & Wood, 1974); “the Rudolf australopithecines, in fact, may have been close to the ‘knuckle-walker’ condition, not unlike the extant African apes” (Leakey, 1971). Their arm lengthening and strengthening is paralleled ontogenetically inthe African apes; Rensch (1972, p. 45) even states that “it isonly after birth that an ape’s arms become disproportionally long”, but this can only be true when arm growth relative to the height in African apes is compared with monkeys (Schultz, 1936, fig. 15).

The possibility should be considered that robustus and boisei did not belong to the same (robust) branch, but that their robust traits represented parallel adaptations (cf. Delson, 1987; Grine, 1987; Trinkaus, 1990; Conroy, 1990, fig. 6.40.d).Indeed, super-robust specimens from East Africa (KNM-WT 17000)appeared in the fossil record before the less robust A. robustus from South Africa, and the morphological differences between africanus and robustus are less than those between robustus and boisei (e.g. Leakey, 1959, 1960; Wood, 1978; Wood & Chamberlain, 1987). This is particularly clear in dental morphology (Hunt &

Vitzthum, 1986; Wood & Uytterschaut, 1987; Wood & Engleman, 1988; Wood et al., 1988). An analysis of root morphology in mandibular premolars, for instance, revealed moderate root reduction in A. africanus, A. robustus and P. troglodytes, pronounced reduction in Homo but root molarization in A. boisei compared withA. afarensis, G. gorilla and most higher primates (Wood et al., 1988).

Possible evolutionary trees of the australopithecines are obscured by the incompleteness of the fossil material, by parallel (e.g. boisei/robustus) or even reverse evolution of some anatomical characters, by mosaic evolution and retention of ancestral characters in some branches (stagnations, and “sudden” accelerations of certain features). Nevertheless, some relationships seem to emerge (Figure 1):

(1) In East Africa, A. boisei – and perhaps some larger afarensis from A.L.333 or Laetoli as well – is morphologically (Tables 2 and 4), and therefore probably cladistically closer to Gorilla than to Pan or Homo. (This does not imply that some of their anatomical features cannot be closer to humans or to chimpanzees than to gorillas. Nor that (all) gorillas must descend from A. boisei. Biomolecular data suggest that the difference between highland and lowland gorilla - like that between common chimp and bonobo - is less than half that between man and chimp (Gribbin & Cherfas, 1983, p. 137), i.e. highland and lowland gorillas possibly diverged 3-2 Myr BP. Inview of the small anterior dentition of A. boisei, the possibilities should be considered that some or all gorillas descend from a form nearer to KNM-WT 17000 than to A. boisei, or - the prevailing opinion - that fossil ancestors of gorillas have not been discovered yet.)

Since Homo and Pan diverged probably one or two million years later than Pan-Homo and Gorilla (e.g. Ruvolo et al., 1991), it is not surprising that Wood (1978), in a classification of East African fossil hominids, states that “by relying solely on morphology, the taxa presented are most obviously subdivided into the ‘robust’ australopithecine taxon Australopithecus boisei, and another group consisting of all the remaining taxa... In contrast to the conformity within the ‘robust’ lineage the ‘non-robust’ hominids display a wide range of variation”.

(2) South African australopiths (Tables 3 and 4) - and probably some very small specimens from East Africa such as Lucy or “H. habilis” as well (cf. Zihlman, 1985; Ferguson,

1987a,b, 1992; Wood, 1978, 1992a,b) - show more affinities with Pan-Homo than with Gorilla. A striking example is the incus bone SK 848, which is clearly more like Homo or Pan than like Gorilla (Rak & Clark, 1979, fig. 1). Because A. robustus lived at the time of KNM-ER 1470 (probably an early Homo), and Taung lived even later (Partridge, 1973, 1985), they could have belonged to the Pan clade but not to the Homo clade. Taung’s endocast, dentition, facial growth and possibly foramen magnumposition strikingly resemble those of apes and chimpanzees (Falk et al., 1989). Simons (1989):

“Dart’s enthusiasm for A. africanus as a human ancestor was occasioned by his misidentification of the lamboid structure as the lunate sulcus and thus reading a human-like sulcal pattern in the natural endocast of the brain of the Taung child”.

Discussion

Why are many paleoanthropologists so reluctant to consider just the possibility that some or all of the australopithecines could have been evolutionarily nearer to one of the African apes than to humans?

(1) When paleoanthropologists discover fossil remains, they often - understandably - tend to stress the human-like features of their finds. Subsequent researchers, however, frequently obtain more detached views.

(2) Man is often considered to possess a great number of features that are uniquely derived from the supposed “primitive hominoid condition”: thick enamel, short canines, forward position of the foramen magnum, short ilia, non-grasping feet, low intermembral index, etc. But the primitive hominoid condition is largely hypothetical: as discussed above, man seems to be more primitive in some of these features than the apes (e.g. thick enamel, low pelvis); and inmany features the differences between the ape species (e.g. between Pongo and Gorilla) are larger than those between humans and some of the apes (e.g. relative arm length, foot shape). Most probably the ancestral hominoids were neither like humansnor like any of the extant ape species.

(3) In the same way, it is often uncritically accepted that the LCA was much more chimp- than human-like. As Hasegawaet al. (1985) say:

“It is unknown whether the last common ancestor of human and chimpanzee was like the living chimpanzee or like the living human. However it seems to have been widely assumedimplicitly that the common ancestor of the two species wasmore like the chimpanzee than the human. There has been a tendency to view hominid features as specialized and thoseof apes as unspecialized. Any fossil hominoids that bear some resemblance to humans have been readily considered tobe human ancestors”.

Such assumptions are reinforced by using terms like “primitive”, “plesiomorphic” or “less advanced” (which imply that the ancestral character is known), where the more neutral“apelike” or (if possible, and more precisely) “chimp-like”, “bonobo-like” or “gorilla-like” would be preferable. The anthropocentric fallacy enshrined in the usage of “primitive” has more than once been challenged (Gribbin & Cherfas, 1993; Edelstein, 1987; Verhaegen, 1990). Since homoplasy, convergence, and reverse (and even fluctuating) evolution are so common, ontogeny may provide more reliable criteria to decide what is primitive (Trinkaus, 1990; cf. Northcutt, 1990). “Morphological characters can be subjected to parallel or convergent evolution, and cannot be used with confidence for phylogenetic reconstructions unless the probability of parallel evolution is evaluated or rejected in a proper way” (Hasegawa et al., 1987).

As we go further back in time, we may expect that human ancestors become more chimpanzee-like, but also that the chimpanzees’ ancestors become more human-like, i.e. display a few human-like features. Assuming that the LCA looked much more like a chimpanzee than a human and that subsequently humans have evolved much more than common chimps is statistically less likely than assuming that the LCA already possessed a few mosaic human-like features (e.g. facultative bipedalism, orthognathism, thicker enamel) and that both branches(Homo and Pan) underwent evolutionary changes towards their present-day representants (e.g. much longer legs in humans, longer arms in chimps). In fact, it seems most economical to

assume that the LCA 8-4 Myr BP looked somewhat like bonobos (or like subadult chimpanzees), which are in several instances- but not, for instance, in body weight - intermediate betweenhumans and common chimps, e.g. in relative canine size, caninedimorphism, orthognathisrn, foramen magnum indices, relative arm and leg lengths, bipedalism and knuckle-walking. Although the LCA lived earlier, the gracile australopiths of 3-2.5 Myr BP (Lucy, Sterkfontein) are the best approximation we presently have: see Aiello & Dean (1990, p. 254), or in Table 3 the quotation of Zihlman et al. (1978).

It seems that, while our ancestors were becoming more and more human-like, the African apes - at first the ancestor of the gorillas and shortly thereafter that of both chimpanzees -for unknown reasons (climatic and habitat changes?) - broke away from our evolutionary direction, partially reversed theirevolution, and became again - the three species to different degrees - more like monkeys in thinner enamel, larger front teeth, prognathism, ectocranial crests, relatively smaller endocast, more dorsal foramen magnum, elongated iliac blades, short femoral necks, less valgus knees, more grasping feet, quadrupedalism, etc. (but not, for instance, in body size, relative arm length, knuckle-walking, pelvic height, number oflumbar, sacral and coccygal vertebrae).

There are admittedly several weak spots in this scenario: the many reversals (notably in the lower limb anatomy) and parallelisms (e.g. anterior dentition, iliac anatomy, knuckle-walking adaptations) in the evolution of Gorilla and Pan. (If Pongois included in the comparison, even more - apparently improbable - parallelisms are needed, although, as discussed above, for most of such features (e.g. sexual dimorphism, foramen magnum position, relative arm length, foot shape), at least one African ape species can be found to be more different from orangs than from humans, and Andrews (1992), ina review of Miocene hominoids, even asserts that “if Sivapithecus belongs in the orangutan clade, as I have argued, the shared [postcranial] morphology of the orang-utan and the African apes must have arisen independently”).

However, if these reversals and parallelisms are correlated (re-adaptations to, for instance, an older, less “innovating” or less human-like lifestyle or environment), thecounter-argument to my scenario fails. Moreover, the traditional hypothesis - that all australopithecines are more

closely related to humans than to African apes - seems to havemore serious difficulties, since it does not explain: (1) the apparent complete absence of fossil ancestors or relatives of any African ape; (2) the various australopith-like features that are present in premature though not in adult African apes(e.g. orthognathy, less dorsal foramen magnum, more humanlike feet); (3) the fact that all australopiths lack the uniquely derived bony features which set man (at least since H. erectus) clearly apart from the other catarrhines (e.g. external nose, very large brain, very long legs), and that they resemble the apes in these respects; (4) that every one of the australopithspecies has more features in common with either gorillas or chimpanzees than with humans (e.g. Tables 2, 3 and 4); (5) andthat at the time of the robust australopiths there already lived more humanlike creatures (KNM-ER 1470).

(Oxnard’s (1984, p. 307-332) proposition - that the australopiths were evolutionarily nearly equidistant from African apes and humans and left no descendants today - does not have the fifth difficulty. Also, in my opinion, Oxnard correctly states that many australopith postcrania were biomechanically unique, and could have represented adaptationsto a well-defined lifestyle (e.g. Verhaegen, 1992).)

Conclusion

A review of the paleo-anthropological literature reveals no data that exclude the possibility that both gorillas and chimpanzees could have had australopith ancestors. Bipedalism is generally considered to be the shared feature that links australopithecines with humans, and there is no doubt that at least some of the australopith species were partial bipeds. But it has never been proven that the African apes’ unique locomotion (plantigrade knuckle-walking) could not have evolved from some kind of (“short”-legged) bipedalism. In fact, insofar as the fragmentary fossil material and the incomplete comparisons with extant apes allow, ontogenetic andmorphological evidence tends to favour the hypothesis that thelast common ancestor of Homo and Pan 8-4 Myr BP was a partially bipedal, gracile australopith with chiefly a mosaic of human and chimpanzee (esp. bonobo) features: low sexual dimorphism, minimal prognathism, slightly enlarged canines, non-protrudingnasal skeleton, smooth ectocranium without crests, “small”

brain with ape-like sulcal pattern, relatively non-flexed basicranium, intermediate position of foramen magnum, “short” forelimbs without knuckle-walking features, low ilia, (very) long femoral necks, “short” legs, (very) valgus knees, full plantigrady, longer and not very abductable halluces.

I expect that when australopith fossil material is re-examined and compared in detail with every one of the large hominoids, in most cases it will resemble either Pan or Gorilla more closely than it resembles Homo and certainly Pongo.

ACKNOWLEDGMENTS – I wish to thank A. S. Ryan, M. Goodman, M. Hasegawa, R. G. Silson, M. R. Kleindienst, E. Morgan and especially J. Verhulst for their corrections and comments on various versions of this manuscript.

References

Aiello L. & Dean C., 1990. An Introduction to Human Evolutionary Anatomy. Academic Press, London.

Andrews P., 1992. Evolution and environment in the Hominoidea. Nature, 360: 641-646.

Andrews P. & Cronin J.E., 1982. The relationships of Sivapithecus and Ramapithecus and the evolution orang-utan. Nature, 297: 541-546.

Ashton E.H. & Zuckerman S., 1952. Age changes in the position of the occipital condyles in the gorilla. American Journal of Physical Anthropology, 10: 277-288.

Begun D. R., 1992. Miocene fossil hominids and the chimp-human clade. Science, 257: 1929-1933.

Beynon A. D. & Wood B. A., 1986. Variations in enamel thickness and structure in East African hominids. American Journal of Physical Anthropology, 70: 177-193.

Beynon A. D., Dean M.C. & Reid D. J., 1991. On thick and thin enamelin hominoids. American Physical Anthropology, 86: 295-309.

Bromage T. G., 1985. Taung facial remodelling: a growth and development study. In (P. V. Tobias, Evolution, pp. 239-245, Alan R. Liss, New York.

Bromage T. G. & Dean M. C., 1985. Re-evaluation of age at death of immature fossil hominids. Nature, 317: 527.

Broom R. & Robinson J. T., 1950. Notes on the pelvis of the fossil ape-men. American Journal of Physical Anthropology, 8:489-494.

Caccone A. & Powell J. R., 1989. DNA divergence among hominoids. Evolution, 43: 25-942.

Calcagno J.M. & Gibson K. R., 1988. Human dental reduction: natural selection or the Probable Mutation Effect. American Journal of Physical Anthropology, 77: 505-517.

Cartmill M., 1982. Basic primatology and prosimian evolution. In (F. Spencer, ed. A History of Physical Anthropology 1930-1980,pp. 14-186, Academic, New York.

Cave A.J.E. & Wheeler Haines R., 1940. The paranasal sinuses of the anthropoid apes. Journal of Anatomy, 43-523.

Conroy G. C., 1990. Primate Evolution. W.W. Norton, New York. Coon S.C., 1954. The Story of Man. Knopff, New York. Dart R. A., 1925. Australopithecus africanus: the man-ape of South America.

Nature, 115, 195- 199. Darwin C., 1903. On the Origin of Species by Means of Natural

Selection. Watts and Co, London. Delson E., 1987. Evolution and palaeobiology of robust Australopithecus.

Nature, 327: 654-655. Demes B. & Creel N., 1988. Bite force, diet and cranial morphology of fossil

hominids. Journal of Human Evolution, 17: 657-670. De Waal F., 1988. Peacemaking among Primates. Harvard

University Press, London. Duckworth W.L.H., 1925. The fossil ape from Taungs. Nature, 115: 236-

237. Eckhardt R.B., 1987. Hominoid nasal region polymorphism and its

phylogenetic significance. Nature, 328:333-335. Edelstein S. J., 1987. An alternative paradigm for hominoid evolution.

Human Evolution, 2: 169-174.Falk D., 1985. Hadar AL 162-28 endocast as evidence that brain enlargement

preceded cortical reorganization in hominid evolution. Nature, 313: 45-47.

Falk D., 1987. Hominid paleoneurology. Annual Review of Anthropology, 16: 13-30.

Falk D., Hildeholt C. & Vannier M. W., 1989. Reassessment of the Taung early hominid from a perspective. Journal of Human Evolution,18: 485-492.

Ferguson W.W., 1987a. Revision of the subspecies of Australopithecus africanus (Primates, Hominidae), including a new subspecies from the late Pliocene of Ethiopia. Primates, 28: 258-265.

Ferguson W.W., 1987b. Reconstruction and re-evaluation of the skull of Homo antiquus (Hominoidea, Homininae) from Hadar. Primates, 28: 377-391.

Ferguson W.W., 1989a. Reappraisal of the taxonomic status o the cranium Stw 53 of the Plio-Pleistocene from Sterkfontein, in South Africa. Primates, 30:103-109.

Ferguson W.W., 1989b. A new species of the genus Australopithecus (Primates – Hominidae) from the Plio-Pleistocene deposits West of Lake Turkana in Kenya. Primates, 30: 223-232.

Ferguson W. W., 1992. “Australopithecus afarensis”: a composite species. Primates, 33: 273-279.

Franciscus R. G. & Trinkaus E., 1988. Nasal morphology and the emergence of Homo erectus. American Journal of Physical Anthropology, 75: 517-527.

Gebo D. L., 1992. Plantigrady and foot adaptation in African apes: implications for hominid origins. American Journal of Physical Anthropology, 89: 29-58.

Gibbs H. L. & Grant P. R., 1987. Oscillating selection on Darwin’s finches.Nature, 327: 511-513.

Gonzalez I. L., Sylvester J. E., Smith T. F., Stamholian D. & Schmickel R. D., 1990. Ribosomal RNA gene sequences and hominoid phylogeny. Molecular Biological Evolution, 7: 203-219.

Goodman M., 1982. Biomolecular evidence on human origins from the standpoint of Darwinian theory. Human Biology, 54: 247-64.

Gribbin J. & Cherfas J., 1983. The Monkey Puzzle. Triad, London.

Grine F. E., 1987. The evolutionary history of the “robust” australopithecines. AnthroQuest, 38: 7-9.

