2005 Andrews & Harrison - Last Common Ancestor Apes and Humans

7 The Last Common Ancestor of Apes and Humans

Peter Andrews and Terry Harrison

Introduction

In approaching the definition of the last common ances-tor of apes and humans, one has first to establish thephylogenetic relationships of the extant taxa based ontheir genealogical affinities rather than on their overallphenetic similarity, that is clade versus grade (Huxley1958; Simpson 1963; Delson 1977; Delson et al. 1977;Eldredge and Cracraft 1980). Paleoanthropology hassuffered considerably from the confusion over thisdichotomy, for the scientific prestige of such luminariesas Simpson and Mayr gave support to the grade conceptthrough their insistence on maintaining the separation ofthe Great Apes in Pongidae and humans in Hominidae(Simpson 1961, 1963; Mayr 1969). This was based inpart on the importance attached to the evolutionarydivergence of humans into a radically different adaptivezone, and this was used to justify their separation fromthe Great Apes at the family level. The two family namesare still used in the Simpson/Mayr sense (Martin 1990;Fleagle 1999), but an increasing number of researchershave proposed alternative taxonomies that are consistentwith currently recognized relationships among the extanthominoids (Goodman 1963, 1975; Delson and Andrews1975; Andrews 1985, 1992; Skelton et al. 1986; Harrison1987, 1993; Skelton and McHenry 1992, 1998; Harrisonand Rook 1997; Goodman et al. 1998; Wood and Collard1999; Delson et al. 2000; Groves 2001; Begun 2002;Kelley 2002; Stringer and Andrews 2005).

Both anatomical and molecular data provide the pri-mary evidence for inferring the evolutionary relation-ships of extant apes. There is now general agreementamong paleoanthropologists, comparative morpholo-gists, and molecular systematists that humans are mostclosely related to chimpanzees, followed by gorillas, andthen orang utans (Miyamoto et al. 1987; Goodman etal. 1990, 1998; Miyamoto and Goodman 1990; Ruvolo1997; Hacia 2001; Groves 2001; Pilbeam 2002; Paabo

2003; Pilbeam and Young 2004). Most current classifica-tions reflect these relationships, although there are varia-tions in preferred nomenclature and ranking. The oneadopted here recognizes two subfamilies within the fami-ly Hominidae–Homininae (humans + African apes) andPonginae (orang utan). The Homininae contains thetribes Gorillini (gorillas) and Hominini (humans + chim-panzees). An equally acceptable alternative (using highertaxonomic ranks) would be to group humans and chim-panzees in subfamily Homininae, and this together withsubfamily Gorillinae in family Hominidae, as distinctfrom family Pongidae for the orang utan (Table 7.01).

It is a relatively simple matter to draw up an exten-sive list of morphological traits that distinguish modernhumans from their extant sister taxon, the chimpanzees(Le Gros Clark 1964, 1971; Aiello and Dean 1990).Many of these are autapomorphies or uniquely derivedfeatures that distinguish humans from all other hominoids.However, it is important to note that chimpanzees are alsoderived relative to the last common ancestor, while insome respects humans retain the inferred primitive homi-noid condition (e.g., humans have five lumbar vertebraeon average, while chimpanzees have reduced this region tofour vertebrae). Among human specializations, the mostprominent, at least in terms of skeletal anatomy, are thechanges in the hip, knee and foot related to development ofupright posture and obligate bipedalism, the greatly

Table 7.1

Superfamily Hominoidea

Family Subfamily Tribe Subtribe Genus

Hylobatidae Hylobates Gibbons

and siamang

Hominidae Ponginae Pongo Orang utan

Homininae Gorillini Gorilla Gorilla

Hominini Panina Pan Chimpanzees

Hominina Homo Humans

1 0 4 Interpreting the Past

enlarged relative brain size, the reduction in the size of thecanines, and the loss of C/P3 sectorial function (along witha corresponding modification in the form of the caninesand anterior premolars). It is this suite of unique featuresthat provides the basis for recognizing extinct species ashomininans (i.e., humans and their close extinct relatives)in the fossil record.

Characters in Stem Clades

The extinct close relatives of humans, such as Homoerectus and Homo neanderthalensis, can be readily shownto be members of Hominina, but it becomes increasinglymore difficult when more distant outgroups are consid-ered. For example, history has shown that researchershave not always accepted the extinct Pliocene hominines,Australopithecus and Paranthropus, as more closely relat-ed to humans than they are to chimpanzees or to otherGreat Apes (Ashton and Zuckerman 1951). However, theaccumulation of a wealth of fossil material over the past80 years, in conjunction with careful and detailed com-parative studies, have demonstrated their affinities moreconvincingly. With the more recent discovery of purport-ed stem homininans from the late Miocene of Africa,such as Ardipithecus, Orrorin, and Sahelanthropus, theproblem has proved even more taxing.

We identify here several key theoretical and practi-cal issues that are at the root of the problem of identify-ing distant human relatives. We believe that these needto be considered when attempting to interpret the phylo-genetic affinities of potential stem homininans. Theseare as follows:1) the problem of determining the affini-ties of stem members of clades where derived traits arerelatively few in comparison to primitive features, andmost of the defining specializations of the extant mem-bers of the clade are lacking; 2) the limitations inherentin reconstructing ancestral morphotypes, which are bynature rather imprecise and fuzzy concepts; 3) the seri-ous issue of the confounding influence of homoplasy orindependently acquired specialized features; and 4) thepaleoanthropological community’s historic bias towardsusing extant taxa as the standard reference for compar-ing fossils (an evolutionary bird’s eye perspective), whena better appreciation of the significance of morphologi-cal features potentially shared with extant hominoidsmight be gained from paying closer attention to the

Miocene precursors from which they were derived (aworm’s eye view of human evolution).

We expand on these issues below, and attempt toillustrate how these problems and limitations might playan important part in the interpretation or misinterpreta-tion of the phylogenetic relationships of purported stemhomininans.

Let’s start with stem groups and the lack of charac-teristics that are traditionally used to define crown clades.As an example, the lack of a tail is a uniquely derivedfeature shared by all extant hominoids among thecatarrhines, and it represents an important characteristicthat traditionally defines the taxon. It could be argued,therefore, that catarrhines that lack a tail constitute mem-bers of the hominoid clade. However, it does not logical-ly follow from this deduction that all hominoids lack atail. Given that successive primate outgroups to thecatarrhines possess a tail, it can be inferred that the lastcommon ancestor of apes and monkeys retained a longexternal tail. Unless tail loss was the initial specializationof hominoids after their divergence from the Old Worldmonkeys, then one would anticipate that stem group apeswould also primitively retain a tail. For example, it hasbeen argued that Proconsul from the early Miocene ofEast Africa, which is widely believed to be an early stemhominoid based on a number of cranio-dental and post-cranial features, may possess a tail. If this indeed is thecase, possession of a tail alone would not preclude itfrom being a hominoid, since it is a retained primitivecatarrhine feature, although it would preclude it frombeing a crown hominoid, since the inference is that thelast common ancestor of extant hominoids lacked a tail.

This example for stem apes serves to illustrate that fea-tures traditionally considered to be evolutionary hallmarksof modern taxa may not be universally applicable whenconsidering fossil stem representatives of the clade. This isequally true for homininans (i.e., humans and their closeextinct relatives). Paleoanthropologists long ago demonstrat-ed that the extraordinary degree of encephalization typical ofmodern humans was not present in early homininans. Itoccurred late in their evolutionary history and was precededby specializations linked to obligate bipedalism and modifi-cations of the canine-premolar complex. However, as dis-cussed above, it is important to emphasize that even thesecharacters, bipedalism and incisiform canines of reduced

1 0 5Last Common Ancestor

size, are not necessary prerequisites for homininan sta-tus, and that one should anticipate finding stem homini-nans that lack one or both of these traditionally recog-nized hallmarks of the clade. Since the degree of proxim-ity of an extinct taxon to the last common ancestor ofPan and Homo is inversely related to the number of phy-logenetically informative characters that link it withmodern humans, one should expect earlier stem homini-nans to become increasingly more difficult to recognizein the fossil record based on such characteristics. Withfewer and fewer characters that are phylogenetically rel-evant to human origins, better and better material willneed to become available in early homininan ancestors,particularly in a wider array of anatomical regions thatare not traditionally recognized as human specializations.

The confounding influence of homoplasy also limitsour ability to precisely reconstruct ancestral morpho-types, which, given our scant knowledge of extinct taxa,are inherently imprecise and fuzzy concepts (despite thefact that systematists usually present them in the form ofconcrete lists of characters). Based on extant catarrhines,it is equally possible to reconstruct individual charactersof the ancestral hominoid morphotype as being morelike Old World monkeys, more like hominoids, intermediate,or uniquely different from the extant forms or their near-est outgroup (Harrison 1987). For example, Le GrosClark (1971) hypothesized that the ancestral catarrhinecondition had an M1 and M2 with a tiny hypoconulid,and that this cusp was subsequently enlarged in hominoidsand lost in cercopithecids. This inferred intermediate ances-tral state is a perfectly reasonable supposition given thatthis is the primitive condition for the successive primateoutgroups. However, the occurrence of large hypoconulidsin fossil stem catarrhines, such as Dendropithecus, thatclearly diverged prior to the dichotomy between hominoidsand cercopithecoids (Andrews 1978), and the retentionof relatively large hypoconulids in specimens of Victoria-pithecus, the earliest Old World monkey (Harrison 1987),conclusively demonstrate that a large hypoconulid on M1

and M2 was the primitive condition for the last commonancestor of extant catarrhines, just as in modern homi-noids. Similarly, Old World monkeys are distinctive amongmodern anthropoids in having a very well-developed cup-shaped depression on the dorso-medial aspect of theneck of the talus for articulation with the medial malleo-

lus of the distal tibia, as well as a dorsal tubercle on thedorso-lateral aspect of the neck, that acts as a bony stopfor the anterior face of the distal tibia. This complex isprobably functionally associated with increasing the sta-bility of the talocrural joint during extreme dorsiflexion ofthe foot (Harrison 1982). Given that these features arelacking or poorly expressed in all extant hominoids,platyrrhines, and non-anthropoid primates, it would bereasonable to conclude that these are autapomorphies ofcercopithecoids. However, these characters are also typi-cally found in fossil tali from the early Miocene of EastAfrica belonging to stem catarrhines and stem hominoids,such as Dendropithecus, Limnopithecus, and Proconsul(Harrison 1982). Once the fossils are introduced into theanalysis, the most parsimonious assumption is that theOld World monkey condition is primitive for catarrhines(unless we accept the improbable scenario that earlyMiocene catarrhines, including Proconsul, are most close-ly related to cercopithecids).

What these examples demonstrate is just how labilethe list of individual traits is that make up the ancestralmorphotype, especially as new data are introduced intothe analysis. The potential for error is compounded oncethe individual traits are combined into an ancestral mor-photype. With this in mind, it is important to view ances-tral morphotypes as fuzzy approximations with relativelylow resolution, rather than precise and accurate formula-tions of the ancestral condition. Nevertheless, morphotypesare likely to be sufficiently detailed and nuanced to beused in correctly interpreting the relationships of highlyderived forms or higher-order taxa, because, in these cases,the power of resolution far outweighs the graininess ofthe data. For example, systematists have no problem cor-rectly associating neandertals with modern humans usingthe ancestral morphotype of humans and chimpanzees, orestablishing the relationships between strepsirhines,platyrrhines and catarrhines. However, in stem forms theproportion of potentially phylogenetically meaningfulcharacters is small in relation to the number of primitivefeatures, and for incomplete fossils, the level of resolutionmay be insufficient to differentiate their preserved anato-my from the ancestral morphotype. If this is the case,there is a serious danger that the outcome of phylogeneticanalyses might be influenced or skewed by the introduc-tion of a few characters of uncertain or dubious utility.