Groves C. P. & Paterson J. D., 1989. Testing hominoid phylogeny with the PHYLIP programs. Journal of Human Evolution, 20: 167-183.

Harrison R. J., 1958. Man the Peculiar Animal. Penguin, Harmondsworth.

Hartman S. E., 1989. Stereophotogrammatic analysis of occlusal morphology of extant hominoid molars: phenetics and function. American Journal ofPhysical Anthropology, 80:145-166.

Hasegawa M., Kishino H. & Yano T., 1985. Dating of the human-ape splitting by a molecular clock mitochondrial DNA. Journal of Molecular Evolution, 2:160-174.

Hasegawa M., Kishino H. & Yano T., 1987. Man’s Place in Hominoidea as inferred from molecular clocks. Journal of Molecular Evolution, 26: 13-147.

Hasegawa M., Kishino H. & Yano T., 1988. Phylogenetic inference from DNA sequence data. In (K. Matsusita, ed.) Statistical Theory and Data Analysis II, pp. 1-13, North-Holland, Amsterdam.

Hasegawa M., Kishino H. & Yano T., 1989. Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed downin Hominoidea. Journal of Human Evolution, 18: 461-476.

Howell F. C. & Wood B. A., 1974. Early hominid ulna from the Omo basin,Ethiopia. Nature, 249: 174-6.

Hunt K. & Vitzthum V. J., 1986. Dental metric assessment of the Omo fossils: implications for the phylogenetic position of Australopithecus africanus. American Journal of Physical Anthropology,71:141-155.

Ikoma E., 1986. Anthropological study of digital and parietal hair of Canadians.American Journal of Physical Anthropology, 69: 483-487.

Inouye S. E., 1992. Ontogeny of knuckle-walking hand postures in African apes. American Journal of Physical Anthropology, Supplement14: 55.

Jenkins L., 1991. Synapomorphic features in Gorilla gorilla, Pan troglodytes and Pliopleistocene hominids. American Journal of Physical Anthropology, Abstracts 60th annual meeting, p. 100.

Johanson D. C. & Edey M. A., 1981. Lucy, the Beginnings of Mankind. Granada, London.

Jungers W. L., 1982. Lucy’s limbs: skeletal allometry and locomotion in Australopithecus afarensis. Nature, 297: 676-678.

Keith A., 1925a. The fossil anthropoid ape from Taungs. Nature, 115: 234-235.

Keith A., 1925b. The Taungs skull. Nature, 116: 462-463. Keith A., 1931. New Discoveries Relating to the Antiquity of

Man. Williams and Norate, London. Kennedy G. E., 1991. On the autapomorphic traits of Homo erectus.

Journal of Human Evolution, 20: 375-412.Kimbel W. H., White T. D. & Johanson D. C., 1984. Cranial

morphology of Australopithecus afarensis: a comparative study based on a composite reconstruction of the adult skull. American Journal of Physical Anthropology, 64: 337-388.

Kinzey W. G., 1970. Basic rectangle of the mandible. Nature, 228: 289-290.

Kleindienst M. R., 1975. On new perspectives on ape and human evolution. Current Anthropology. 16: 644-646.

Korey K. A., 1990. Deconstructing reconstruction: the OH 62 humerofemoral index. American Journal of Physical Anthropology, 83:25-33.

Kortlandt A., 1975. On new perspectives on ape and human evolution: reply. Current Anthropology, 16: 647- 651.

Laitman J. T. & Heimbuch R. C., 1982. The basicranium of Plio-Pleistocene hominid as an indicator of their upper respiratory systems. American Journal of Physical Anthropology, 59: 323-343.

Latimer B., Ohman J.C. & Lovejoy C. O., 1987. Talocrural joint in African hominoids: implications for Australopithecus afarensis. American Journal of Physical Anthropology, 74: 155-175.

Leakey L. S. B., 1959. A new fossil skull from Olduvai. Nature, 184: 491-493.

Leakey L. S. B., 1960. The affinities of the new Olduvai australopithecine. Nature, 186: 456-458.

Leakey R. E., 1971. Further evidence of Lower Pleistocene hominids from East Rudolf, North Kenya. Nature, 231: 242-245.

Leakey R. E., 1981. The Making of Mankind. Michael Joseph, London.

Leakey R. E. F. & Walker A., 1988. New Australopithecus boisei specimens from East and West Lake Turkana, Kenya. American Journal of Physical Anthropology, 76: 1-24.

Le Gros Clark W. E., 1978. The Fossil Evidence for Human Evolution. University of Chicago Press, Chicago.

Lewin R., 1987. Bones of Contention. Simon & Schuster, New York.

Martin L., 1985. Significance of enamel thickness in hominoid evolution. Nature, 314: 260-263.

Masters A. V., Falk D. & Gage T. B., 1991. Effects of age and gender on the location and orientation of the foramen magnum in rhesus macaques (Macaca mulata). American Journal of Physical Anthropology, 86: 75-80.

McHenry H. M., 1978. Fore- and hindlimb proportions in Plio-Pleistocene hominids. American Journal of Physical Anthropology, 49: 15-22.

McHenry H. M., 1983. The capitate of Australopithecus afarensis and A. africanus. American Journal of Physical Anthropology, 62: 187-198.

McHenry H. M., 1991. Petite bodies of the “robust” australopithecines. American Journal of Physical Anthropology, 86: 445-454.

McHenry H. M., 1992. Body size and proportions in early hominids. AmericanJournal of Physical Anthropology, 87: 407-431.

Nishida T., 1980. Local differences to water among wild chimpanzees. FoliaPrimatologica, 33: 189-209.

Northcutt R.G., 1990. Ontogeny and phylogeny: a re-evaluation of conceptual relationships and some applications. Brain, Behavior and Evolution, 36: 116-140.

Oxnard C. E., 1984. The Order of Man. Yale University Press, New Haven.

Partridge T. C., 1973. Geomorphological dating of openings at Makapansgat, Sterkfontein, Swartkrans and Taung. Nature, 246: 75-79.

Partridge T.C., 1985. Spring flow and tufa accretion at Taung. In (P.J. Tobias, ed.) Hominid Evolution, pp. 171- 187. Alan R. Liss, New York.

Pilbeam D., 1982. New hominoid skull material from the Miocene of Pakistan. Nature, 295: 232-234.

Rak Y. & Clarke R. J., 1979. Ear ossicle of Australopithecus robustus. Nature, 279: 62-63.

Rak Y. & Howell F.C., 1978. Cranium of a juvenile Australopithecus boisei from the Lower Omo Basin, Ethiopia. American Journal of Physical Anthropology, 48: 345-366.

Reader J., 1988. Missing Links. Penguin, London. Rensch B., 1972. Homo sapiens, from Man to Semigod. Columbia

University Press, New York. Robinson J. T., 1960. The affinities of the new Olduvai specimen. Nature,

186: 456-458. Robinson J. T., 1972. The bearing of East Rudolf fossils on early hominid

systematics. Nature, 240: 239-240. Ruvolo M., Disotell T. R., Allard M. W., Brown W. M. &

Honeycutt R. L., 1991. Resolution of the African hominoid trichotomy by use of a mitochondrial gene sequence. Proceedings of the NationalAcademy of Sciences, U.S.A., 88: 1570-1574.

Ryan A. S. & Johanson D. C., 1989. Anterior dental microwear in Australopithecus afarensis: comparisons with human and nonhuman primates. Journal of Human Evolution, 18: 235-268.

Sarich V. M., 1977. Rates, sample sizes, and the neutrality hypothesis for electrophoresis in evolutionary studies. Nature, 265: 24-28.

Sarich V.M. & Wilson A. C., 1967. Immunological time scale for hominid evolution. Science, 158: 1200-1203.

Schmid P. & Stratil Z., 1986. Growth changes, variations and sexual dimorphism of the gorilla skull. In (J.B. Else & P.C. Lee, eds.) Primate Evolution, pp. 239-247, Cambridge University Press, Cambridge.

Schoenemann P. T., 1989. Comparison of intraspecific craniometric variabilityin Homo, Pan and Gorilla. American Journal of Physical Anthropology, 78: 298.

Schultz A. H., 1936. Characters common to higher primates and characters specific for man. Quarternary Review of Biology, 11: 259-283 and 425-455.

Schultz A. H., 1941. Ontogenetic specializations of man. Archiv Julius Klaus-Stiftung, XXIV: 197-216.

Schultz A. H., 1941. Growth and development of the orang-utan. Contributions to Embryology, XXIX: 57-1 10.

Schultz A. H., 1950. The physical distinctions of man. Proceedings of the American Philosophical Society, 94: 428-449.

Schultz A. H., 1955. The position of the occipital condyles and of the face relative to the skull base in primates. American Journal of Physical Anthropology, 13: 97-120.

Seger J., 1987. El Nino and Darwin’s finches. Nature, 327: 461. Senut B., 1980. New data on the humerus and its joints in Plio-Pleistocene

hominids. Collegium Anthropologicum, 4: 87-93. Sheldon P., 1988. Making most of the evolution diary. New Scientist,

1596: 52-54. Silson R. G., 1988. Additive Gene Systems. Greenfield

Publications, Tring. Sibley E. G., Comstock J.A. & Ahlquist E. G., 1990. DNA

hybridization evidence of hominoid phylogeny - a reanalysis of data. Journalof Molecular Evolution, 30: 202-236.

Simons E. L., 1989. Human origins. Science, 245, 1343-1350. Singh J.D., 1982. Distribution of hair on phalanges of the hand in Nigerians.

Acta Anatomica, 112: 31-35. Smith G.E., 1925. The fossil anthropoid ape from Taungs. Nature, 1 15:

235. Stem J. T. & Susman R.L., 1983. The locomotor anatomy of

Australopithecus afarensis. American Journal of Physical Anthropology, 60: 279-317.

Tobias P. V., 1968. Pleistocene deposits and new fossil localities in Kenya. Nature, 217: 479-480.

Trevino S., 1991. Grain-collection, Humans' Natural EcologicalNiche. Vantage Press, New York.

Trinkaus E., 1990. Cladistics and the hominid fossil record. American Journal of Physical Anthropology, 83: 1-11.

Verhaegen M. J. B., 1990. African ape ancestry. Human Evolution, 5: 295-297.

Verhaegen M. J. B., 1992. Did robust australopithecines partly feed on hard parts of Gramineae? Human Evolution, 7: 63-64.

Vigilant L., Stoneking M., Harpending H., Hawkes K. & Wilson A. C., 1991. African populations and the evolution of human mitochondrial DNA. Science, 53: 1503-7.

Walker A., Leakey R. E., Harris J. M. & Brown F. H., 1986. 2.5-Myr Australopithecus boisei from West of Lake Turkana, Kenya. Nature, 322: 517-552.

White T. D. & Harris J. M., 1977. Suid evolution and correlation of African hominid localities. Science, 198: 13-21.

Wood B. A., 1978. Classification and phylogeny of East African hominids. In (P. V. Tobias, ed.) Hominid Evolution, pp. 351-372, Alan R. Liss, New York.

Wood B. A., 1992a. Old bones match old stones. Nature, 355: 678-679. Wood B. A., 1992b. Origin and evolution of the genus Homo. Nature, 355:

783-790. Wood B. A., Abbott S. A. & Uytterschaut H., 1988. Analysis of the

dental morphology of Plio-Pleistocene hominids. IV. Mandibular postcanine root morphology. Journal of Anatomy, 156: 107-139.

Wood B. A. & Chamberlain A. T., 1987. The nature, and affinities of the "robust" australopithecines: a review. Journal of Human Evolution, 16: 625-641.

Wood B. A. & Engleman C.A., 1988. Analysis of the dental morphology of Plio-Pleistocene hominids: V. Maxillary postcanine tooth morphology. Journal of Anatomy, 161: 1-35.

Wood, B. A. & Uytterschaut H., 1987. Analysis of the dental morphology of Plio-Pleistocene hominids: III. Mandibular premolar crowns. Journal of Anatomy, 154: 121-156.

Woodward A. S., 1925. The fossil anthropoid ape from Taungs. Nature, 115: 235-236.

Zihlman A. L, Cronin J.E, Cramer D. L. & Sarich V.M., 1978. Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature, 275: 744-746.

Zihlman A. L., 1985. Australopithecus afarensis: two sexes or two species? In(P. V. Tobias, ed.) Hominid Evolution, pp. 213-220, Alan R. Liss, New York.

Table 4A - Measurements of australopithecine, African ape and human skulls

foramen magnum indicesa 333-45 Sts.5 O.H.5 ER-406 Pt PpPeking

- basion I (51.4) 43.7 54.9 40.5 33.3 41.6 81.1

- basion II (77.2) 66.2 69.3 (57.1) 52.0 61.3 87.2

- opisthion I (15.9) (14.2) 27.6 15.6 11.2 16.3 31.8

- opistbion II (21.3) (19.4) 33.3 (20.6) 16.2 22.1 33.5

frontal bene indicesb recon. Sts.5 SK-48 O.H.5 ER-406 Gorilla PtPeking

- B at post-orb.constrict.(mm) 66.0 64.0 (67.0) 69.4 62.0 69.0 70.5 96.0

- minimum frontal B (mm) - 48.0 (27.0) (25.0) 31.0 44.2 54.7 86.0- fronto-temporal B index - 75.0 40.3 36.0 50.0 64.1 77.4

89.6- superior facial B (mm) 107.0 93.5 (100.0) 115.5 114.0 125.3 106.2 121.0- inner biorbital B (mm) 94.0 84.2 (93.0) 97.0 100.0 105.1 90.0

111.0- fronto-facial B index 62.0 68.4 65.7 60.3 54.4 55.5 66.6

79.3- fronto-biorbital B index 78.6 76.0 72.0 71.5 62.0 66.0 78.4

86.5

rel.H ant.masseter originc recon. Sts.5 SK-48 O.H.5 ER-406 Gorilla PtHomo

- zygomax.-alveolar margin 24.0 32.0 38.3 36.0 40.0 36.4 24.6 18.1- orbitoalveolar H (47.5) 51.0 61.0 75.1 62.0 71.3 51.2 41.3- zm-alv/lorb-alv.index 50. 5 62.7 62.8 47.9 64.5 51.2 48.0 43.8

mandibulad recon. Sts.7 SK O.H.5 Natron Gorilla Pt Homo- ramus H (mm) 55.0 61.0 60.7 65.0 47.0

67.0 43.1 35.9 - ramus B (mm) 55.0 46.8 54.5 - 52.8 62.5 46.4 37.4- H/B % 100.0 130.0 111.4 - 89.0 108.0 92.9

94.7

mandibular fossa e MLD A.rob. O.H.5 G male Pt male Homo- L (mm) 22.7 26.7 27.8 27 25 25.0- B (mm) 30.4 31.9 34.4 46 29 23.8- D (mm) 7.8 9.5 8.7 10 7 14.5- L/B % 74.6 83.5 81.1 58.7 86.3 99.0- D/L % 34.2 35.8 31.2 37.1 27.9 61.4- D/B % 25.5 29.8 25.2 22.1 24.1 60.8

bite forcef recon. Sts.5 SK-48 ER-406 Gorilla Pt PpHomo

- infratemporal fossa (cm²) (16.0) 9.7 (11.0) 18.3 17.5 12.7 7.5 7.2- molar crown are (cm²) 5.38 5.87 5.73 8.92 6.42 3.53 2.45 2.86- bite force equivalent M² 13.9 7.8 12.2 18.0 15.6 10.9 6.6 6.7- bite force equivalent at I 9.2 5.3 9.0 12.0 9.4 6.5 3.9 4.3

incisal microwearg A.afar. Gorilla PtEskimo

- wear striae (/mm²) 4.40 3.02 5.27 6.85- pits (/mm²) 2.17 1.87 3.87 2.17

- pit diameter (mm) .07 .06 .06 .18- wear striation orientation 61° 60° 37° 17°

Table 4A-4B - Legend

H human(like); Pt common chimp(like); Pp pygmy chimp(like); G gorilla(like); G>P, P>G apelike; Pp? like Pt, but possibly even more like Pp (no figures available for Pp);+ very much like ... ; - well outside African hominoid range; B breadth; D depth; H height; L length; recon. reconstruction of large A.afarensis; 333-45 large A.afarensis from A.L.333-45; Sts.5, Sts.7 A.africanus from Sterkfontein; MLD A.africanus MLD-37138 from Makapansgat; SK mean of A.robustus SK-12, SK-23 and SK-34 from Swartkrans; O.H.5, ER-406 A.boisoi from Olduvai and Turkana; Natron from Peninj River; Peking H.erectus; Eskimo H.sapiens. In extant hominoids, measurements are means of males and females, unless mentioned otherwise.

a Kimbel et al., 1984, table 9 e Tobias, 1968, table 1b ibid., table 6 f Demes & Creel, 1988, table 1 and 2c ibid., table 5 g Ryan et al., 1989, table 21d ibid., table 2

Table 4B - Australopiths compared with African hominoids

foramen magnum indicesa 333-45 Sts.5 O.H.5 ER-406(Gorilla??)

- basion I Pp Pp+ Pp Pp+- basion II He Pp Pp Pp>Pt- opisthion I Pp+ Pp He Pp+

- opistbion II Pp+ Pp>Pt He+ Pp

frontal bene indicesb recon. Sts.5 SK-48O.H.5 ER-406 (Pp??)

- B at post-orb.constriction G>P G>P G>P+ G>P+ G>P- minimum frontal B (mm) G>P G- G- G- - fronto-temporal B index P+ G- G- G-- superior facial B (mm) P+ Pp? P H>PG H>PG- inner biorbital B (mm) Pp? Pp? P P>G G>P - fronto-facial B index P+ P+ G>P G>P G+

- fronto-biorbital B index

rel.H ant.masseter originc recon. Sts.5 SK-48 0.H.5ER-406 (Pp?)

- zygomax.-alveolar margin P+ G>P G+ G+ G-- orbitoalveolar H P P+ P>G G G>P- zm-alv/lorb-alv.index G+ G>P- G>P- P+ G>P-

mandibulad recon. Sts.7 SK 0.H.5 Natron(Pp??)

- ramus H (mm) G>P G G G+ P - ramus B (mm) G>P P+ G>P P>G- H/B % H>PG G- G+ P>H

mandibular fossa e MLD A.rob. O.H.5(Pp??)

- L (mm) H=P G G- B (mm) P+ P+ P- D (mm) P G+ G>P- L/B % P P+ P- D/L % G>P+ G+ P- D/B % P>G+ P>G+ P>G+

bite forcef recon. Sts.5 SK-48 ER-406(all)

- infratemporal fossa (cm²) G Pp>t Pt G+- molar crown area (cm²) G G G G- - bite force equivalent M² G HP Pt>G G- bite force equivalent at I G+ H>P G+ G-

incisal microwearg A.afar. (Pp??)

- wear striae (/mm²) P>G- pits (/mm²) H+- pit diameter (mm) G>P+- wear striation orientation G+

Figure 1 - An example of a possible evolutionary tree of fossil hominids

0 Myr BP Gg Pt Pp Hs : : : : Hn : : : He : : : He

1 ? : : He Ab ? : He Ab Ar ? He Ab Ar O.H.62 .

2 Ab . . . ?ER-1470

. . . .

WT-17000 At ? . ?BC-1

: At ? .3 : ?Lucy .

?A.L.333 : :

4 ?Laetoli Gorilla gorilla Pt Pan troglodytes Pp Pan paniscus Ab Australopithecus boisei Ar A. robustus At A. africanus transvaalensis He Homo erectus Hn Homo neanderthalensis Hs Homo sapiens sapiens

DID ROBUST AUSTRALOPITHECINES PARTLY FEED ON HARD PARTS OF GRAMINEAE?

Human Evolution 7: 63-64, 1992

Estimates of bite force suggest that Paranthropus boisei and P. robustus fed on “low-energy food that had to be processed in great quantities”, “a hard object diet”, “food objects... hardand round in shape” (Demes & Creel, 1988). According to studies on molar enamel microwear of South African australopithecines, “Paranthropus ate substantially more hard

food items than Australopithecus” (Grine & Kay, 1988). Studies on incisal microwear suggest that “P. robustus may have ingested foods that required less extensive incisal preparation than the foods consumed by A. africanus” (Ungar & Grine, 1991), but “incisors need not be employed in the manipulation of hard objects” (Ungar & Grine, 1989). However, the precise nature ofthe robust australopithecine diet is still unknown.

A solution may be found in the remarkable parallelism between the dentitions of robust australopithecines, especially P. boisei, and the giant panda, Ailuropoda melanoleuca. In comparison with respectively non-robust australopithecines andnon-panda bears, both have less prognathic faces, relatively smaller incisors and canine teeth, broader and heavier cheek bones, broader molars and premolars and “molarized” premolars,and thicker molar and premolar enamel (Aiello & Dean, 1990; DuBrul, 1977; Grassé, 1955). The heavy grinding apparatus of P. boisei could have been an adaptation for processing, among other things, tough parts of bamboo plants, on which giant pandas almost exclusively feed. The stalks of bamboo and other Gramineae such as sugar cane fit the description of low-energyfood as well as that of hard and round food objects.

P. boisei has been discovered in former lagoons (Carney et al.,1971) and montane forests (Bonnefille, 1976), and P. robustus, near streamside or marsh vegetations (Brain, 1981, p. 189). Insuch environments the bamboo or reed species on which some primates feed are abundant (e.g. MacKinnon, 1978; Glander et al.,1989).

This diet is not as unlikely for a hominid as it may seem.Humans eat grains of different Gramineae (rice, com, wheat), and our closest relatives are known to feed also on harder parts of Gramineae: common chimpanzees like to chew sugar canestalks, and young mountain gorillas love the young shoots of bamboo while the adult males crack the stalks of bamboo (MacKinnon, 1978). Other primates that cat different parts of bamboo are Rhinopithecus roxellana, Cercopithecus mitus kanditi, Callicebus moloch and three Hapalemur species (Glander et al., 1989). An electron microscope study of the enamel surface of the teeth of Gigantopithecus blacki indicates that also this fossil ape, whichdeveloped thick enamel and strongly molarized premolars in parallel with the robust australopithecines, fed partly on Gramineae, possibly bamboo (Ciochon et al., 1990).

It must be possible to test this hypothesis by comparing molar enamel microwear of Gigantopithecus, Paranthropus and Ailuropoda.

References

Aiello L. & Dean C., 1990. Human Evolutionary Anatomy, Academic Press, London.

Bonnefille R., 1976. Implications of pollen assemblage from Koobi Fora Formation, East Rudolf Kenya. Nature, 264: 403-407.

Brain C. K., 1981. The hunters or the hunted? University of Chicago Press, Chicago.

Carney J., Hill A., Miller J. A. & Walker A., 1971. Late australopithecine from Baringo District, Kenya. Nature 230: 509-514.

Ciochon R. L., Piperno D. & Thompson R. G., 1990. Opal phytoliths on the teeth of the extinct ape Gigantopithecus blacki: implications for paleodietary studies. Proceedings of the National Academy of Sciences USA, 87: 8120-8124.

Demes B. & Creel N., 1988. Bite force, diet, and cranial morphology of fossil hominids. Journal of Human Evolution, 17: 657-670.

Du Brul E. L., 1977. Early hominid feeding mechanisms. American Journal of Physical Anthropology, 47: 305- 320.

Glander K. E., Wright P. C., Seigler D. S., Randrianasolo V. &Randrianasolo B., 1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. American Journal of Primatology, 19: 119-124.

Grassé P. P., 1955. Traité de Zoologie, Masson & Cie, Paris, Vol. 1 7.

Grine F. E. & Kay R. F., 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature, 333: 765-768.

MacKinnon J. R., 1978. The ape within us, Collins, London. Ungar P. S. & Grine F. E., 1989. Maxillary central incisor wear in

Australopithecus and Paranthropus. American Journal of Physical Anthropology, 78: 317.

Ungar P. S. & Grine F. E., 1991. Incisor size and wear in Australopithecus africanus and Paranthropus robustus. Journal of Human Evolution, 20: 313-340.

AFRICAN APE ANCESTRY

Human Evolution 5: 295-297, 1990

It is commonly believed that the australopithecines are more closely related to humans than to African apes. This view is hardly compatible with the biomolecular data, which place the Homo/Pan split at the beginning of the australopithecine period. Nothing in the fossil hominid morphology precludes thepossibility that some australopithecines were ancestral to gorillas or chimpanzees and others to humans.

Key words: Hominid evolution, gorilla, chimpanzee, Australopithecus, Lucy, Taung.

It is commonly thought that from a period covering at least the last four million years, no fossils of ancestors of the African apes have been found so far, although hundreds of hominid fossils have been discovered from that period. The usual explanation for this remarkable absence of fossil apes is low fossilisation probability in tropical forests (where the ancestral apes presumably lived).

A more likely solution is that not only man, but also the African apes have descended from the australopithecines (e.g.,Gribbin & Cherfas, 1983; Hasegawa et al., 1985; Edelstein, 1987).The molecular clock leaves little doubt that the man/chimp split occurred between 6 and 4 Myr BP (Hasegawa et al., 1985), which is in the beginning of the australopith period from about 6 (Lukeino, Lothagam) until 1 Myr BP (Taung).

Australopithecines are generally believed to be closer to man than to apes because of their dental and locomotor features. Like man, they have much thicker molar enamel than apes, but enamel thickness has been secondarily reduced in theAfrican apes (Martin, 1987). The robust forms show much smaller anterior teeth than the adult males of G. gorilla and P. troglodytes (differences with the females are less). But bonobos have rather small and only slightly dimorphic canine teeth (Zihlman et al., 1978). Since the prognathism of Negroes comparedwith other humans developed in about 200,000 years (Cann et al., 1987), the evolution of the (indeed much more pronounced) ape prognathism in 1 Myr cannot be considered impossible.

The humanlike orientations of afarensis, distal femoral and tibial articulations (Stern & Susman, 1983), the short iliac bones of Lucy and A. africanus (McHenry, 1982), and the more central foramen magnum in the robust australopiths and Taung are thought to be correlated with bipedality. However, Gribbin& Cherfas (1983), Hasegawa et al. (1985) and Edelstein (1987) have argued that the African apes’ ancestors were more bipedal. Also bonobos have a more central foramen (Kimbel et al.,1984) and frequently walk bipedally (Zihlman et al., 1978).

The mistake of many palaeoanthropologists - the anthropocentric fallacy using «primitive» for «gorilla-» or «chimp-like» - is described by Hasegawa et al. (1985): «It seems to have been widely assumed implicitly that the common ancestor (of man and chimp) was more like the chimpanzee».

Cranial resemblances between australopithecines and apes are listed in Table 1. Also «the Homo like features of Australopithecine limb bones tend to have been greatly exaggerated in the literature (O. J. Lewis, pers. comm.). Mostafarensis postcranials (AL 288, 129, 333) are different from bothhumans and apes, but the scapula, humerus, ulna, knee, hand and foot bones are more like apes (McHenry, 1982; Stern & Susman, 1983; Senut, 1981; Feldesman, 1982; Tardieu, 1986; Sarmiento, 1987; Deloison, 1985).

Lucy’s pelvic girdle AL 288 resembles the apes in some respects (lateral enlargement of iliac blades, small auricularand acetabular articulation surfaces, small lumbosacral angle;McHenry, 1982; Stern & Susman, 1983; Abitbol, 1987), and her upper limb looks rather bonobo-like (Stern & Susman, 1983; Feldesman, 1982). Also A. africanus scapula Sts 7 (McHenry, 1982), its hand bones (TM 1526) and those of A. robustus (SKW 14147, SK 84 and 85) are more chimp than humanlike (Lewis, 1977). The enormous L40-19 ulna of A. boisei is of gorilla size, and morphologically intermediate between man and common chimp (Feldesman, 1982).

Although the picture is confused by the retention of ancestral characters in populations that split not very long before (e.g., large and small A. afarensis) and by parallel evolution (both robust forms lived at the same time), it givesme the following impressions. A. boisei and perhaps some of the larger A. afarensis are closer to Gorilla, while Lucy and the South African australopiths show more affinities with Homo-Pan (but A.robustus, living at the time of KNM-ER 1470, could not belong to

the Homo lineage). The Taung child, which lived even later thanA. robustus, is perhaps ancestral to Pan paniscus or to Pan troglodytes.

Table l - Cranial resemblances of australopiths with apes

The australopith dentition is more apelike in development pattern (Conroy & Vannier, 1987), enamel growth rate (Bromage & Dean, 1985), dental morphology (Johanson & Edey, 1981), and enamel microwear.

All australopithecine brain endocasts appear to be ape rather than humanlike in size and sulcal pattern (Falk, 1985).

The composite A. afarensis skull (mostly AL 333; Kimbel et al., 1984) «looked very much like a small female gorilla» (Johanson & Edey, 1981).

The extensive pneumatization of the AL 333-45 temporal bone is also seen in chimpanzee males and some gorillas; «the pattern of pneumatization in A. afarensis is also found only in the extant apes among other hominoids» (Kimbel et al., 1984).

KNM-WT 17000 had «extremely convex inferolateral margins of the orbits such as found in some gorillas» (Walker et al., 1986).

«The ‘keystone’ nasal bone arrangement suggested as a derived pattern diagnostic of Paranthropus is found in an appreciable number of pongids, particularly clearly in some chimpanzees» (Eckhardt, 1987).

A. robustus incus SK 848 resembles Pan more than Homo and certainly than Gorilla (Fig. 1 in Rak & Clarke, 1979).

A. africanus Sts 5 resembles a bonobo skull (Zihlman et al., 1978). The Taung skull has much more chimp than human traits

(Bromage, 1985) and is indeed much too recent (Partridge, 1985) to be on the line to Homo.

Its «pneumatization has also extended into the zygoma and hard palate. This is intriguing because an intrapalatal extension of the maxillary sinus has only been reported in chimpanzees and robust australopithecines among higher primates» (Conroy & Vannier, 1987).

References

Abitbol M. M., 1987. Evolution of the lumbosacral angle. American Journal of Physical Anthropology, 72: 361-372.

Bromage T. G., 1985. Taung facial remodeling: a growth and development study. In: P. V. Tobias, ed. Hominid Evolution, pp. 239-245,Liss, New York.

Bromage T. G. & Dean M. C., 1985. Re-evaluation of age at death of immature fossil hominids. Nature, 317: 525-527.

Cann R. L., Stoneking M. & Wilson A. C., 1987. Mitochondrial DNA and human evolution. Nature, 325: 31-36.

Conroy G. C. & Vannier M.W., 1987. Dental development of toe Taung skull from computed tomography. Nature, 329: 625-627.

Deloison Y., 1985. Comparative study of calcanei of primates and Pan-Australopithecus-Homo relationships. In: P. V. Tobias, ed. Hominid Evolution, pp. 143-147, Liss, New York.

Eckhardt R.B. Hominoid nasal region polymorphism and its phylogenetic significance. Nature, 328: 333-335.

Edelstein S. J., 1987. An alternative paradigm for hominoid evolution. Human Evolution, 2: 169-174.

Falk D., 1985. Hadar AL 162-28 endocast as evidence that brain enlargement preceded cortical reorganization in hominid evolution. Nature, 313: 45-47.

Feldesman M. R., 1982. Morphometrics of the ulna of some Cenozoic «hominoids». American Journal of Anthropology, 57: 187.

Gribbin J. & Cherfas J., 1983. The monkey puzzle, Triad, Paladin. Hasegawa M., Kishino H, & Yano T., 1985. Dating of the human-ape

splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22: 160-174.

Johanson D. C. & Edey M. A., 1981. Lucy, Granada, London. Kimbel W. H., White T. D. & Johanson D. C., 1984. Cranial

morphology of Australopithecus afarensis: a comparative study based on a composite reconstruction of toe adult skull. American Journal of Physical Anthropology, 64: 337-388.

Lewis O. J., 1977. Joint remodelling and the evolution of the human hand. Journal of Anatomy, 123: 157-201.

Martin L., 1987. Significance of enamel thickness in hominoid evolution. Nature, 314: 260-263.

McHenry H. M., 1982. The first bipeds: a comparison of the A. afarensis and A. africanus postcranium and implications for toe evolution of bipedalism. Journal of Human Evolution, 15: 177-191.

Partridge T. C., 1985. Spring flow and tufa accretion at Taung. In: P. V.Tobias, ed. Hominid Evolution, pp. 171-187, Liss, New York.

Rak Y. & Clarke R. J., 1979. Ear ossicle of Australopithecus robustus. Nature, 279: 62-63.

Sarmiento E. E., 1987. Long bone torsions of the lower limb and its bearing upon the locomotor behavior of australopithecines. American journal ofPhysical Anthropology, 72: 250-251.

Senut B., 1981. Humeral outlines in some hominoid primates and in Pliopleistocene hominids. American journal of Physical Anthropology, 56: 257-283.

Stern J. T. & Susman R. L., 1983. The locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology, 60: 279-317.

Tardieu C., 1986. The knee joint in three hominid primates: application to Plio-Pleistocene hominids and evolutionary implications. In: D. M. Taub & F.A. King, eds. Current Perspectives in primate Biology, pp.182-192, Van Nostrand Reinhold, New York.

Walker A., Leakey R. E., Harris J. M. & Brown F. H., 1986. 2.5-Myr Australopithecus boisei from west of Lake Turkana, Kenya. Nature, 322: 517-522.

Zihlman A.L., Cronin J. E., Cramer D. L. & Sarich V. M., 1978.Pygmy chimpanzee as a possible prototype for the common ancestor of humans, chimpanzees and gorillas. Nature, 275: 744-746.