Returning to the example of the significance of pres-ence or absence of a tail in ancestral hominoids, there isthe possibility that tail loss in catarrhines might havebeen acquired independently in different lineages and isnot a feature exclusive to hominoids. This one character,when considered alone, would then incorrectly identifyunrelated forms as close relatives of hominoids.

The final key point that we have raised is what weperceive as a tendency at present towards using extantspecies, and particularly the chimpanzee, as the standardreference by which to distinguish putative homininanancestors. Humans and chimpanzees have had distinctevolutionary trajectories for at least the last five millionyears, and this is apparent both in their small degrees ofdifference in their DNA (Goodman et al. 1990; Pilbeam1996; Ruvolo 1997) and in the presence of morphologi-cal differences (Groves 2001). This is a valid approach,what we have called a bird’s eye perspective on evolution,and in species-rich taxa it is most effective, but it is leasteffective when comparing one species with another in aspecies-poor group. We are therefore advocating theadditional worm’s eye view of human evolution basedon the much greater diversity of fossil apes presentthroughout most of the Miocene Period.

Many of the issues raised above are pertinent to theinterpretation of fossil taxa that are inferred to be stemhomininans. Does the occurrence in a fossil taxon of one ortwo features found uniquely in humans among extant homi-noids provide sufficient evidence to distinguish it as a memberof the Hominina? For example, are characters that we tradi-tionally recognize as specializations indicative of bipedalismin humans, interpretable as primitive hominin features withdifferent functional meaning that have been lost in chim-panzees? Are characters associated with bipedalism homolo-gous traits in all species? Could they have been acquired asa result of parallel evolution in other hominoid lineages?These are fundamental questions that can only be answeredwith a careful and critical examination of the fossil evidencefor hominoid evolution. With this in mind, we review theevidence of the fossil apes to show the range of morphologyexisting during the middle to late Miocene. Although noneof these taxa can be specifically linked phylogenetically tothe late Miocene and Pliocene homininans, they do providea broad comparative context by which to project the ances-tral condition from which homininans were derived.

Miocene HominoidsEvidence from AfricaMorotopithecus bishopi, from the early Miocene ofUganda, is based on material originally attributed toProconsul major (Allbrook and Bishop 1963; Pilbeam1969; Andrews 1978; Gebo et al. 1997; Harrison 2002).It has similar adaptations of the skull and teeth toAfropithecus, but differs from most species of Proconsul,with narrow incisors, robust canines, enlarged premo-lars, and thick enameled molars (Andrews and Martin1987; Andrews 1992). It is derived relative to other earlyand middle Miocene species of fossil apes, includingProconsul and Nacholapithecus, but similar to extanthominoids, in having a lumbar vertebra with robustpedicles, lack of anapophyses, reduced ventral keeling,caudally inclined spinous process, and dorsally orientedtransverse processes arising from the pedicle (Walker andRose 1968; Ward 1993; Sanders and Bodenbender 1994;MacLatchy et al. 2000). The Moroto lumbar vertebraprovides the earliest evidence of the structural reorgani-zation of the vertebral column in the direction of extanthominoids, and contrasts with the long and flexible lowerback of Proconsul (Ward 1993; Sanders and Bodenbender1994; Harrison 2002). Other postcranials attributed toMorotopithecus are similar to those seen in Proconsul, andit probably retained the primitive catarrhine pattern in itsappendicular skeleton (Pickford et al. 1999; Maclatchy2000). Most researchers recognize Morotopithecus as astem hominoid (Gebo et al. 1997; MacLatchy et al. 2000;Harrison 2002; Young and MacLatchy 2004), moreadvanced postcranially than any of the early to middleMiocene hominoids from East Africa, although one of us(TH) has growing suspicions that it might be a primitiveid that has converged on extant hominoids in its axialskeleton as an adaptation for increased orthogrady in alarge-bodied catarrhine (Harrison 2002).

Equatorius and Nacholapithecus from the middleMiocene of East Africa retain many primitive charactersthat they share with Proconsul, and their affinities arestill uncertain (Ishida et al. 1999, 2004; Ward et al.1999; Kelley et al. 2002; Ward and Duren 2002;Kunimatsu et al. 2004). However, the newly describedpostcranial material of these taxa point to them beingmore derived than Proconsul (Sherwood et al. 2002;Ishida et al. 2004), and together they may form a clade


that is the sister taxon to extant hominoids (Kelley 2002;Kunimatsu et al. 2004). There is also controversy overtheir relationship with the slightly younger fossil hominoidfrom the middle Miocene of Fort Ternan, Kenyapithecuswickeri (Pickford 1985; Harrison 1992; Ward et al.1999; Kelley et al. 2000; Benefit and McCrossin 2000;Ward and Duren 2002), but they lack derived featurespresent in Kenyapithecus (see below). Simons and Pilbeam(1965) referred Kenyapithecus wickeri to the Asianspecies Ramapithecus punjabicus, thought at that timeto have been an early human ancestor because of its rel-atively large thick enameled teeth and supposed roundeddental arcade. In addition the jaws were extremely robust,the front teeth appeared small, and the face appeared tobe short, again all similarities with humans. However,these are all characters commonly found in other laterMiocene apes, and “Ramapithecus” is now recognizedas belonging to Sivapithecus. There is also a distalhumerus from Fort Ternan that is attributed toKenyapithecus wickeri (Andrews and Walker 1976;Harrison 1992). It is very similar to Equatorius africanusfrom Maboko Island, indicating that the Fort Ternan apewas also a semi-terrestrial quadruped (McCrossin andBenefit 1994; McCrossin et al. 1998; Sherwood et al.2002). This evidence for some degree of ground-living,occurring as it does so early in hominoid evolution, ispertinent to understanding later stages of human evolution.