LETTER TO THE EDITOR

Human Evolution 2: 381, 1987Sir,

The aquatic ape theory states that our hominid ancestors spent a considerable part of their day swimming and diving in a river, lake or sea, and, at least partially, ate aquatic food. The AAT is supported by our lack of body hair, our thickfat-layer and several other features absent in non-human primates, but widespread among aquatic mammals (HARDY 1960, MORGAN 1982, VERHAEGEN 1985).

The ability to speak is a uniquely human character. Innumerable attempts explaining it have been made, but the question how language emerged has not yet been solved. Recently it has been suggested that the origin of speech was facilitated by our aquatic past (MORGAN 1982 pp. 92-105, MORGAN & VERHAEGEN 1986). All aquatic mammals control their breathing “voluntarily”, i.e. through the primary motor cortex. When surfacedthey open the airway whenever they went to inhale air, and they can hyperventilate and then close the airway whenever they intend to dive.

The human primary motor cortex (area 4) is much larger than that of apes, mostly due to the expansion of the areas for the musculature of mouth, throat and breathing. Just in front of that enlarged area 4 lies the typically human Broca’s area. In present-day man, it coordinates the activities of the enlarged area 4, to produce the right sound on the right time.Brcoca’s area may have been originated in a previous aquatic phase to coordinate the muscles commanded by the enlarged area4, to make the right airway muscle contract on the right time:just before, during or just after a dive. In order to use thisvoluntary control for improving his vocalizations, our ancestor must have been able to interpret his own sound production (feedback). This was improved by the evolution of the arcuate fasciculus, a typically human pathway between Broca’s area and Wernicke’s area (GESCHWIND 1972). Wernicke’s area, a primary language area used for decoding spoken language, lies dorsal to primary auditory cortex and to the principal sensoryareas for mouth and throat. In Wernicke’s area, connections could be made with other nearby association areas, and a certain sound or combination of sounds could be associated with something that our ancestor was aware of (hearing, seeing, feeling, doing) at the same time. Compared with a

chimp’s brain, our association areas are enormously enlarged. These areas amplified the possibilities of the sound producingapparatus: they act as the hardware of the computer, whereas the sound analysing and producing areas act as the input/output apparatus; the particular language is the software.

Most authors discussing language origins try to explain our speech capacity by an enormous improvement of vocalizing abilities that already existed in rudimentary form in pre-human primates, but fail to explain how exactly this could have occurred. In my opinion, most of these problems are readily solved by the application of the aquatic theory to thevocal and breathing apparatus.

GESCHWIND N., 1972. Language and the brain. Scient. Amer., 226: 76-83.

HARDY A. C., 1960. Was man more aquatic in the past? New Scient., 7: 642-5.

MORGAN E., 1982. The aquatic ape. London: Souvenir. MORGAN E. & VERHAEGEN M., 1986. In the beginning was the water. New

Scient., 1498: 62-63. VERHAEGEN M., 1985. The aquatic ape theory: evidence and a possible scenario.

Med. Hypoth., 16: 16-32.

POSSIBLE PREADAPTATIONS TO SPEECH:A PRELIMINARY COMPARATICE APPROACH

Marc Verhaegen and Stephen Munro

Human Evolution 19: 53-70, 2004

Abstract

Human language is a unique phenomenon and its evolutionaryorigins are uncertain. In this paper we attempt to explore some of the preadaptations that might have contributed to the origin of human speech.

The comparative approach we use is based on the assumptionthat all features of a species are functional, and that all features can be compared with those of other animals and correlated with certain lifestyles. Using this method we

attempt to reconstruct the different evolutionary pathways of humans and chimpanzees after they split from a common ancestor.

Previous results from comparative studies suggest human ancestors may not have evolved on the open African savannas aswas once believed, but more probably were coastal omnivores feeding on plant matter and easy to catch invertebrates such as shellfish from beaches and shallow waters. Fossil and archaeological data suggest this coastal phase occurred at thebeginning of the Pleistocene, when Homo ergaster-erectus dispersed between East-Africa, North-Africa, South-Asia and Indonesia.

This paper presents comparative data suggesting the various human speech skills may have had their origins at different times and may originally have had different functions. Possible preadaptations to speech include, for instance, musical skills present in a variety of primate species (sound production); airway closure and breath-hold diving for collecting seafood (voluntary breath control); and suction feeding adaptations for the consumption of fruit juiceor certain seafoods (fine control of oropharyngeal movements).The different evolutionary pathways of chimpanzees and humans might explain why chimpanzees lack language skills and why human language is a relatively recent phenomenon.

Key words

Speech origins, language evolution, hominid diet, human evolution, aquatic theory, musical abilities, diving abilities, suction feeding, consonants, Homo erectus, seafoods, comparative biology.

Introduction – Comparative Anthropology

Three major components of human language – phonology, semantics, and syntax – are acquired successively from about the first, the second and the third year of life (Hirsch-Pasek& Golinkoff 1996). This succession may reflect the human linguistic evolutionary stages: pre-language, one-word sentences, and grammatical or ‘true’ language. This paper discusses the first stage, the phonetic pre-adaptations for language, and is based mostly upon comparative data with othermammals.

In constructing human evolutionary models, paleoanthropologists tend to focus on the fossil evidence, but the comparative method (comparing the anatomy, physiology, behaviour, DNA etc. of living animals) is probably more secure, systematic and reliable.

By using the comparative data we adopt an analytical and functionalistic approach. Biological features are generally inherited independently of each other (Mendel’s Laws), due to the crossing-over and independent assortment of chromosomes during gametic reproduction. This recombination of genetic material may not only explain how features can evolve in parallel, i.e., apart from each other, but also why selection,working on different features in parallel in all members of a population, can be so efficient. Since most biological features are polygenetic (influenced by more than one gene) they can be ‘fine-tuned’ through the processes of recombination andselection. All species have gone through an immense period of recombination and selection – not one of all our millions of ancestors died before it had produced fertile offspring – therefore every feature must have had one or more functions. These functions are not always obvious, for instance, featurescan have multiple functions and functions can change over time(evolutionary opportunism), but by comparing the similar features of different species it is often possible to identifygeneral trends and correlations between certain features and particular lifestyles or environments.

The comparative approach can be used for the anatomical, physiological and behavioural features of all animals. According to biomolecular data (DNA and proteins), chimpanzeesare our closest relatives. By comparing the features of humansand chimpanzees, therefore, it may be possible to work back

towards the Last Common Ancestor of Homo and Pan, and attempt to reconstruct its likely habitat and behaviour. It may also be possible to determine which features humans have since acquired, and the type of environmental factors that may have been responsible for these acquisitions.

Perhaps the main drawback of the comparative approach is the insufficient data available for the great majority of species. Many anthropologists, for example, are not particularly familiar with the anatomies, physiologies and behaviours of non-primate species, and have shown a preferencefor the hominid fossil evidence rather than the comparative evidence. However, while the fossil record can provide additional insights, its importance can also be overstated. Fossils are incomplete – typically they are fragmented pieces of bone without soft parts – and are usually of uncertain relation to living species. Frequently, species, age and sex are unknown, and sometimes the geological age and palaeo-environment are uncertain.

In this paper, we first briefly outline the results of ourcomparative studies and present a hypothesis for human evolution: a waterside scenario (Verhaegen & Puech 2000; Verhaegen et al. 2002). Then, more specifically, we compare the anatomy and physiology of the food and airways of humans, chimpanzees and other mammals, provide a list of possible functions, and attempt to determine how and why the human peculiarities associated with speech evolved.

A Waterside Scenario

Most researchers agree that our remote primate ancestors lived in trees, but there is some disagreement as to how humans became independent of trees. Recently, there has been asteady accumulation of evidence suggesting that humans may nothave evolved in a warm and dry environment as was once commonly believed, but instead may have evolved in warm and wet conditions, at the edge between land and water (Hardy 1960; Ellis 1991; Morgan 1997; Bender et al. 1997; Tobias 1998; Verhaegen et al. 2002). Anatomical, physiological, biochemical and palaeo-environmental data tend to support this view. At the 1999 symposium on Water and Human Evolution, in Ghent, Belgium (Vaneechoutte 2000), it was proposed that our ancestors were coastal or riverside omnivores who not only consumed

terrestrial plants and animals, but also collected food from shallow waters. This scenario is supported by a comparison of some typically human features with those of other mammals.- Bipedality: climbing-wading origin? Primates, perhaps because they

are traditionally climbing animals, have a tendency to adoptan erect posture, and this behaviour is accentuated in primate species that frequently wade through shallow water. Proboscis monkeys, for example, cross shallow stretches of water on two legs when moving from one mangrove tree to another (Napier & Napier 1967). Lowland gorillas wade on their hindlimbs through forest swamps in search of wetland plants and sedges (Chadwik 1995; Doran & McNeilage 1997). Dental microwear and isotopic evidence suggest the australopithecine diet may have also included such plants (Puech et al. 1986; Puech 1992; Sponheimer & Lee-Thorp 1999). Therefore it is likely that Pliocene hominids also regularlywaded bipedally in the shallow waters of forest clearings, gallery forests or mangrove areas, possibly in search of floating fruit, wetland plants, reed sedges, fish or shellfish (DuBrul 1977; Ellis 1991; Broadhurst et al. 1998; Verhaegen 1992; Verhaegen et al. 2002). This is corroborated bythe recent discoveries of the 7- to 6-million year-old, probably bipedal-and-climbing, hominids Sahelanthropus tchadensisand Orrorin tugenensis in shallow perilacustrine environments (Brunet et al. 2002; Senut et al. 2001).

- Thick enamel and stone tool use: hard-shelled foods? A combination of thick molar enamel and stone tool use is known to have existed in various Homo species, and exists today in capuchin monkeys and sea otters. Sea otters have large, flatcheekteeth, which resemble those of australopithecines (Walker 1981), and use stones to crack open shellfish while floating on their backs. Capuchins open nuts with stones anduse oyster shells to remove shellfish from the trunks of mangrove trees (Fernandes 1991). Chimpanzees, which have thinner molar enamel, manipulate stones to crack open hard-shelled nuts. Human Pliocene ancestors, perhaps in the same way as mangrove capuchins, might have used stones or other hard objects to remove coconuts from palm trees, to crack hard nutshells, or to remove and open oysters from the trunks of mangrove trees (Verhaegen et al. 2002).

During the late Pliocene or early Pleistocene, members of the genus Homo – as opposed to our more distant relatives the

australopithecines – might have also learned how to duck the head underwater and to dive and collect underwater shellfish as well as other aquatic resources. Humans have much more efficient diving capabilities than nonhuman primates (Schagatay 1996; Morgan 1997; Bender 1999; Verhaegen et al. 2002). Indeed, Homo fossils – as opposed to australopithecines– are typically found near shellfish (Chiwondo, Chemeron, Nariokotome, Zhoukoudian, Boxgrove, Terra Amata, Rabat, Hopefield, Gibraltar and others). Although sea level rises andthe actions of tides and waves have drastically reduced the chances of discovering hominid fossils at sea beaches, Homo erectus remains have been discovered amid shellfish, barnacles and corals, from the early Pleistocene skull of Mojokerto at Java (Ninkovich & Burckle 1978), to the late Pleistocene Acheulean tools of Eritrea (Walter 2000; Walter et al. 2000). Stone tools discovered on Flores suggest Homo erectus crossed a 19 km wide, deep oceanic channel more than 800,000 years ago (Morwood et al. 1998; Tobias 1998). We have argued that the fast dispersal of Homo erectus at the beginning of the Pleistocene between Algeria (Aïn-Hanech), Israel (Yiron, Ubeidya) and Java(Mojokerto) occurred along the Mediterranean and Indian Ocean coasts, where foods could be gathered from both the land and sea (Verhaegen et al. 2002). From the coasts, different Homo sidebranches could have migrated up rivers into the interiors of Africa and Eurasia, where fossilisation chances may have been more likely. Initially restricted to the edges of rivers,swamps and lakes, some Homo populations later moved to areas further from permanent water. Whereas stone tool use for cracking hard-shelled foods may have been a preadaptation for the development of lithic technologies, the diving abilities of our ancestors might have been a preadaptation for the development of voluntary speech (Morgan 1997; Diller 2000).

Like Darwin (1871), however, we believe human sound production probably has deeper roots, beginning at a time whenour ancestors were still arboreal. There may be several overlapping preadaptations for speech, including musical abilities, swallowing abilities, the ability to close the airways, the ability to control breathing, and the ability to communicate symbolically.

A Short Survey of Food- and Airway Adaptations in Mammals

In most animals the mouth is used primarily for feeding, and most oropharyngeal adaptations are directly linked to feeding behaviour (foodway). In amniotes (reptiles, birds, mammals) the nose is primarily for breathing (airway). Sound production outside the water is normally linked to the airway,but for the production of loud sounds a wider space may be advantageous. This is possibly why singing birds and barking dogs make a connection between the airway and the mouth. The traditional functions of the mouth, nose and throat cavities are discussed here under three headings: air, sound and food.

1. AIROn land: All land mammals breathe air through their

nostrils, though some can also inhale and exhale through theirmouths. A number of hypotheses have been put forward to explain the evolutionary function of the human external nose. For example, it has been argued that the human nose is designed to prepare air for breathing: to purify, moisturise, filter or warm it, or to retain water from expired air, etc. (Franciscus & Trinkaus 1988a, 1988b). There are, however, no comparative examples of mammals developing an external nose for similar reasons. The only other primate with a well developed external nose is the mangrove-dwelling proboscis monkey, which is well known for its swimming ability and can swim several metres under water (Napier & Napier 1967).

Most land mammals, as opposed to humans (except babies), have their larynx positioned high in the throat. At rest, the larynx connects with the nasal passage, its entrance well within the nasal cavity, and acts as a barrier separating the nasal passage from the oral cavity. This means most mammals can swallow fluids (and in some species semi-solid materials) and breathe simultaneously (Laitman 1985; Crompton et al. 1997). Some mammals, like red deer and koalas, have a permanently lowlarynx, but have evolved (at least in red deer) a long velum which connects the nasal cavity with the larynx when at rest. Humans have a descended larynx, like koalas and red deer, but lack an elongated velum. Thus, while most mammals, including human babies, can swallow fluids and breathe simultaneously, humans above the age of about six months cannot.

In water: Diving mammals must be able to close their airways underwater. They must also have adaptations that allowfor the considerable water pressure that can be placed upon

air-filled cavities (middle ear, sinuses, bronchi, lungs) and for the great and sudden pressure changes that can be experienced while diving and surfacing. Moreover, they must beable to inhale large amounts of air rapidly when they surface in order to minimise the length of time between dives. It has been argued that some semi- or ex-aquatic mammals, such as tapirs, elephants, hooded and elephant seals, initially evolved elongated external noses to help them breathe and to prevent water from entering the airways while wading or swimming (the human nose seems well designed hydrodynamically to keep water out of the airways while swimming at the surfaceor under water or while dipping the head under water or divinginto water). Most aquatic mammals normally breathe through thenostrils (the whales’ blowhole), although some, like walruses,frequently mouth-breathe (Fay 1982).

Olfaction: Most mammals use the air they breathe for olfaction. In land mammals the sense of smell is very important, but in many aquatic mammals this function has been reduced and in some cases completely lost (Dehnhardt 2002).

Panting: The rapid forcing in and out of air through the mouth is a method used by many mammals (including humans when thermoregulatory sweating does not work well, for instance, invery humid conditions) to help reduce body temperature. In dogs, the velum (soft palate) opens during inhalation and closes during exhalation with each pant cycle (Schmidt-Nielsen& Taylor 1970; Biewener et al. 1985).

2. SOUNDCalls: Sound production is derived from the function of

breathing. Instinctive and territorial sound productions, like barks and roars, are seen in many mammals; humans cry and laugh aloud when stimulated. Many of these ‘automatic’ sounds are reflexes controlled by neural centres in the brain stem. Most are produced by the glottis slit between the vocal folds in the larynx. The lower the larynx during sound production, the louder and more impressive the territorial calls (Fitch 2000; Ohala 2000). An extreme example is the male hammerhead bat, which has an extremely large and low, in fact intrathoracal, larynx (Rosevear 1965). Monkeys, dogs, pigs andall other mammals examined so far, lower the larynx and close the velum during loud vocalisations. In male red and fallow deer, during roaring, and probably also in other mammals during loud calls, the vocal tract has a horizontal (oral) and

vertical (pharyngeal) tube, which is reminiscent of the permanent situation in humans. This two-tube configuration is said to have implications for sound production, the expanded pharynx perhaps allowing humans to produce the full range of speech sounds (Laitman 1985). Many primates, including all hominoids except humans and smaller gibbons, have large laryngeal airsacs, possibly for making their long calls louderor faster or for preventing hyperventilation (Hewitt et al. 2002;Ankel-Simons 2000).