Dispersal of Apes Out of AfricaAt around 15 million years ago, fossil apes appear forthe first time in Europe. The earliest ape from Eurasia isa single tooth attributed to Griphopithecus fromEngelswies in southern Germany (Heizmann 1992;Andrews et al. 1996; Heizmann and Begun 2001).Slightly younger is material from the Czech Republicand Turkey belonging to the same genus (Alpagut et al.1990; Andrews et al. 1996; Heizmann and Begun 2001;Kelley 2002). Griphopithecus is best known fromPasalar and Candir in Turkey, dated to 14–15 Ma, con-temporary with Kenyapithecus from Fort Ternan.Griphopithecus alpani from Pasalar was originallyknown from a small collection of teeth made by HeinzTobien in 1970 (Andrews and Tobien 1977). Since thattime nearly 2,000 specimens have been found, including15 upper and lower jaws and 17 hand and foot bones,

but by far the most common element continues to be iso-lated teeth (Alpagut et al. 1990; Martin and Andrews1993). The lower jaw of Griphopithecus alpani isrobust, like that of Kenyapithecus, and the symphysis ofthe lower jaw is similar in having a large inferior torus,but the upper jaws are less robust, and the incisors,canines and premolars are most similar to those ofEquatorius africanus.

In contrast to this, a second, less common, fossil apespecies is identified at Pasalar with upper incisors lack-ing central pillar, presence of inflated medial and lateralmarginal ridges on both uppers and lowers, canines rela-tively narrow, high crowned in both males and females,lingual cingulum on lower canines and premolars, pre-molars with approximately equal cusp sizes, robust max-illa with flat floor of maxillary sinus, and with incisivecanal like that of Dryopithecus laietanus, with a broadopening between the floor of the nasal passage and thepalate. Most of these are recognized as being sharedderived features providing evidence of relationshipbetween the new species at Pasalar and Kenyapithecusclose enough to attribute them to the same genus(Martin and Andrews 1993; Ward et al. 1999; Kelley etal. 2005). Conversely, Griphopithecus alpani andEquatorius africanus lack these characters and share whatis inferred to be primitive characteristics, so that theirsimilarity does not imply close relationship since theyconform to the generalized and probably widespread apemorphology of the middle Miocene (Kelley et al. 2000;but see Begun 2000 for an alternative view).

Origin of the Orang utanThe specialized cranial morphology of Sivapithecus con-firms an evolutionary link with the orang utan. The skullhas a dished shape, concave when viewed from the side;the distance between the eyes is very narrow, unlikealmost all other apes; the cheek region of the face isbroad and faces towards the front rather than partly tothe side as in most apes; and the morphology of thenaso-alveolar region is similar to that of the orang utanand different from all other apes, both fossil and recent(Pilbeam et al. 1977, 1980; Andrews and Cronin 1982;Pilbeam 1982; Ward and Kimbel 1983; Ward and Pilbeam1983; Ward and Brown 1986; Andrews and Pilbeam 1996;Ward 1997; Kelley 2002). In many other respects, however,


Sivapithecus is like other contemporary fossil apes. Itsteeth are little different from those of Kenyapithecus,Griphopithecus or Ankarapithecus, and indeed all of thesefossils have at one time or another been included in thegenus Sivapithecus on the basis of this similarity. Themolars of Sivapithecus had thick enamel and were rela-tively large, as in these other genera, and like them itslower jaw was robust. Its skull was lightly built, notheavily buttressed as in living Great Apes. Its postcra-nials indicate quadrupedal, above-branch pronogradeadaptations, although it was almost certainly partly ter-restrial (Pilbeam et al. 1980, 1990; Rose 1983, 1986,1989, 1994, 1997; Spoor et al. 1991; Madar et al. 2002).All these characters differ from the suite of charactersshared by the living Great Apes and presumed to havebeen present in their last common ancestor, associatedwith forelimb suspension and vertical climbing.

Herein lies a problem, for if Sivapithecus is truly thesister taxon to Pongo, then we need to determine howbest to accommodate a crown hominoid that lacks thesespecializations that are common to all living apes. Threealternative explanations have been proposed:1) Sivapithecus retains a morphological pattern close tothe primitive hominoid morphotype, while extant homi-noids have independently acquired forelimb-dominatedsuspensory and climbing specializations (Andrews 1992;Begun 1993, 1994; Larson 1998), so that Sivapithecuscould be related to Pongo based on cranial evidence;2) Sivapithecus has developed cranial specializations inparallel to Pongo, while the postcranial morphology rep-resents the primitive hominoid condition, and Sivapithecusis the sister taxon to all extant hominids (Pilbeam 1996);and 3) the postcranial morphology of Sivapithecus rep-resents a specialized condition that is derived from asuspensory last common ancestor of crown hominoids,and is associated with reacquisition of a suite of charac-ters that more closely resembles the primitive catarrhinepronograde pattern (Andrews and Pilbeam 1996; Ward1997). We currently favor the last of these alternativescenarios, which has Sivapithecus as either sister taxonto Pongo based on cranial evidence or to all extanthominids if that evidence fails.

The suite of skull characters that individually arefound in various configurations in other fossil homi-noids are found together in Ankarapithecus meteai from

the late Miocene of Turkey (Andrews and Tekkaya 1980;Alpagut et al. 1996; Kappelman et al. 2003). One set ofcharacters links it with forms found to the east, such asSivapithecus and the orang utan. These include the elon-gated and shallow sloping premaxilla, narrow incisivecanal, narrow interorbital distances, expanded zygomaticregion, enlarged upper central incisors, thick enameledmolars. A second set of characters links it with formsfound in Europe, such as Graecopithecus freybergi (verylow crowned upper incisors) and Dryopithecus laietanus(moderate development of the supra-orbital tori, shapeof the symphysis). This mixture of characters confirmsthat there is no simple geographical dichotomy in cranialmorphology and phylogenetic relationships, with easternEurasian morphologies linked to the orang utan andwestern Eurasian morphologies perhaps linked with theAfrican apes (Begun 1992, 1994; Moyà-Solà and Köhler1993, 1995, 1996; Cameron 1997). Parts of both sets ofcharacters are present in Ankarapithecus, so that if itwere to be linked with one or other descendant clades,the non-fitting characters would have to be interpretedas convergent or conservative. On present evidence, weconsider it most likely that Ankarapithecus is the sistertaxon to the Sivapithecus-Pongo clade, whereby somefeatures shared with Dryopithecus are inferred to beprimitive for hominoids (see Begun and Güleç 1998).

Suspensory Fossil ApesDryopithecus from the late Miocene of Europe is one ofthe best known fossil hominoids, but interpretationsconcerning its evolutionary relationships remain con-tentious (Begun 1992, 1994; Moyà-Solà and Köhler1993, 1995, 1996; Cameron 1997). The skulls are light-ly built, as in other fossil apes, and there are fairly well-developed brow ridges, as in Ankarapithecus meteai.This feature is different from the Sivapithecus indicusskull, and other differences are that the nasal aperture isnarrow and the interorbital distance is broad. LikeSivapithecus indicus, however, the cheek region is flatand directed forward, as it is also in Ankarapithecusmeteai. The anatomy of the floor of the nasal passageand palate, a highly derived region in Sivapithecus indi-cus, has the primitive ape condition in Dryopithecus lai-etanus, and this region differs little from Proconsul andGriphopithecus. Its cheek teeth are primitively small and


lack the thickened enamel of the other fossil apes from thesame period. In fact, the teeth of Dryopithecus differ fromthe primitive pattern seen in Proconsul only in minordetails, such as loss of the upper molar lingual cingulum.

It is this combination of characters that has producedthe confusion over the relationships of Dryopithecus. Insome characters it is like Pongo, in others it is like theAfrican apes, while in others still it is like neither and issimply primitive. However, in one respect it is not primi-tive at all and it differs from most other fossil apes. Withthe remarkable discovery of a partial skeleton fromSpain (Moyà-Solà and Köhler 1996), it has been possibleto establish that Dryopithecus possessed the full suite ofpostcranial features of the forelimb, hindlimb, and axialskeleton that is functionally related to the type of fore-limb suspensory and arboreal climbing and clamberingbehaviors seen in extant apes. In particular, its legs werehighly mobile in a manner like the orang utan, and ithad extremely long arms and hands adapted for forelimbsuspension, characters that are conspicuously lacking inmost other fossil apes. These characters point to anarboreal life with little or no access to the ground. Thisis consistent with the subtropical forest habitats inferredfor Dryopithecus localities (Andrews et al. 1997).

One fossil hominoid that shares suspensory adapta-tions with Dryopithecus is Oreopithecus bambolii(Harrison 1987; Sarmiento 1987; Harrison and Rook1997). This ape, from the late Miocene of Italy andSardinia (Andrews et al. 1996), is known from a nearlycomplete skeleton and a large number of isolated andassociated postcranial remains, jaws and teeth, and itrepresents the best known Miocene hominoid (Hurzeler1958; Szalay and Delson 1979; Delson 1987; Andrewset al. 1996; Harrison and Rook 1997). It had long arms,a broad thorax, short trunk, mobile hindlimbs, andpowerful grasping hands and feet, and, like Dryopithecusand modern Great Apes, it was adapted for forelimbsuspension and arboreal climbing (Straus 1963; Harrison1987 1991; Sarmiento 1987; Harrison and Rook 1997).However, it has recently been argued that Oreopithecuswas also specialized for terrestrial bipedalism, similar tohumans (Köhler and Moyà-Solà 1997; Rook et al.1999), but the overall evidence contradicts this claim,and indicates that these apparent similarities to humansare most likely adaptations for climbing and bipedalism

in an arboreal setting (Harrison 1991). Oreopithecus isalso strange in the unique specializations of its teeth,which are unlike those of any other fossil ape. Thesepeculiarities are due to the development of dietary spe-cialization in an insular environment (Hürzeler andEngesser 1976; Harrison and Harrison 1989; Harrisonand Rook 1997; Moyà-Solà et al. 1999). Were it not forthese, Oreopithecus would appear rather more similar toDryopithecus, and it is likely to be a close relative(Harrison and Rook 1997; Moyà-Solà and Köhler 1997).

Conclusions for Miocene ApesIt is apparent that there is nothing to link any one ofthese various fossil apes with human ancestry, nor, forthat matter, with African ape ancestry. Two groups oflater Miocene fossil ape have been distinguished above.One has robust jaws, enlarged molar teeth with thickenamel, and some buttressing of the face to accommo-date chewing stresses caused by the large teeth and ahard fruit or seed diet. They lived in seasonal woodlandto forest environments and were adapted to some degreeof terrestrial positional behaviors. The other groupinhabited wetter, less seasonal forests, and were commit-ted arboreal hominoids employing a form of locomotionthat involved forelimb suspension and climbing. Theirjaws were more lightly built and their teeth not enlarged,so that their diet must have comprised leaves and softfruits. The latter group is known only from Europe andAsia; the former group is known from both these conti-nents as well as from Africa. This may be significant, forall the early evidence for human evolution during theperiod 7–2 million years ago is African.