Song: Musicality in animals is often correlated with an arboreal (many birds, some primates) or aquatic (some cetaceans and pinnipeds) lifestyle. The songs of humpback whales are particularly well-known. Primate examples include the pant-hoots of chimpanzees. Male proboscis monkeys, who have longer external noses than females and infants, are said to use the nose as an organ of resonance in vocalization (Ankel-Simons 2000), and even to produce a typical double sound through the nose and mouth at the same time (Napier & Napier 1985). More elaborate songs are seen in some monogamousprimates such as indris, tarsiers, titi monkeys and gibbons (Darwin 1871; Vaneechoutte & Skoyles 1999; Müller & Anzenberger 2002). At least in primates, these sounds appear to be largely under the emotional control of the limbic cortex(Deacon 1997). The songs of birds, as well as mammals, differ according to the population (dialects). Birds typically learn their songs from their fathers during a sensitive period earlyin life (presong).

Speech: Speech production is uniquely human, though some birds, such as mockingbirds and parrots, can mimic human speech (Pepperberg 2000). Human speech sounds are produced by muscles under the voluntary control of the greatly enlarged precentral cortex (Brodmann’s Area 4, the motor cortex that controls fine skeletal muscle movements). Consonants are produced by using the lips, tongue, jaw, velum, pharynx and glottis, although in birds (with inflexible beaks and reduced tongues) these sounds are probably imitated by muscle contractions in the syrinx, the vocal organ, where the right andthe left bronchus come together. The only mammals known so farthat can mimic human utterances, presumably without any understanding of the meaning, was a harbour seal that had learned to produce (albeit with a throaty voice) fragments of humanlike speech from a fisherman, probably at a sensitive

period early in its life (Ralls et al. 1985; Deacon 1997), and toa very limited extent a beluga whale (Eaton 1979). Very variable sounds such as clicks, though not humanlike, are produced by dolphins in the nasal air passages, probably mainly by using the larynx, which, unlike the human larynx, isvery ‘ascended’, i.e. permanently locked in the nasal cavity (Slijper 1958; Dudok van Heel 1970).

3. FOODBiting: The anatomy of the oral cavity in mammals is

probably influenced mainly by its primary function, the processing of food through biting, chewing and swallowing. Many fruit-eaters have spatulated incisive teeth, as do most primates including humans, whereas these are more conical in meat- or insect-eaters (for primates see Ankel-Simons 2000), and can be reduced in terrestrial and aquatic plant-eaters. Terrestrial carni-, insecti- and omnivorous mammals typically have long canines, whereas pure herbivores, including the aquatic sirenians, have reduced or absent canine teeth. Aquatic carnivores such as cetaceans, and to a lesser degree pinnipeds, generally do not have very long canines. All their teeth (front teeth and cheekteeth) tend to be sharp and conical, probably for catching slippery fish or squid. An obvious exception is the walrus, which has long canine tusks probably for intraspecific display (e.g. de Muizon 1995). Large front teeth can be important for attacking sexual rivalsor as a defence against predators, or as a warning signal. It has been argued that showing the front teeth, as is seen in human laughter, can indicate the physical strength, health andself-confidence of an individual.

Chewing: Premolars and molars are for processing the food,for instance, cracking hard foods with thick enamel, chewing calorie-poor plants with flat cheekteeth, cutting through tough plant food or insect exoskeletons with sharp ridges of thin enamel, or slicing meat with the carnassial teeth. Typically, mammals such as ungulates and carnivores, as well as most primates except humans, have low, long and horizontal palates with transversal ridges of cornified epithelium, probably for fixing food while chewing (Romer & Parsons 1977).

Swallowing: As already discussed, in most mammals the larynx at rest is engaged in the nasal cavity, which means that swallowing fluids (mouth to esophagus) and breathing (nose to larynx) at the same time is possible. A permanently

lowered larynx makes this impossible for humans, except babies. Not all kinds of food have to be chewed thoroughly. Asopposed to herbivores, carnivores often swallow large food boluses, which seems to require a large pharyngeal space (laryngeal descent creates a larger pharyngeal space, see figure 1). Foods such as fruit juice and tree exudate (some bats and primates) or insects and grubs (ant-eaters, bears) can be sucked and swallowed without chewing. Some juice- or sap-sucking New World monkeys show features that are believed to increase the suction drainage force, such as an angular andhighly vaulted palate in some marmosets and a humanlike closedupper dental arch with incisiform canines in dusky titis (Hill1957; Hershkovitz 1977; Jones & Anderson 1978). Many pinnipeds, most notably walruses and bearded seals, have roundtongues and smooth vaulted palates, probably to enable them tomore easily suck the smooth and slippery seafoods out of shells (King 1972; de Muizon 1993). Most land mammals, including nonhuman primates, and most aquatic mammals, including hippos, otters and furseals, have palatal ridges, but these are lacking in some cetaceans, crabeater seals, elephant seals and walruses (Roger Crinion, personal communication). The absence of palatal ridges may allow food to slide through the mouth unchewed. The strong suction feeding of walruses probably requires a round and relatively narrow oral cavity and a strong retractable tongue, and possibly an enlarged pharyngeal space and lowered larynx (Fay 1982; de Muizon 1993). Most aquatic mammals can swallow food underwater, although it is not clear which specific adaptations make this possible. In many aquatic mammals such as walruses, sealions and seacows, the epiglottis, the lid that covers the well-developed larynx of humans during swallowing and prevents food entering the trachea, is not as well developed as it is in humans, monkeys, pigs and probably most terrestrial mammals (Negus 1949).

Possible Explanations for the Human-Chimp Differences

Chimpanzees lack an external nose, slitlike nostrils and a philtrum (the vertical furrow in the human upper lip), and have a shorter and more direct air passage from the nostrilsto the nasopharynx than humans (see figures 1 and 2). In humans the nasal air passage is both longer and narrower and

has an inverted U shape (with the nostrils underneath the nose instead of in front).

Chimpanzees have a larger and more protruding mouth (prognathism) with larger canine teeth and corresponding gaps(diastemas) in the opposite jaw, whereas humans have a smaller mouth with everted lips, a closed and parabolic tooth row and teeth of nearly equal height (Hocket 1967; Laitman 1985).

Chimps have a flat tongue and a long and transversally ridged palate, whereas humans have a round, thick and bulbous tongue, a much-shortened oral space and a short, wide, deep palatal ‘vault’. The human tongue can be shaped to fit tightly against the arched and smooth palate.

In chimpanzees, the gap between the palate and larynx is smaller than in humans, who have a tongue bone (hyoid) and larynx “retreated still farther down in the neck” (DuBrul 1958). Humans have a well-developed larynx and very muscularvocal folds, but lack airsacs (Negus 1949).

Humans have a very large representation of the oral muscles in Area 4 (see above), and only in humans does damage of Area4 produce muteness (Deacon 1997). Humans, unlike chimpanzeesand other primates, have an Area 4 representation of the larynx and breathing musculature, have direct fibers connecting Area 4 to the nucleus ambiguus (cortico-ambiguus connections), and can voluntarily control the larynx muscles(nucleus ambiguus) and the breathing muscles (brain stem).

1. SINGING – VOCAL FOLDSBabies of two or three months produce cooing sounds. This

is called vocalising and is performed with the vocal folds in thelarynx, without much oral movement. Soon thereafter, even in deaf children, the babbling starts to include labial consonants,and syllables are produced (consonant plus vowel). In babies older than six months, the sound pattern already resembles thenative language, and ‘dialogues’ with the mother stimulate theutterances. This sensitive period of automatic sound production andthe learning of local dialects resembles the subsong period in birds (Deacon 1997).

The early prelingual sounds, without symbolic meaning, maycorrespond with the elaborate songs of nonhuman primates like gibbons. Music powerfully affects the emotions (anthems, hymns, marches, love songs), and is used by humans as a territorial and pair- or group-binding behaviour, as it is by

other animals. Well-developed musical abilities and duet-singing are seen in monogamous primates such as gibbons. Bonobos (pygmy chimpanzees) engage in group-chorusing and rival males have been observed engaging in vocal duels (De Waal 1997). Some aquatic species such as humpback whales (polygynous) also use complex melodic utterances for territorial behaviour. Interestingly, the harbour seal raised by a fisherman only ‘spoke’ in a humanlike way when it was not engaged in emotional or territorial behaviour (Deacon 1997). It is known that musical training in young children induces anenlargement of the temporal and insular cortex (planum temporale)in the left brain hemisphere, and can lead to an improvement in a child’s ability to hear absolute tones (Schlaug et al. 1995). Intonation is an indispensable element of all spoken languages, and almost half the world’s languages are tonal.

Ohala (2000) argues that our descended larynx could not have evolved as an adaptation for speech, since men, who have an even lower larynx than women, are not better adapted for speech than women, who perform better in verbal tests. In fact, the comparative evidence suggests that laryngeal descentmay have occurred in order to make the voice more impressive (Fitch 2000; Ohala 2000). This, however, does not explain why the human larynx is incapable of making a direct connection from the nasal passage to the larynx and cannot engage in the nasopharynx (intranarial or suprapalatal), as it does in human babies and most land mammals.

2. DIVING – AIRWAYS At birth, humans have a larynx that can engage in the

nasopharynx, then, between four and six months, the larynx begins to descend. One possible explanation for laryngeal descent in humans could be the need to breathe a large amount of air in a short period of time to facilitate diving (Morgan 1997). Whales and dolphins have permanently intranarial larynges, ascended rather than descended.

All humans, probably unlike most nonhuman primates, can easily learn to dive, and several human populations, such as some Indonesian and Oceanic populations, as well as the Ama ofKorea and Japan, collect shellfish through breath-hold diving (Schagatay 1996).

Diving, as seen in aquatic or semi-aquatic mammals, requires a voluntary control of breathing. In contrast with

land mammals, divers must be able to take a deep breath just before they intend to dive, and breathe deeper and faster between dives. They must also be able to hold their breath underwater, paradoxically at the very time when their oxygen needs are highest. In contrast, terrestrial mammals intensify their breathing when they need more oxygen – while running, for example. This may explain why humans are unique among primates in being able to control the larynx and breathing musculature at will.

Diving also requires the complete closure of the airways underwater, so water can be kept out of the lungs. Humans can close the oral (e.g. small mouth with fleshy lips, closed tooth row, bulbous tongue and smooth palate) and nasal passages (e.g. slitlike nostrils, longer and narrower airway) much more completely than chimpanzees can (figure 1). It has been suggested that human ancestors might have been able to close the nostrils by pressing the upper lip (moustached or not) against the nostrils as some people do today when they dive (figure 2). The upper lip with the human philtrum seems “perfectly made for this. The two lines descending from the nose plug up the holes, while the recess in the middle allows for the bridge between the holes” (Peter van de Graaf, in Morgan 1997).

The inverted U shaped nasal passage in humans may have helped to keep water out of the airways while ducking the headunderwater.

3. FEEDING – MOUTH AND TONGUEIt has also been suggested, on the basis of comparative

evidence, that our permanently descended larynx, incapable of engaging in the nasopharynx, might have been a useful adaptation for suction of certain slippery foods or juices (Roger Crinion, personal communication). Animals featuring a descended larynx include not only some deer and koalas that produce loud calls, but also so-called suction feeders such as some bats and perhaps some sap-feeders. It is possible that laryngeal descent allows considerable retraction of the hyoid and tongue so that the pressure in the oral cavity can be lowered, which is one possible way to accommodate underwater suction, as in walruses, or for sucking juicy fruits, as is seen in some bats (Sprague 1943; Rosevear 1965; Hildebrand 1974; Fay 1982).

Other adaptations seen in mammals that regularly suction-feed are a small mouth, a smooth and vaulted palate, and a smooth and round tongue that can be shaped to fit tightly against the palate, as well as a closed parabolic upper tooth row without long canines and diastemas (gaps in the tooth row would hinder suction). These features, in different combinations, are seen in sloth bears, some bats and primates that suck insects, fruit pulp or exudates, and in particular in walruses and other pinnipeds that include shellfish, squid or fish in their diet. These features also typically distinguish humans from apes.

The human sucking adaptations could have been used for fruits and/or for smooth aquatic foods. Humans do not have to chew raw oysters in order to eat them, and are able to swallowsmall fish whole. Moreover, humans can swallow food underwater, and can also keep their mouths open underwater without swallowing or inhaling water. Feeding underwater requires a fine co-ordination of the lips, mouth, tongue and throat in order to keep water out of the airways and, at leastin marine environments, to prevent ingestion of too much seawater. The human tongue is extremely flexible and is well adapted for manipulating objects within the mouth. It is also well designed to help expel water from the mouth.

Some of the mouth-closing and/or feeding adaptations mightexplain why the human tongue is able to close the oral cavity at different places, allowing a diverse number of consonants to be produced, for example, at the alveolar, palatal, velar and uvular articulation places. The only nonhuman mammals, as far as we know, that are able to reproduce recognisable piecesof human speech are the harbour seal (Ralls et al. 1985) and possibly a beluga whale (Eaton 1979).

Concluding Remarks

The combination of comparative and fossil data suggests that by about 1.8 million years ago human ancestors may have become more reliant on wading and diving than on climbing.

A waterside mammal might be expected to have greater control of the lips, tongue and throat muscles for seafood consumption, as well as voluntary control of the airway and breathing musculature for swimming and diving. This oral cavity and airway control might have been preadaptative to theevolution of human speech, particularly in combination with the already well-developed rhythmical, melodic and duetting abilities of our primate ancestors.

A wading-and-diving lifestyle might have also required a different method of communication. Traditional primate communication systems such as smell and certain types of body language (such as posture, for example, though not facial expression) may have been less effective in a semi-aquatic milieu when compared to a purely terrestrial or arboreal one (Morgan 1997). Derek Ellis (personal communication) notes “howwell sound travels over water, compared to being muffled in forests, and even compared to grassland. Foraging beach and lagoon apes could separate quite widely and still remain in contact by vocalising.”

It is possible that the modifications to our ancestors’ food and airway entrances coincided with an early stage in thedisproportionate expansion of the human neocortex, in particular Area 4 (precentral) and Area 44 (Broca), which control the fine movements of the mouth and throat muscles – whether for singing, swallowing or diving. Humans, as opposed to chimpanzees and other primates, have disproportionally large neocortical areas when compared to the brain stem (e.g. Deacon 1997). Of these, the temporal and insular areas (including the Areas 4, 44 and Wernicke), where sounds are produced, processed and interpreted, seem to have undergone the greatest enlargement (Semendeferi & Damasio 2000). Perhapsin this part of the brain, the pre-existing functions of song production, food consumption and airway control were integrated into a system that could produce voluntary and articulated sounds, i.e. the beginnings of speech. The integration of this voluntary sound production system with thesymbolic powers that may have already existed in primates (Savage-Rumbaugh 1986), might have been made possible due to the extra brain tissue (association or integration cortex) that developed during human evolution.

Acknowledgements

We are greatly indebted to Tecumseh Fitch, Elaine Morgan and Roger Crinion for information, corrections and ideas.

References

Ankel-Simons, F. 2000. Primate Anatomy. Academic Press, San Diego.

Bender, R. 1999. Die evolutionsbiologische Grundlage des menschlichen Schwimmens, Tauchens und Watens. Dissertation, University of Bern, Switzerland.

Bender. R., Verhaegen, M. & Oser, N. 1997. Der Erwerb menschlicher Bipedie aus der Sicht der aquatic ape theory.Anthropologischer Anzeiger, 55, 1-14.

Biewener, A., Soghikian, G. & Crompton, A. 1985. Regulation ofrespiratory airflow during panting and feeding in the dog.Respiratory Physiology, 61, 185-195.

Broadhurst, C. L., Cunnane, S. C. & Crawford, M. A. 1998. RiftValley fish provided brain-specific nutrition for early Homo. British Journal of Nutrition, 79, 3-21.

Brunet, M., Guy, F., Pilbeam, D., Mackaye, H. T., Likius, A., Ahounta, D., Beauvilain, A., Blondel, C., Bocherens, H., Boisserie, J.-R., De Bonis, L., Coppens, Y., Dejax, J., Denys, C., Duringer, P., Eisenmann, V., Fanone, G., Fronty, P., Geraads, D., Lehmann, T., Lihoreau, F.,  Louchart, A., Mahamat, A., Merceron, G., Mouchelin, G., Otero, O., Pelaez Campomanes, P., Ponce De Leon, M., Rage,J.-C., Sapanet, M., Schuster, M., Sudre, J., Tassy, P., Valentin, X., Vignaud, P., Viriot, L., Zazzo, A. & Zollikofer, C. 2002. A new hominid from the Upper Miocene of Chad, Central Africa. Nature, 418, 145-151.

Chadwik, D. 1995. Ndoki – last place on earth. National Geogaphic,188, 2-43.

Crompton, A. W., German, R. Z . & Thexton, A. J. 1997. Mechanisms of swallowing and airway protection in infant mammals (Sus domesticus and Macaca fasicularis). Journal of Zoology, 241, 89-102.

Darwin, C. 1871. The descent of man. Appleton, New York.Deacon, T. W. 1997. The symbolic species. Norton, New York.Dehnhardt, G. 2002. Sensory systems. A. R. Hoelzel ed. Marine

mammal biology. Blackwell Publishing, Oxford.de Muizon, C. 1995. Walrus-like feeding adaptation in a new

cetacean from the Pliocene of Peru. Nature, 375, 745-748.De Waal, F. 1997. Bonobo: the forgotten ape. University of California Press.Diller, K. 2000. Why linguists and anthropologists should be

interested in the aquatic ape theory for the origin of speech. J-L. Dessalles & L. Ghadakpour eds. The evolution of language. Ecole Nationale Supérieure des Télécommunications, Paris.

Doran, D. M. & McNeilage, A. 1997. Gorilla ecology and behaviour. Evolutionary Anthropology, 6, 120-130.

Dudok van Heel, W. H. 1970. Dolfijn, hoe doe je het? Van Kampen, Amsterdam.DuBrul, E. L. 1958. Evolution of the speech apparatus. Charles C. Thomas Publications.DuBrul, E. L. 1977. Early hominid feeding mechanisms. American

Journal of Physical Anthropology, 47, 305-320.

Eaton, R. L. 1979. A beluga whale imitates human speech. Carnivore, 2, 22-23.

Ellis, D. 1991. Is an aquatic ape viable in terms of marine ecology and primate behaviour? M. Roede, J. Wind, J. Patrick & V. Reynolds eds. The aquatic ape: fact or fiction? Souvenir, London.

Fay, F. H. 1982. Ecology and biology of the Pacific walrus Odobenus rosmarus divergens. North American Fauna, 74, 1-279.

Fernandes, M. E. B. 1991. Tool use and predation of oysters (Crassostrea rhizophorae) by the tufted capuchin, Cebus apella apella, in brackish water mangrove swamp. Primates, 32, 529-531.

Fitch, T. 2000. Vocal production in nonhuman mammals: implications for the evolution of speech. J-L. Dessalles &L. Ghadakpour eds. The evolution of language. Ecole Nationale Supérieure des Télécommunications, Paris.

Franciscus, R. G. & Trinkaus, E. 1988a. The Neanderthal nose. American Journal of Physical Anthropology, 75, 209-210.

Franciscus, R. G. & Trinkaus, E. 1988b. Nasal morphology and the emergence of Homo erectus. American Journal of Physical Anthropology, 75, 517-527.

Hardy, A. C. 1960. Was man more aquatic in the past? New Scientist, 7, 642-645.

Hershkovitz, P. 1977. New World monkeys (Platyrrhini), Volume 1. University Press, Chicago.

Hewitt, G., MacLarnon, A. & Jones K. E. 2002. The functions ofthe laryngeal air sacs in primates: a new hypothesis. Folia Primatologica, 73, 70-94.

Hildebrand, M. 1974. Analysis of vertebrate structure. Wiley, New York.Hill, W. C. O. 1957. Primates: Comparative anatomy & taxonomy,Volume III: Hapalidae. University Press, Edinburgh.Hirsch-Pasek, K. & Golinkoff, R. M. 1996. The origins of grammar.

MIT, Cambridge, Mass. Hocket, C. F. 1967. The foundations of language in man, the

small-mouthed animal. Scientific American, 217, 141-144.Jones, C. & Anderson, S. 1978. Callicebus moloch. Mammalian Species,

112, 1-5.King, J. 1972. Observations on phocid skulls. R. J. Harrison

ed. Anatomy of marine mammals, Volume 1. Academic Press, New York.

Laitman, J. T. 1985. Evolution of the hominid upper respiratory tract: the fossil evidence. P. V. Tobias ed. Hominid evolution: past, present and future. Liss, New York.

Morgan, E. 1997. The aquatic hypothesis. Souvenir, London. 392Morwood, M. J., O’Sullivan, P. B., Aziz, F. & Raza, A. 1998.

Fission-track ages of stone tools and fossils on the east Indonesian island of Flores. Nature, 392, 173-176.

Müller, A. E. & Anzenberger, G. 2002. Duetting in the titi monkey Callicebus cupreus: structure, pair specificity and development of duets.Folia Primatologica, 73, 104-115.

Napier, J. R. & Napier, P. H. 1967. A handbook of lving primtes. Academic Press, New York.Napier, J. R. & Napier, P. H. 1985. The natural history of the primates.

MIT, Cambridge, Mass.Negus, V. E. 1962. The comparative anatomy and physiology of the larynx.

Hafner, New York.Ninkovich, D & Burckle, LH 1978. Absolute age of the base of the hominid-bearing bed in Eastern Java. Nature, 275, 306-308.

Ohala, J. J. 2000. The irrelevance of the lowered larynx in modern Man for the development of speech. J-L. Dessalles &L. Ghadakpour eds. The evolution of language. Ecole Nationale Supérieure des Télécommunications, Paris.

Puech, P-F. 1992. Microwear studies of early African hominid teeth. Scanning Microscopy, 6, 1083-1088.

Puech, P-F., Cianfarani F. & Albertini H. 1986. Dental microwear features as an indicator for plant food in earlyhominids: a preliminary study of enamel. Human Evolution, 1,507-515.

Pepperberg, I. M. 2000. The Alex studies: cognitive and communicative abilities of grey parrots. Harvard University Press, Cambridge, Mass.

Ralls, K., Forelli, P. & Gish, S. 1985. Vocalizations and vocal mimicry in captive harbor seals, Phoca vitulina. Canadian Journal of Zoology, 63, 1050-1056.

Romer, A. S. & Parsons, T. S. 1977. The vertebrate body. Saunders, Philadelphia.

Rosevear, D. R. 1965. The bats of West Africa. British Museum, London.

Savage-Rumbaugh, S. 1986. Ape languages: from conditioned response to symbol. Columbia University Press, New York.

Schagatay, E. 1996. The human diving response: effects of temperature and training. Dissertation, University of Lund, Sweden.

Schlaug, G., Jäncke, L., Huang, Y. & Steinmetz, J. 1995. In vivo evidence of structural brain asymmetry in musicians. Science, 267, 699-701

Schmidt-Nielsen, K. B. W. & Taylor, C. R. 1970. Panting in dogs: unidirectional airflow over evaporative surfaces. Science, 169, 1102-4.

Semendeferi, K. & Damasio, H. 2000. The brain and its main anatomical subdivisions in living hominoids using magneticresonance imaging. Journal of Human Evolution, 38, 317-332.

Senut, B., Pickford, M., Gommery, D., Mein, P., Cheboi, K. & Coppens, Y. 2001. First hominid from the Miocene (Lukeino Formation, Kenya). Comptes Rendus de l’Academie de Sciences de Paris, Series IIa (Sciences de la Terre et des planètes), 332, 137-144.

Slijper, E. J. 1958. Walvissen. Centen’s Uitgeverij, Amsterdam. Sponheimer, M. & Lee-Thorp, J. A. 1999. Isotopic evidence for

the diet of an early hominid, Australopithecus africanus. Science, 283, 368-370.

Sprague, J. M. 1943. The hyoid bone region in placental mammals. American Journal of Anatomy, 72, 385-472.

Tobias, P. V. 1998. Water and Human Evolution. Out There, 35, 38-44. <http://allserv.rug.ac.be/~mvaneech/outthere.htm>

Vaneechoutte, M. 2000. Water and human evolution. Human Evolution, 15, 243-251. <http://allserv.rug.ac.be/~mvaneech/Symposiu m .h tml>

Vaneechoutte, M. & Skoyles, J. 1999. The memetic origin of language: humans as musical primates. Journal of Memetics, 2. <http://allserv.ru g .ac.be/~mvaneech / ORILA.FIN.html >

Verhaegen, M. 1992. Did robust australopithecines partly feed on hard parts of Gramineae? Human Evolution, 7, 63-64.

Verhaegen, M. & Puech, P.-F. 2000. Hominid lifestyle and diet reconsidered: paleo-environmental and comparative data. Human Evolution, 15, 175-186.

Verhaegen, M., Puech, P.-F. & Munro, S. 2002. Aquarboreal ancestors? Trends in Ecology and Evolution, 17, 212-217.

Walker, R. 1981. Diet and teeth – dietary hypotheses and humanevolution. Philosophical Transactions of the Royal Society London B, 292, 57-64.

Walter, R. 2000. Out of Africa. <http://www.exn.ca/h o minids/outofafrica.cf m >

Walter, R. C., Buffler, R. T., Bruggemann, J. H., Guillaume, M. M. M., Berhe, S. M., Negassi, B., Libsekal, Y., Cheng, H., Edwards, R. L., von Cosel, R., Néraudeau, D. & Gagnon,D. 2000. Early human occupation of the Red Sea coast of Eritrea during the last interglacial. Nature, 405, 65-69.

Table 1 -- Nose-Mouth-Throat Differences with Chimps Human feature + additional

descriptionPossible function(s) originally

External nose

long, narrow nose passage

Keeping water out of airways? Sexual selection?? Resonance??

Inferior nostrils

human philtrum in upper lip

Keeping water out? Nose closure (figure 2)? Acoustic??

Smaller mouth

with red everted lips

Mouth closure. Suction of fruits? of seafood? Sexual selection??

Vaulted palate

with parabolic toothrow

Food suction, e.g. fruits? seafood? Underwater??

Round tongue

fits nicely in palate

Chewing & swallowing. Food suction? Vocalisation?

Smooth palate

less transversal ridges

Swallowing smooth and slippery seafood? Suction?

Very low larynx

no intranarial engagement

Vocalisation? Suction? Large intake of breath?Choking danger!

Mobile larynx

large pharyngeal space

Vocalisation? Suction? Swallowing large food boluses?

Flexible glottis

very muscular vocal folds

Singing (tone height). Glottis closure for diving??

Mouth breathing

under volitional control

Diving? Singing? Speaking?

Baby babbling

song: sensitive period

Singing? Speaking?

Table 2 -- Possible Explanations of the Human-Chimp Differences

Song? Seafood? Diving?Abilities

. Tone & rhythm

. Duetting. Smooth & slippery. Swallowing underwater??

. Voluntary breathing

. Airway closure

Human vs. chimpfeatures

. vocal folds very muscular

. sensitive period &babbling

? lower larynx & louder calls

? mobile larynx? no laryngeal

? small mouth & fleshy lips

? smooth palate with less ridges

? vaulted palate & round tongue

? mobile hyoid & larynx? large pharynx

? small mouth & evertedlips

? philtrum & slitlike nostrils

? long & narrow nasal passage

? round tongue, smooth palate

airsacs ?? laryngeal descentAnimal examples

. Musicality: many birds; gibbon, titi, tarsier, indri; humpback whale

. Speech imitation: some birds, harbour seal

. Suction feeding: sloth bear; walrus & other pinnipeds; some primates & bats

. External nose: proboscis monkey, tapir, elephant,

hooded & elephant seal

. Airway closure & voluntary

breathing in divingmammals

Secondary use in speech

. Tone, intonation

. Rhythm

. Dialogue

. Sound imitation

. Extreme lip, tongue &pharynx control; dental, palatal etc. closures easy (not only labial)

. Click sounds

. Breathing muscles: voluntary in- & expiration

. Airway closures at lips, tooth row, palate, velum, glottis…

Figure 1 –

Midsagittal Section through the Heads of a Chimpanzee and a Human (after Laitman1985). Note the protruding nose and chin, the round tongue and short, vaulted, smooth palate, and the lowered larynx in humans.

Figure 2 –

Possible Function of Upper Lip and Philtrum: Closing the Nostrils (after Morgan 1997). Note that human ancestors were more prognathous, and possibly had moustaches, so that the upper lip was closer to the nostrils.

HOMINID LIFESTYLE RECONSIDERED:PALEO-ENVIRONMENTAL AND COMPARATIVE DATA

Marc Verhaegen and Pierre- François Puech

Human Evolution 15: 151-162, 2000

It is traditionally believed that human ancestors evolved in awarm and dry environment. The available evidence, however, favours the vision that it happened in a warm and wet environment. The paleo-environmental data suggest that the early australopithecines Australopithecus anamensis, afarensis and africanus lived in warm, moist, and wooded landscapes such as gallery forests. In the Pleistocene, the robust australopithecines A. robustus and boisei seem to have dwelt in more open, possibly cooler and generally dryer places, in the vicinity of shallow and relatively stagnant waters of lakesides, lagoons, marshes and riverbanks. Dental and microwear studies suggest that the australopithecines, more than Western lowland gorillas, regularly fed on aquatic herbaceous vegetation (AHV).

Homo fossils, on the other hand, as suggested by the paleo-environmental data, are more frequently discovered near lakes,seas and rivers where molluscs were abundant. Shellfish could provide a dietary supplement for their frugivorous diet. This is how early hominines might have learned to use stones to crack bivalves. This subsequently could have led to stone tooluse for other purposes.

Key words: Hominids, australopithecines, enamel thickness, microwear, bipedalism, tool use, palaeo-environment, savanna theory

INTRODUCTION

The savanna hypothesis of human evolution was strongly promoted by Professor Dart in 1924 after the discovery of the skull of Taung in South Africa’s treeless grasslands. He wrote(1925):

‘South Africa, by providing a vast open country with occasional wooded belts and a relatively scarcity of water,together with a fierce and bitter mammalian competition, furnished a laboratory such as was essential to this penultimate phase of human evolution.’

And:‘It will appear to many a remarkable fact that an ultra-simian and pre-human stock should be discovered, in the first place, at this extreme southern point in Africa, and,secondly, in Bechuanaland, for one does not associate with the present fringe of the Kalahari desert an environment favourable to higher primate life. It is generally believedby geologists (vide A. W. Rogers, “Post-Cretaceous Climates of South Africa,” African Journal of Science, vol. xix., 1922) that the climate has fluctuated within exceedingly narrow limits in this country since Cretaceous times.’

While we now known that the South African climate did change since the time of Taung (Partridge, 1985), Dart was thus convinced that the present and the ancient environment did notdiffer significantly and that the Taung child had lived in such open grasslands. Dart only got recognition a few decades later. Piltdown Man (rather big brain and big teeth) was unmasked as a fraud and anthropologists accepted the Taung fossil (small brain, small teeth) as a more likely link

between apes (small brain, big teeth) and humans (big brain, small teeth). However, they not only accepted Dart’s view on Taung’s affinity, but also his view on Taung’s lifestyle in a dry and open country. While many anthropologists today no longer automatically follow the savanna hypothesis (e.g. Tobias, 1995; Wood, 1996), the idea remains unquestioned in most popular books.

However, a savanna past of humans is comparatively and physiologically improbable, since humans in most respects differ from savanna-dwellers (e.g. Schmidt-Nielsen, 1979; Morgan, 1982, 1990; Verhaegen, 1991, 1997). In a comparison ofhumans with apes, arboreal, semi-aquatic, fully aquatic and savanna mammals (Verhaegen, 1993), not one feature distinguishing the savanna mammals was found in humans. Mammals of dry, warm and open landscapes are relatively independent of drinking-water and water-containing nourishment, have a high tolerance of dehydration and radiation heat, have high diurnal body temperatures and high daily temperature fluctuations, and high renal concentration power. They usually have very large external ears, a slender build, and running velocities of 30 miles per hour and more. They are unguli- or digitigrade, not plantigrade like opossums, bears, racoons, eared seals or African hominoids. Most of them do not have dextrous hands like racoons, many otters and primates. They never have abundant fat tissues under the skin like humans, but protect themselves from the sun with fur (or with dust coverings in elephants or rhinoceroses). Their vocalisations are less varied than those of dolphins, otters or primates are. They never copulate face to face as some slow branch-hangers (sloths, pottos, orang-utans), marine mammals (cetaceans, sirenians) and humans do. All have an excellent sense of smell, as opposed to many marine mammals and humans. Most of them grow up fast and reachadulthood in less than three years. They often sustain body temperatures of more than 40°C (Grant’s gazelle can maintain 46°C for many hours) and show temperature fluctuations of morethan 6° between day and night. Their urine concentration can be twice that of humans and more. They can bear a dehydration of 20 per cent, whereas in humans a dehydration of more than 10 per cent is fatal without medical intervention. They are very conservative with salt and water (many savanna mammals, even carnivores like the fennec fox, do not need drinking-

water), and they never sweat ten to fifteen litres a day as humans can do in hot environments (hunting-dogs and many othersavanna-dwellers do not sweat at all).

Recently, anthropologists are appreciating these data: ‘physiologically, biochemically and histologically, we should be hopeless as savanna-dwellers. All of the former savanna supporters must swallow our earlier words’ (Tobias, 1995). Since humans differ strongly from such animals, a thorough reconsideration of the available fossil data is necessary. Ourdiscussion will be mainly based on the paleo-environmental evidence and on the dental and microwear evidence of hominids.