Distinguishing Human Ancestors

The key question to ask is what unique features consti-tute the specializations of the human lineage after its ini-tial divergence from the last common ancestor withchimpanzees. They need to be demonstrably differentfrom characters in fossil apes, distinct from characterspresent in living chimpanzees (and fossil chimpanzees ifthey were known), but present in humans. As discussedabove, various autapomorphic character complexes arepossible contenders, such as enlarged brains, reducedsexual dimorphism in body mass, upright posture andbipedalism, reduced canine size and modification of the


C/P3 homing complex, thick molar enamel, enlargedcheek teeth, and robust jaws. It was noted in the intro-ductory remarks that the fossil record not only helps toprovide a chronology for the transformation sequence,but also provides a broader comparative base for betterunderstanding and critical appreciation of the limita-tions of our phylogenetic inferences. With this in mind,the first two specializations of humans can be discount-ed immediately, for a dramatic increase in brain sizeoccurred late in human evolution, after two millionyears ago, and sexual dimorphism in body massremained high for about as long. Thick enamel on thecheek teeth, large molars, and robust jaws are commonto most homininans, but as we have seen this suite offeatures was also widespread in one of the major groupsof Miocene fossil apes. The only characters we are leftwith to distinguish stem homininans are those associatedwith bipedalism and changes in the size and form of thecanines and anterior premolars, but is this enough?

The Miocene fossil hominoid record provides cluesto suggest that one needs to be cautious about interpret-ing any such characteristics as evidence of relationshipto humans. Given the fuzzy nature of ancestral morpho-types, is it possible that the last common ancestor ofchimpanzees and humans possessed some specializationsof the postcranium that are commonly considered terres-trial bipedal traits, but are, in fact, adaptations forclimbing or arboreal bipedal behaviors, such as has beensuggested for Oreopithecus (Harrison 1991). Moreover,given that terrestrial specializations of the postcranialskeleton were more common among Miocene hominoidsthan they are in modern apes, it is conceivable that someground living fossil apes with no connection with humanancestry may have experimented with terrestrial bipedal-ism. In other words, are a few traits typically associatedwith terrestrial bipedalism in humans sufficient groundsto support the inference that later Miocene apes withsimilar specializations are in fact bipedal at all, and if so,could they have acquired these specialization in parallel?

A similar note of caution needs to be applied tocanine reduction and modification of the anterior pre-molars, since we know that there was a progressive ten-dency in later Miocene hominoids to acquire these special-izations. For example, Oreopithecus and Gigantopithecusboth exhibit relative reduced canines and various

degrees of molarization of their P3 (Hürzeler 1958, 1968;Szalay and Delson 1979; Harrison and Rook 1997), andthis is one of the main reasons why these taxa have beenphyletically linked to humans in the past. If Oreopithecushad been found in Africa, rather than isolated on anancient island in the Mediterranean, and it had retainedgeneralized thick enameled molars typical of many otherMiocene hominoids, there is no question that it wouldhave been considered a serious contender as an earlyhomininan. However, given its unique specializations, wecan infer that the characters of the postcranium and denti-tion of Oreopithecus that appear to link it uniquely withhumans are either primitive hominoid retentions orhomoplasies, rather than being indicative of a close phy-logenetic relationship. Lessons learned from Miocenehominoids highlight the need to be extremely careful inhow we interpret the fossil evidence for human evolu-tion, and they show that the search for human ancestorscannot be based simply on an uncritical demonstrationof a few apparently shared characteristics. We consider itlikely that characteristics associated with bipedalism andwith modifications of the canine-premolar complexoccurred independently in different lineages of laterMiocene hominoids. This means that scrutiny of pur-ported stem homininans will require careful and detailedcomparisons of the pertinent morphology (not justrecognition of general similarity), and, just as important-ly, will require that greater attention be given to mor-phological features which contradict their homininanaffinities and which point to relationships with otherhominoid clades. This will be the only way to establishtrue synapomorphy or homoplasy in purported homini-nans, and to overcome the innate tendency of paleoan-thropologists to preferentially link hominoids from thelater Miocene of Africa to the human lineage.

Earliest Purported Homininans

One of the earliest possible homininans (provisionally datedto 7–6 Ma) has been discovered recently not from the RiftValley of East Africa, but from the site of Toros-Menalla,Chad, in north central Africa (Brunet et al. 2002;Vignaud et al. 2002). The material, consisting of aremarkably complete although crushed cranium, andsome isolated jaw fragments and teeth, has been namedSahelanthropus tchadensis. The cranium has a short


lower face, a broad interorbital region, a strong andcontinuous supraorbital torus, a small braincase with alow posteriorly placed sagittal crest and well-developednuchal crest, a short basioccipital, small canines and rel-atively small cheek teeth with moderately thick enamel(Brunet et al. 2002). This is a combination not seen inany fossil ape. Superficially, the cranium is closest inmorphology to Graecopithecus freybergi from the lateMiocene of Greece (Bonis and Melentis 1987; Bonis andKoufos 1997), but the enlarged molars, thicker enameland a number of key features of the face in Graecopithecusdistinguish the two taxa. In addition, there are similari-ties between Sahelanthropus and Gorilla in the form ofthe orbits, wide interorbital distance, shape of the nasalaperture, and the well-developed supraorbital torus andneurocranial cresting. Sahelanthropus is believed toshare several derived features that link it with laterhomininans (Brunet et al. 2002). These include small,apically worn canines and a short basicranium with ananteriorly placed foramen magnum. However, the deter-mination that the canine was relatively small is based onthe inference that the well-developed supraorbital torusin the cranium implies that it belonged to a male indi-vidual. Since we do not have sufficient material to estab-lish the extent of sexual dimorphism in supraorbitaltorus form in Sahelanthropus or Miocene hominoidsgenerally, it is not certain whether this individual wasmale or female. It could equally be argued that the smallcanine, which we know is a good indicator of sex inmost catarrhine primates, signifies that the cranium wasthat of a female individual (see also Wolpoff et al.2002). Moreover, the relative size and obliquity of thelong-axis of the preserved roots for P3 in the mandiblefragment of Sahelanthropus suggests that the crown wasrelatively long and oriented in a fashion that wouldallow upper canine honing. At present, in the absence ofpostcranial material from Chad, there is no evidence toconclude that S. tchadensis was bipedal. The position ofthe foramen magnum may indicate a close relationshipwith later homininans, but as discussed below furthercomparative and functional studies are needed to assessthe significance of this character (see Wolpoff et al. 2002).

Similar in age is another recently discovered fossilhominoid, Orrorin tugenensis, which has been suggestedto be an early homininan (Senut et al. 2001). A number

of specimens, mainly isolated teeth and postcranialremains, have been recovered from localities in theLukeino Formation of northern Kenya, dating to ca.5.8–6.0 Ma (Sawada et al. 2002). The molars are rela-tively small and have thick enamel, as in the Chad homi-noid, and both differ from later homininans, in whichthe molars and premolars are enlarged. They also differfrom late Miocene fossil apes, where thickened enamel isassociated with molar/premolar enlargement, althoughthere are similarities with early Miocene Afropithecusturkanensis in these characters. The canine in Orrorin islarge and pointed like those of apes, both conditionsunlike that seen in Sahelanthropus tchadensis and laterhomininans. The femur resembles that of Pliocenehomininans in several respects that are interpreted asderived traits associated with bipedalism: presence of anobturator externus groove, elongated femoral neck, awell-developed gluteal tuberosity, and thicker cortex infe-riorly than superiorly on the femoral neck (Pickford et al.2002). In order to appreciate the functional significance ofthese traits, a wider comparative study is needed beforethey can be accepted as definitive evidence of bipedalism.

Evidence on the femoral neck morphology hasrecently been presented by Galik et al. (2004). From CTscans of the femoral neck of Orrorin, the authors havebeen able to show that the thickness of the cortical boneinferiorly is greater than that superiorly, and that a simi-lar pattern is a distinctive specialization of humans amonghominoids associated with bipedalism. Even setting asidesome of the technical and methodological issues that pre-vent these data from being compared directly with similardata from previous studies on early hominids and non-human primates (Ohman et al. 1997; Rafferty 1998;Gibbons 2004), there are grounds to be cautious aboutthe interpretation that the femur is necessarily from abipedal primate. Rafferty’s (1997) study of bone distribu-tion in the femoral neck of a wider taxonomic samplingof primates indicates that non-human hominoids areunusual in this respect, and that most quadrupedal primates,including Old World monkeys, have a relatively thickerinferior cortex than superior cortex in the femoral neck,closer to the human pattern. It seems that this feature isnot restricted to bipedal homininans, but occurs inpronograde quadrupedal primates, where similar weightdistributions on the hindlimbs occur. The cortical pattern


in the femoral neck in Orrorin may rule out the possibil-ity that it was an agile forelimb dominated climber, butit does not preclude the possibility that it was a moregeneralized pronograde quadruped, like some of laterMiocene hominoids from Eurasia.

Another genus and species of early homininan,Ardipithecus ramidus, is known from Aramis in theMiddle Awash region of Ethiopia, dated to ca. 4.4 Ma(White et al. 1994; Woldegabriel et al. 1994). Sharedderived features apparently linking it with later homini-nans include: canines smaller and more incisiform thanin chimpanzees; the P3 has a weaker mesiobuccal projec-tion of the crown base and lacks a functional homingfacet; the foramen magnum is relatively anteriorly placedreflecting a shortened basioccipital segment. The latter,at least, has been functionally associated with bipedality(White et al. 1994). Based on the illustrations providedby White et al. (1994), and taking into account the smallsample of fossils available, their worn and damaged con-dition, and the degree of canine sexual dimorphismknown for Miocene hominoids, the canines and lowerpremolars do not strike us as being remarkably differentfrom what one might expect to see in other known homi-noids from the middle to late Miocene of Eurasia andAfrica. Obviously, we are hesitant to say much beyondthis until we have had the opportunity to compare theoriginal material. The shortened basioccipital, in whichthe anterior border of the foramen magnum is intersect-ed by the chord connecting the right and left carotidcanals, is certainly a unique feature that links Ardipithecuswith later humans (and Sahelanthropus) among all livinghominoids. However, since this region is unknown forother later Miocene hominoids, its distinctiveness fromearlier forms is uncertain. Clearly, further comparativework on the cranial base in wider range of modern pri-mates (and other mammals) is needed to document andto understand the distribution and functional signifi-cance of this feature. Since a shortened cranial base,similar to that found in Ardipithecus, occurs in someshort-faced Old World monkeys and platyrrhines, it ispossible that it is more closely tied functionally to headpostures in both quadrupeds and bipeds, so that it is nota distinctive trait characteristic of bipeds alone.

Subsequent finds of Ardipithecus from Asa Komaand Kuserale Members, in the Middle Awash of

Ethiopia, dated to 5.2–5.8 Ma, have been assigned to adifferent species, A. kadabba (Haile-Selassie 2001;Woldegabriel et al. 2001; Haile-Selassie et al. 2004).Initially, the taxon was designated as a subspecies ofA. ramidus, but the dental differences between themwere deemed sufficient to separate them at the specieslevel (Haile-Selassie et al. 2004). Given the differences,we consider it likely, when they are better known, thatthey will prove to be assignable to two different genera(see also Begun 2004). An important difference betweenthem is that A. kadabba has larger ape-like canines and aP3 with a mesiobuccal wear facet, implying at least somedegree of functional honing. Certainly these teeth lookvery similar to those of other later Miocene hominoidsfrom East Africa and Eurasia. The most critical piece ofevidence advanced by Haile Selassie (2004) as an impor-tant characteristic linking A. kadabba with later homini-nans, is the occurrence of a dorsally canted proximaljoint surface on an isolated proximal pedal phalanx.However, as noted by Begun (2004), a similar configura-tion is known in Sivapithecus, which was an arborealpronograde quadruped (Rose 1986).