PALEO-MILIEU

Not only the Taung cranium, but most hominid fossils - from a time span covering at least the last six million years - have been found in varied, but consistently wet environments: in humid forested areas or in the immediate proximity of abundant water collections at the time. However, there are the well-known difficulties of paleo-ecological reconstructions (Shipman & Harris, 1988): ‘taphonomic events […] may selectively destroy or distort the fossil record and the association among species’; animals ‘may stray out of their preferred habitats into other areas’; ‘habitats are often complex and mosaic’; ‘ecological zones or habitats [migrate] across basins in response to climatic and other fluctuations’; and, most importantly, ‘depositional variables […] bias the fossil record by sampling a disproportionate number of habitats related to water (e.g. lake margins, streams, channels, deltas) and by failing to sample many open-country habitats farther away from water sources’. Indeed, that many hominid fossils have been discovered in such places by no means proves that they actually lived there. However, it certainly does not exclude it.

The following list confirms the comparative evidence that it is rather improbable that the hominids ever lived in a savanna milieu, and provides a more shaded picture. Lukeino KNM-LU 335 “pre-australopithecine”: ‘The red beds

seems to contain marginal lacustrine deposits as indicated by the presence of algal mats and lacustrine bivalves (including complete specimens with valves in the closed position)’ (Pickford, 1975).

Tabarin KNM-TH 13150 “pre-australopithecine”: ‘The fauna includes aquatic animals such as molluscs, fish, turtles, crocodiles, and hippotami, along with others that might be found in the vicinity of a lake of river’ (Ward & Hill, 1987).

Ardipithecus ramidus: ‘Sedimentological, botanical and faunal evidence suggests a wooded habitat for the Aramis hominids […] Aquatic elements (turtle, fish, crocodile) are rare. Large mammals (hippopotamus, proboscideans, rhinos, equids, giraffids, bovines) are rare. Primates are very abundant’ (WoldeGabriel et al., 1994); ‘[…] interpreted to have been aclosed woodland. At Aramis, aquatic species and large mammals are rare, and colobines make up over 30% of all vertebrate specimens collected’ (Leakey et al., 1995).

Kanapoi KNM-KP 29281 Australopithecus anamensis: Fish, aquatic reptiles, kudus and monkeys are prevalent. ‘A wide gallery forest would have almost certainly been present on the largeriver that brought in the sediments’ (Leakey et al., 1995).

Chad KT 12 A. cf. afarensis: ‘The non-hominid fauna contains aquatic taxa (such as Siluridae, Trionyx, cf. Tomistoma), taxaadapted to wooded habitats (such as Loxodonta, Kobus, Kolpochoerus) and to more open areas (such as Ceratotherium, Hipparion) […] compatible with a lakeside environment’ (Brunetet al., 1995).

Garusi-Laetoli L.H. A. anamensis or afarensis: Teeth and mandiblefragments, the hardest skeletal parts which are frequently left over by carnivores (Morden, 1988), come from wind-blownand air-fall tuffs (Leakey et al., 1976). Cercopithecine andcolobine monkeys are present (Protsch, 1981; Leakey et al., 1976).

Hadar, Afar Locality: ‘Generally, the sediments represent lacustrine, lake margin, and associated fluvial deposits related to an extensive lake that periodically filled the entire basin’ (Johanson et al., 1982)

Hadar AL.333 A. afarensis: ‘The bones were found in swale-like features […] it is very likely that they died and partially rotted at or very near this site […] this group of hominids was buried in streamside gallery woodland’ (Radosevich et al., 1992).

Hadar AL.288 gracile A. afarensis: Lucy lay in a small, slow moving stream. ‘Fossil preservation at this locality is excellent, remains of delicate items such as crocodile and

turtle eggs and crab claws being found’ (Johanson & Taieb, 1976).

Makapan A. africanus: ‘[…] very different conditions from thoseprevailing today. Higher rainfall, fertile, alkaline soils and moderate relief supported significant patches of sub-tropical forest and thick bush, rather than savannah. Taphonomic considerations […] suggest that sub-tropical forest was the hominins’ preferred habitat rather than grassland or bushveld, and the adaptations of these animals was therefore fitted to a forest habitat’ (Rayner et al., 1993; see also Reed, 1993; and Wood, 1993).

Taung australopithecine: ‘the clayey matrix from which the Taung cranium was extracted, and the frequent occurrence of calcite veins and void fillings within it (Butzer, 1974, 1980) do suggest a more humid environment during its accumulation’ (Partridge, 1985).

Sterkfontein A. africanus and Swartkrans A. robustus: Many South African australopithecines are discovered in riverside caves, presumably often filled with the remainders of the consumption process of large felids (Brain, 1981).

Kromdraai: A. robustus was found near grassveld and streamside or marsh vegetation, in the vicinity of quail, pipits, starlings, swallows, and parrots, lovebirds and similar psittacine birds (T. N. Pocock in Brain, 1981).

Turkana KNM-ER 17000 and 16005: A. aethiopicus was discovered near the boundary between overbank deposits of large perennial river and alluvial fan deposits, amid water- and reedbucks (Walker et al., 1986).

Lake Turkana: ‘The lake margins were generally swampy, with extensive areas of mudflats […] Australopithecus boisei was more abundant in fluvial environments, whereas Homo habilis was rare in such environments […] Australopithecus fossils are more common than Homo both in channel and floodplain deposits. The gracile hominids […] seem to be more restricted ecologically to the lake margin than are the robust forms’ (Conroy, 1990).

Ileret A. boisei: ‘the fossil sample reflects climatic and ecological environmental conditions differing significantly from those of the present day. At Ilerat, 1.5 Myr ago, climatic conditions must have been cooler and more humid than today, and more favourable to extensive forests […] Theprominence of montane forest is particularly striking […]

dominated by Gramineae and Chenopodiaceae appropriate to themargins of a slightly saline or alkaline lake’ (Bonnefille, 1976).

Konso A. boisei: ‘The highly fossiliferous sands at the mid-section of KGA10 are interpreted to be the middle to distal portions of an alluvial fan, deposited adjacent to, and extending into, a lake. Fossils and artefacts deriving from horizons of sands and silts are not abraded and show evidence of minimal transport. A large mammalian assemblage has been collected from the deposits, showing a striking dominance of Alcelaphini […] to indicate the presence of extensive dry grasslands at KGA10’ (Suwa et al., 1997).

Chesowanja A. boisei: ‘The fossiliferous sediments were deposited in a lagoon […] Abundant root casts […] suggest that the embayment was flanked by reeds and the presence of calcareous algae indicates that the lagoon was warm and shallow. Bellamya and catfish are animals tolerant of relatively stagnant water, and such situation would also be suitable for turtles and crocodiles’ (Carney et al., 1971).

Olduvai middle Bed I: A. boisei O.H.5 as well as habilis O.H.7 andO.H.62 were found in the most densely vegetated, wettest condition, with the highest lake levels (Walter et al., 1991), near ostracods, freshwater snails, fish, and aquatic birds (Conroy, 1990); ‘[…] the middle Bed-I faunas indicate a very rich closed woodland environment, richer than any part of the present-day savanna biome in Africa […]’ (Fernández-Jalvo et al., 1998). ‘Fossilized leaves and pollen are rare in the sediments of Beds I and II, but swampvegetation is indicated by abundant vertical roots channels and casts possibly made by some kind of reed. Fossil rhizomes of papyrus also suggest the presence of marshland and/or shallow water’ (Conroy, 1990). ‘[…] Cyperaceae fruitswere common in H. habilis habitat (Bonnefille, 1984). Ancient Egyptians ate Cyperus papyrus root which was also present at Olduvai in swamp-margins and river banks’ (Puech, 1992).

Olduvai O.H.24 habilis: ‘Crocodile remains predominate among the faunal material from this site and more than 2,000 teethwere found. Tortoise plates, shells of Urocyclid slugs, fishvertebrae and scales, bird bones and pieces of ostrich eggshell were also relatively common (Leakey et al., 1971).

Malawi UR 501 early Homo: ‘The Plio-Pleistocene Chiwondo Beds of Northern Malawi have yielded molluscs and fragmented

remains of fish, turtles, crocodiles and large mammals […] Microvertebrates and carnivores are virtually unrepresented in the assemblage […] The general ecological setting of the Malawi Rift during the Late Pliocene was a mosaic environment including open and closed, dry and wet habitats,and which harbored a small and ecologically unstable paleolake Malawi’ (Schrenk et al., 1995).

Chemeron KNM-BC1 early Homo: ‘The Fish Beds […] seem to be almost entirely lacustrine and fluviatile; fish remains are abundant […] Molluscs also lived in the lake, and locally their remains accumulate to form shelly limestones’ (Martyn & Tobias, 1967).

Turkana Boy KNM-WT 15000 H. erectus: ‘Mammalian fossils are rare at this locality, the most abundant vertebrate fossils being parts of small and large fish. The depositional environment was evidently an alluvial plain of low relief […] Typical lacustrine forms (for example, ostracods, molluscs) could invade the area […] The only other fauna found so far in the fossiliferous bed are many opercula of the swamp snail Pila, a few bones of the catfish Synodontis andtwo fragments of indeterminate large mammal bone […]’ (Brownet al., 1985).

Mojokerto H. erectus: ‘The basal part of the Putjangan Beds is composed of volcanic breccias containing marine and freshwater molluscs. The rest of the Putjangan Beds is composed of black clays of lacustrine origin’ (Ninkovich & Burckle, 1987).

Peking H. erectus: ‘A big river and possibly a lake were located to the east and contained various water species; along the shorelines grew reeds and plants, which were home for buffalo, deer, otters, beavers and other animals’ (Poirier, 1978); ‘[…] accumulation in quiet water. The cave at this time was probably the locus of ponded water and was probably more open to the atmosphere’ (Weiner et al., 1998).

Hopefield, Rabat & Terra Amata: H. erectus fossils came from sandstone made up from dune sand resting upon a former sea beach (De Lumley, 1990). In Terra Amata, ‘there are also indications that the inhabitants ate oysters, mussels and limpets – shells of which are present. The presence of fish bones and fish vertebrae indicate that the population also fished’ (Poirier, 1987).

AUSTRALOPITHECINE LIFESTYLE

The list shows that some very early hominids, more than later australopithecines, have been found near lacustrine molluscs (Lukeino and Tabarin ca. 6.5 and 5 Myr BP). Ardipithecus ramidus, supposedly another early hominid, must have lived in awooded habitat, amid predominantly colobine monkeys (Aramis ca. 4.5 Myr BP). Pliocene australopithecines ca. 4-3 Myr BP apparently frequently dwelt in warm and humid, more or less closed environments (gallery forest or wooded habitat in Kanapoi, Chad, Hadar, Makapansgat, but inconclusive for Garusi-Laetoli). Pleistocene robust australopithecines since 2.5 Myr BP probably lived in generally dryer and more open landscapes (grassland in Kromdraai and Konso), but their remains lay in riverbanks, lagoons, marshes, lake-margins, near papyrus (Olduvai) and reed (Kromdraai, Olduvai, Chesowanja).

Although ‘all nine Konso A. boisei specimens were recovered among the predominantly dry grassland fauna of KGA 10’ (Suwa et al., 1997), this does not mean that they lived in a savannamilieu, since ‘nearby subsites were also moist and wooded’ (Delson, 1997). Fragmentary fossils like those of Laetoli and Konso are often the remains of carnivore meals (Morden, 1988).Leopards, which preyed upon australopithecines, prefer to feedin dry circumstances and therefore drag away their prey, sometimes several hundred meters (Brain, 1981).

The preponderance of wet environments in our list is striking, but this was not considered to be inconsistent with a savanna view, because it was believed that the fossil recordsampled a disproportionate number of habitats related to water(see the above citation from Shipman and Harris, 1988). To be sure, that the hominids have been discovered in humid or wet habitats does not allow firm conclusions about how much time they spent there, but the possibility that wetter rather than drier conditions influenced hominid evolution can not be ignored. Therefore, paleo-ecological data must be verified andsupplemented through anatomical and especially dental studies of the fossils.

It is generally agreed that all australopithecines have skeletal features of bipedality. Early graciles also show clear indications of tree climbing such as curved manual and

pedal phalanges, though such features are less obvious in the robusts.

Dental studies suggest that whereas gracile australopithecines preferred softer fruits and vegetables, therobusts’ diet included harder food items (e.g. Robinson, 1954;Du Brul, 1977; Walker, 1981; Puech, 1992; Lee-Thorp et al., 1994). Estimates of robust australopithecine bite force suggest ‘low-energy food that had to be processed in great quantities’ and food objects ‘hard and round in shape’ (Demes & Creel, 1988). Du Brul (1977) noticed dental parallelisms between the robust australopithecines and the bamboo-eating giant panda Ailuropoda melanoleuca (broad, high and heavy cheekbones, reduced prognathism and front teeth, broad back teeth, premolar molarisation), as opposed to gracile australopithecines, respectively non-panda bears.

Papyrus and reed were present in the paleo-environment of the later australopithecines (e.g. Olduvai, Chesowanja, Kromdraai), and Cyperaceae and Gramineae are part of the diet of living African hominoids. Gorillas eat sedges and bamboo shoots and stalks, gorillas and chimpanzees eat cane, chimps and humans eat water lilies, and rice and other cereals are staple food for humans. Supplementing their diet with parts ofgrasslike plants might have been enabled the robusts to bridgethe dry season, when fruits and soft vegetables were scarce.

Studies of dental enamel microwear provide other details. In the early australopithecines of Garusi-Laetoli and Hadar (A. afarensis 4-3 Myr BP), the cheekteeth enamel has a polished surface and the microwear looks like that of the capybara Hydrochoerus hydrochaeris and that of the mountain beaver Aplodontia rufa (Puech et al., 1986). These animals are semi-aquatic rodents that feed mainly on sappy marsh and riverside herbs, grasses and bark of young trees. It has recently become clear that Western lowland gorillas G. g. gorilla spend some time eating aquatic herbaceous vegetation (AHV) like Hydrocharitaceae herbs and Cyperaceae sedges (Doran & McNeilage, 1997).

Comparisons of molar enamel in South African fossils show that A. robustus ate substantially more hard food items than A. africanus (Grine & Kay, 1988). Incisal microwear suggests that A. robustus may have ingested foods that required less extensive incisal preparation than the foods consumed by A. africanus, such as fruits (Ungar & Grine, 1991), and ‘incisors need not be

employed in the manipulation of hard objects’ (Ungar & Grine, 1989).

The enamel of the East African robusts (Olduvai and Peninj) displays more pits, wide parallel striations and deep recessed dentine, resembling that of the beaver Castor fiber, thateats riverine and riverside herbs, roots of water lilies, barkand woody plants in a temperate climate. ‘Many food plants growing in marsh land and indeed many grasses, have high concentrations of siliceous particles known as opal phytoliths. The consumption of such foods produces a great deal of wear, and the enamel and dentine have a blunted appearance. Ancient Egyptians ate papyrus shoots (Puech et al., 1983b) and we suppose that [O.H.16] did the same with swamp margin plants’ (Puech, 1992). Whereas the East African robusts seem to have had aquatic plants and papyrus shoots in their diet and ate more woody plants than the earlier australopithecines, habilis O.H.16 apparently supplemented the AHV of the earlier australopithecines with acid fruits (Puech,1984). In the habilis cheekteeth, the margins of the striae have been polished and slightly etched, resembling the microwear ofthe coypu Myocastor coypus. This rodent feeds on reed, sedges, marsh plants, fruits and molluscs in river and lake margins. It thus seems that an early australopithecine diet of fruits (larger front teeth) and AHV (polishing) was supplemented withunripe fruits (acid etching) in habilis, and with woody plants inthe robusts (more wear).

The suggestion of Walker (1981) that A. boisei KNM-ER 406 and 729 were bulk-eaters of whole fruits, ‘small, hard fruits with casings, pulp, seeds and all’, could explain the deep recessed occlusal dentine, but not the glossy appearance of heavily polished enamel, which is more typical for marsh plantfeeders. In terrestrial grazers such as sheep, tooth wear is faster, with a different gradient and fabric-like grooves.

These microwear data are consistent with the strontium/calcium ratios in Swartkrans fossils (Sillen, 1992).Apart from partial carnivory (rather unlikely with the robusts’ dentition, see Du Brul, 1977; Walker, 1981), Sillen provides two possible explanations for the low Sr/Ca of A. robustus: eating leaves and shoots of forbs and woody plants (kudu diet), and eating food derived from a wet microhabitat, for instance, from well-drained streamside soils.

In our opinion, the coincidence of several independent lines of evidence (paleo-milieu, dental morphology, enamel microwear, Sr/Ca ratios) leaves little doubt that some or all australopithecines fed regularly on AHV growing in shallow waters, much more than Western gorillas do today (Chadwik, 1995; Doran & McNeilage, 1997). It is conceivable that hominidbipedality first arose in the shallow waters of gallery or mangrove or swamp forests. ‘One of the strong points about theaquatic theory is in explaining the origin of bipedality. If our ancestors did go into the water, that would forced them towalk upright’ (Stringer, 1997). That a gradual evolutionary transition from forest to marshland is possible is illustratedby the Western lowland gorillas that spend some time feeding on AHV, wading bipedally, sitting and playing in marshy forestclearings (Chadwik, 1995; Doran & McNeilage, 1997; NDR TV film, 1997).

HOMININE LIFESTYLE

A major distinction between fossil Australopithecus and Homo is the reduction of the last molar (from M1<M2<M3 to M1<M2>M3). This might have been the result of a new, cultural factor: the frequent use of stone tools by the Homo species. 2.5-Myr-old stone tools ‘are found in floodplain environments,close to margins of channels that carried the volcanic cobblesused as raw material for tool manufacture’ (Semaw et al., 1997).

In other mammals, hard objects are used for opening shellfish or nuts. Sea otters Enhydra lutris crush shellfish with stones, chimpanzees Pan troglodytes use stones to crack nuts, mangrove capuchin monkeys Cebus apella apella use oyster shells ashammers to open oysters fixed to the roots and lower branches of mangrove trees (Fernandes, 1991).

Homo species lived in places where freshwater or marine bivalves were more abundant (e.g. Chiwondo, Chemeron, “TurkanaBoy”, Mojokerto, Terra Amata) than in the australopithecine habitats. Whereas Australopithecus appears to have lived near inland rivers and marshes, early Homo seems to have occupied also bivalve-rich areas such as mangrove forests and other seacoasts. This would explain the “sudden” appearance of Homo erectus-like people along the Indian Ocean and inland along the rivers. They colonised the Indian Ocean shores as far as Java

perhaps as early as 2 Myr BP. In contrast with australopithecines, they must have crossed deep-water straits like those of Gibraltar and Flores (Morwood et al., 1998), andtheir remains have been found all over the Old World, from Indonesia to the Cape and England (e.g. seashore remains in Mojokerto, Hopefield, Rabat, Gesher Benot Ya’aqov, Terra Amata, Boxgrove).

A dietary supplement of shellfish eating, perhaps only seasonal, could also help to explain the dramatic increase in brain size in Homo. It would have abundantly provided the elements essential for brain-growth. It has been claimed that the composition of the long-chain poly-unsaturated fatty acidsin tropical fish and shellfish is ‘more similar to that of thehuman brain than any other food source known’ (Broadhurst et al., 1998).

NATURA NON FACIT SALTUM

This “wet” scenario requires no great evolutionary steps.Forest-dwelling herbivores like capybaras, tapirs or pygmy hippos are partially adapted to the water collections in the tropical or subtropical rain or gallery or mangrove forests, but remain four-legged. In these shallow waters, primates - which, because of their arboreal history, have very mobile joints and a tendency to body erectness - easily adopt a bipedal stance and gait. Lowland gorillas go wading on their hind legs through swamps to get edible sedges and AHV (Chadwik, 1995; Doran & McNeilage, 1997). Proboscis monkeys Nasalis larvatus cross stretches of water on two legs to reach other mangrove trees (Morgan, 1997; Ellis, 1991). Japanese monkeys Macaca fuscata on islands walk bipedally into the sea (e.g. Morgan, 1997).

In mangrove swamps, lower tree parts are occupied with bivalves, which are exposed at low tide (Fernandes, 1991). No doubt, inventive inhabitants of such places began to exploit these rich food sources, just as capuchin monkeys do, who feedon crustaceans and oysters. These relatively large-brained primates even use oyster shells to crack other oysters when nostones are available (Fernandes, 1991). Probably, human ancestors, who already cracked hard-shelled nuts and fruits with stones, used pebbles as tools, at first for opening shellfish and later for processing other food sources like

carcasses of hippopotamuses (e.g. Bunn, 1981). Once they mastered how to cut through skins with sharp stones or to use stone tools for processing wood, they would have seen new niches open to them, encouraging them to invade the inland along the rivers.

Physiological data make it very probable that the phase of partial shellfish collection at one time included frequent diving (Schagatay, 1996). Today, human populations all over the world still collect shellfish or seaweed through diving. It could perhaps explain some human parallelisms with sea-mammals, according to the ideas of the so-called aquatic hypothesis of human evolution (Westenhöfer, 1924, 1942; Hardy,1960; Morgan, 1982, 1990, 1997).

Among these adaptations, those for diving and breath-holding (Schagatay, 1996), in combination with an older sound production as in many arboreal animals like gibbons (Darwin, 1871), could have led the basis for the voluntary and articulate sound production of human speech (Verhaegen, 1997).In this respect, Derek Ellis (personal communication) remarks ‘how well sound travels over water, compared to being muffled in forests, and even compared to grassland. Foraging beach andlagoon apes could separate quite widely and still remain in contact by vocalising’.

Although both Australopithecus and Homo species seem to have dwelt at the edge between land and water, the differences in paleo-milieu, dentition, tool use and brain size suggest that both had different lifestyles. Nevertheless, there is a completely natural sequence of small behavioural innovations that could lead from early australopithecines to modern humans(points 2 to 5 are seen in chimps or gorillas, see Yamakoshi, 1998; Chadwik, 1995; Ellis, 1991; Nishida, 1980; Golding, 1972). frugi- and herbivory in tropical forests (all hominoids), using stones to crack hard-shelled fruits and nuts, frugi- and herbivory also in forest clearings, plus “short”-legged bipedal wading in shallow waters, plus more frequent surface-swimming, wading and swimming also in mangrove forests, plus feeding on bivalves growing on lower tree parts, using shells or stones to crush shellfish, using stone tools for various purposes, colonising the seashores and rivers as omnivores,

re-invasion of the land along the rivers, long-legged bipedalism on land.

CONCLUSION

The combination of comparative, physiological and paleo-environmental data makes a savanna evolution improbable, but does not exclude a temporary evolution of human ancestors and relatives at the edge between land and water. Many human features cannot be explained by a history of tree or forest dwelling alone, but find convergences in primates that live in mangrove areas, such as proboscis monkeys and some tufted capuchins. The paleo-environmental and dental data suggest a gradual evolution, in strongly overlapping phases, from frugi-and herbivores in gallery or tropical or mangrove forests to “short”-legged bipedal waders in forest clearings or mangrove swamps, to omnivores and partial shellfish feeders along seacoasts and rivers, and finally to long-legged bipedalists on land.

ACKNOWLEDGEMENTS - We wish to thank Roger Crinion, Elaine Morgan,Derek Ellis, Erika Schagatay, Charles Oxnard, Norman McPhail, Paul Crowley, Nicole Oser and Renato Bender for information orcorrections.

References

Bonnefille R., 1976. Implications of pollen assemblages from the Koobi Fora Formation, East Rudolf, Kenya. Nature, 264: 403-407.

Brain C. K., 1981. The Hunters or the Hunted? University of Chicago Press, Chicago.

Brown F.H., Harris J. M., Leakey R. E. & Walker A., 1985. Early Homo erectus skeleton from west Turkana, Kenya. Nature, 316: 788-792.

Brunet M., Beauvillain A., Coppens Y., Heintz E., Moutaye A. H. E. & Pilbeam D., 1995. The first australopithecine 2,500 kilometres west of the Rift Valley (Chad). Nature, 378: 273-275.

Bunn H. T., 1981. Archaeological evidence for meat-eting by Plio-Pleistocene hominids from Koobi Fora and Olduvai Gorge. Nature, 291: 574-577.

Chadwik D., 1995. Ndoki – last place on earth. National Geographic, 188: 2-45.

Conroy G. C., 1990. Primate evolution. Norton, New York.

Dart R. A., 1925. Australopithecus africanus, the man-ape of South Africa. Nature, 115: 195-199.

Darwin C., 1871. The Descent of Man, and Selection in Relationto Sex. John Murray, London.

De Lumley H. & De Lumley M.-A., 1990. De Homo erectus verovert de Oude Wereld. In (Y. Coppens, ed.) Vijf miljoen jaar menselijkavontuur, pp. 46-67. Paleis Schone Kunsten, Brussels.

Demes B. & Creel N., 1988. Bite force, diet, and cranial morphology of fossil hominids. Journal of Human Evolution, 17: 657-670.

Doran D. M. & McNeilage A., 1997. Gorilla ecology and behavior. Evolutionary Anthropology, 6: 120-130.

Du Brul E. L., 1977. Early hominid feeding mechanisms. American Journal of Physical Anthropology, 47: 305-320.

Ellis D., 1991). Is an aquatic ape viable in terms of marine ecology and primate behaviour? In (M. Roede, ed.). The Aquatic Ape - Fact or Fiction?, pp. 36-74. Souvenir, London.

Fernandes M. E. B., 1991. Tool use and predation of oysters (Crassostrearhizophorae) by the tufted capuchin, Cebus apella apella, in brackish water mangrove swamp. Primates, 32: 529-531.

Fernández-Jalvo Y., Denys C., Andrews P., Williams T., DauphinY. & Humphrey L., 1998. Taphonomy and palaeoecology of Olduvai Bed-I(Pleistocene, Tanzania). Journal of Human Evolution, 34: 137-172.

Golding R. R., 1972. A gorilla and chimpanzee exhibit at the University of Ibadan Zoo. International Zoo Yearbook, 12: 71-76.

Grine F. E. & Kay R. F., 1988. Early hominid diets from quantitative image analysis of dental microwear. Nature, 333: 765-768.

Johanson D. C. & Taieb M., 1976. Plio-Pleistocene hominid discoveries in Hadar, Ethiopia. Nature, 260: 293-297.

Johanson D. C., Taieb M. & Coppens Y., 1982. Pliocene hominids from the Hadar Formation, Ethiopia (1973-1977), stratigraphic, chronologic, and paleoenvironmental contexts, with notes on hominid morphology and systematics. American Journal of Physical Anthropology, 57: 373-402.

Leakey M. D., Clarke R. J. & Leakey L. S. B., 1971. New hominid skull from Bed I, Olduvai Gorge, Tanzania. Nature, 232: 308-312.

Leakey M. D., Hay R. L., Curtis G. H., Drake R. E., Jackes M. K. & White T. D., 1976. Fossil hominids from the Laetoli Beds. Nature, 262: 460-462.

Leakey M. G., Feibel C. S., McDougall I. & Walker A., 1995. New four-million-year-old hominid species from Kanapoi and Allia Bay, Kenya. Nature, 376: 565-571.

Lee-Thorp J. A., van der Merwe N. J. & Brain C. K., 1994. Diet ofAustralopithecus robustus at Swartkrans from stable carbon isotopic analysis. Journal of Human Evolution, 27: 361-372.

Martyn J. & Tobias P. V., 1967. Pleistocene deposits and new fossil localities in Kenya. Nature, 215: 476-480.

Morden J., 1988. Towards a hominid taphonomy, carnivore consumption of human carcasses. American Journal of Physical Anthropology, 75: 251.

Morgan E., 1982. The Aquatic Ape. Souvenir, London.Morgan E., 1990. The Scars of Evolution. Souvenir, London.Morgan E., 1977. The Aquatic Ape Hypothesis. Souvenir, London.Morwood M. J., O’Sullivan P. B. & Raza A., 1998. Fission-track ages

of stone tools and fossils on the east Indonesian island of Flores. Nature, 392: 173-176.

Ninkovich D. & Burckle L. H., 1978. Absolute age of the base of the hominid-bearing bed in Eastern Java. Nature, 275: 306-308.

Nishida T., 1980. Local differences in reactions to water among wild chimpanzees. Folia primatologica, 33: 189-209.

NDR TV film, 1997. Gorillas. Discovery Channel Pictures and Silverback Productions.

Partridge T., 1985. Spring flow and tufa accretion at Taung. In (P. V. Tobias, ed.) Hominid Evolution, pp. 171-187. Liss, New York.

Pickford M., 1975. Late Miocene sediments and fossils from the Northern Kenya Rift Valley. Nature, 256: 279-284.

Poirier F. E., 1987. Understanding Human Evolution. Englewood Cliffs, Prentice-Hall.

Protsch R. R. R., 1981. Die archäologischen und anthropologischen Ergebnisse der Kolh-Larsen-Expeditionen in Nord-Tanzania 1933-1939. Band 4, 3., Tübinger Monographien zur Urgeschichte. Universität Tübingen, Tübingen.

Puech P.-F., 1984. Acidic-food choice in Homo habilis at Olduvai. Current Anthropology, 25: 349-350.

Puech P.-F., 1992. Microwear studies of early African hominid teeth. Scanning Microscopy, 6: 1083-1088.

Puech P.-F., Cianfarani F. & Albertini H., 1986. Dental microwear features as an indicator for plant food in early hominids: a preliminary study of enamel. Human Evolution, 1: 507-515.

Radosevich S. C., Retallack G. J. & Taieb M., 1992. Reassessment of the paleoenvironment and preservation of hominid fossils from Hadar, Ethiopia. American Journal of Physical Anthropology, 87: 15-27.

Rayner R. J., Moon B. P., Masters J. C., 1993. The Makapansgat australopithecine environment. Journal of Human Evolution, 24: 219-231.

Reed K. E., 1993. Building on the past: four million years or so of hominid evolution. South African Journal of Science, 89: 519-520.

Robinson J. T., 1954. Prehominid dentition and hominid evolution. Evolution, 8: 324-334.

Schagatay E., 1996. The Human Diving Response – Effects of Temperature and Training. University of Lund, Lund.

Schmidt-Nielsen K., 1979. Desert Animals – Physiological Problems of Heat and Water. Dover, New York.

Schrenk F., Bromage T. G., Gorthner A. & Sandrock O., 1995. Paleoecology of the Malawi Rift, vertebrate and invertebrate faunal contexts of the Chiwondo Beds, northern Malawi. Journal of Human Evolution, 28:59-70.

Semaw S., Renne P., Harris J. W. K., Feibel C. S., Bernor R. L., Fesseha N. & Mowbray K., 1997. 2.5-million-year-old stone tools from Gona, Ethiopia. Nature: 385, 333-336.

ShipmanP. & Harris J. M., 1988. Habitat preference and paleoecology of Australopithecus boisei in Eastern Africa. In (F. F. Grine, ed.) Evolutionary History of the “Robust” Australopithecines, pp. 343-382. Aldine de Gruyter, New York.

Sillen A., 1992. Strontium-calcium ratios (Sr/Ca) of Australopithecus robustus and associated fauna from Swartkrans. Journal of Human Evolution, 23: 495-516.

Stringer C., 1997. Discussion. RSA Journal, November/December: 115.

Suwa G., Asfaw B., Beyene Y., White T. D., Katoh S., Nagaoka S., Nakaya H., Uzawa K., Renne P. & WoldeGabriel G., 1997. The first skull of Australopithecus boisei. Nature, 389: 489-492.

Tobias P. V., 1995. Lecture. University College London, November 14.

Ungar P. S. & Grine F. E., 1989. Maxillary central incisor wear in Australopithecus and Paranthropus. American Journal of Physical Anthropology, 78: 317.

Ungar P. S., & Grine F. E., 1991. Incisor size and wear in Australopithecus africanus and Paranthropus robustus. Journalof Human Evolution, 20: 313-340.

Verhaegen M., 1991. Human regulation of body temperature and water balance. In (M. Roede, ed.) The Aquatic Ape – Fact or Fiction?, pp. 182-192. Souvenir, London.

Verhaegen M., 1993. Aquatic versus savanna, comparative and paleo-environmental evidence. Nutrition and Health, 9: 165-191.

Verhaegen M., 1997. In den Beginne was het Water. Hadewijch, Antwerp.

Walker A., 1981. Diet and teeth – dietary hypotheses and human evolution. Philosophical Transactions of the Royal Society London B, 292: 57-64.

Walker A., Leakey R., Harris J. M. & Brown F. 1986. 2.5 Myr Australopithecus boisei from west of Lake Turkana. Nature, 322: 517-522.

Walter R. C., Manega P. C., Hay R. L., Drake R. E. & Curtis G.H., 1991. Laser-fusion 40Ar/39Ar dating of Bed I, Olduvai Gorge, Tanzania. Nature, 354: 145-149.

Ward, S. & Hill A., 1987. Pliocene hominid partial mandible from Tabarin, Baringo, Kenya. American Journal of Physical Anthropology, 72: 21-37.

Weiner S., Xu Q., Goldberg P., Liu J. & Bar-Yosef O., 1998. Evidence for the use of fire at Zhoukoudian, China. Science, 281: 251-253.

Westenhöfer M., 1924. Das menschliche Kinn, seine Entstehung und anthropologische Bedeutung. Archiv für Frauenkunde und Konditionsforschung, 10: 239-262.

Westenhöfer M., 1942. Der Eigenweg des Menschen. Berlin: Mannstaede.

WoldeGabriel G., White T. D., Suwa G., Renne P., de Heinzelin J., Hart W. K. & Heiken G., 1994. Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature, 371: 330-333.

Wood B., 1993. Four million years of hominid evolution in Africa. Evolutionary Anthropology, 2: 117-119.

Wood B., 1995. Apocalypse of our own making. Nature, 379: 687.Yamakoshi G., 1998. Dietary responses to fruit scarcity of wild chimpanzees at

Bossou, Guinea: possible implications for ecological importance of tool use. American Journal of Physical Anthropology, 106: 283-295.

Received September 30, 1998 Accepted April 10, 1999