Conclusion

This brief review of fossils from the late Miocene ofAfrica shows that it is not always an easy task to identifyshared derived characteristics that link them definitivelyto later homininans. We have listed four issues causingdifficulties in identifying human ancestors:1) the problem of determining the affinities of stemmembers of clades where derived traits are relatively fewin comparison to primitive features, and most of thedefining specializations of the extant members of theclade are lacking; 2) the limitations inherent in recon-structing ancestral morphotypes, which are by naturerather imprecise and fuzzy concepts; 3) the serious issueof the confounding influence of homoplasy or independ-ently acquired specialized features; and 4) the paleoan-thropological community’s historic bias towards usingextant taxa as the standard reference for comparinghomininan fossils and neglecting the Miocene precursorsfrom which they were derived. Many of the purportedhomininan autapomorphies are in fact shared with mid-dle and late Miocene fossil apes in whole or in part, andthe neglect of this source of evidence undermines many


previous interpretations of human evolution. Before onecan decide on the significance of any character, it isimperative that a careful and detailed comparative andfunctional study of the pertinent features is undertaken,based both on a broader range of modern taxa thanAfrican apes and humans, and on comparisons withother Miocene hominoids: what we have distinguishedas the bird’s eye view, from the top down, and theworm’s eye view, from the bottom up. Such comparisonswould allow a better appreciation of the nature of thecharacters that comprise the ancestral morphotype ofchimpanzees and humans, so that we can be better pre-pared to distinguish features that are potentially mis-leading, such as primitive features and parallelisms, fromthose that are truly indicative of close phylogenetic rela-tionship. With this broader comparative perspective inplace, it will be possible to attach greater confidence tothe characters used to link these fossil hominoids to thehuman lineage.

Acknowledgements

We would like to acknowledge the inspiration thatDavid Pilbeam has been to us. So much of what wewrite about today has its foundation in David’s work, andhe has been a seminal influence on paleoanthropology formore than 30 years. We also thank Dan Lieberman andan anonymous referee for constructive comments on thetext of this paper.

References

Aiello, L., and C. Dean1990 An Introduction to Human Evolutionary

Anatomy. Academic Press, New York.

Allbrook, D., and W. W. Bishop1963 New fossil hominoid material from Uganda.

Nature 197:1187–1190.

Alpagut, B., P. Andrews, and L. Martin1990 New Miocene hominoid specimens from the

Middle Miocene site of Pasalar, Turkey. Journalof Human Evolution 19:397–422.

Alpagut, B., P. Andrews, M. Fortelius, J. Kappelman, I. Temizsoy, H. Celebi, and W. Lindsay

1996 A new specimen of Ankarapithecus meteaifrom the Sinap Formation of central Anatolia.Nature 382:349–351.

Andrews, P.1978 A revision of the Miocene Hominoidea of

East Africa. Bulletin of the British Museum(Natural History), Geology Series 30:85–225.

1985 Family group systematics and evolutionamong catarrhine primates. In Ancestors: TheHard Evidence, edited by E. Delson, pp. 14–22.Alan R. Liss, New York.

1992 Evolution and environment in theHominoidea. Nature 360:641–647.

Andrews, P., and J. Cronin1982 The relationships of Sivapithecus and

Ramapithecus and the evolution of the orang-utan. Nature 297:541–546.

Andrews, P., and L. B. Martin1987 Cladistic relationships of extant and fossil

hominoids. Journal of Human Evolution16:101–118.

Andrews, P., and D. Pilbeam1996 The nature of the evidence. Nature

379:123–124.

Andrews, P., and I. Tekkaya1980 A revision of the Turkish Miocene hominoid

Sivapithecus meteai. Palaeontology 23:85–95.

Andrews, P., and H. Tobien1977 New Miocene locality in Turkey with evi-

dence on the origin of Ramapithecus andSivapithecus. Nature 268:699–701.


Andrews, P., and A. Walker1976 The primate and other fauna from Fort

Ternan, Kenya. In Human Origins, edited byG. L. Isaac and E. R. McCown, pp. 279–304.W. A. Benjamin, Menlo Park, CA.

Andrews, P., D. R. Begun, and M. Zylstra1997 Interrelationships between functional mor-

phology and paleoenvironments in Miocenehominoids. In Function, Phylogeny, and Fossils:Miocene Hominoid Evolution and Adaptations,edited by D. R. Begun, C. V. Ward, and M. D.Rose, pp. 29–58. Plenum Press, New York.

Andrews, P., T. Harrison, E. Delson, R. L. Bernor, andL. Martin

1996 Distribution and biochronology of Europeanand Southwest Asian Miocene catarrhines. InThe Evolution of Western Eurasian NeogeneMammal Faunas, edited by R. L. Bernor,V. Fahlbusch and H. W. Mittmann, pp. 168–207.Columbia University Press, New York.

Ashton, E. H., and S. Zuckerman1951 Some cranial indices of Plesianthropus and

other primates. American Journal of PhysicalAnthropology 9:283–296.

Begun, D. R.1992 Miocene fossil hominids and the chimp-

human clade. Science 257:1929–1933.

1993 New catarrhine phalanges from Rudabánya(northeastern Hungary) and the problem of par-allelism and convergence in hominoid postcra-nial morphology. Journal of Human Evolution24:373–402.

1994 Relations among the Great Apes and humans:new interpretations based on the fossil great apeDryopithecus. Yearbook of PhysicalAnthropology 37:11–63.

2000 Middle Miocene hominoid origins. Science287:2375a.

2002 European hominoids. In The Primate FossilRecord, edited by W. C. Hartwig, pp. 339–368.Cambridge University Press, Cambridge.

2004 The earliest Hominins—is less more? Science303:1478–1480.

Benefit, B. R., and M. L. McCrossin2000 Middle Miocene hominoid origins. Science

287:2375a.

Bonis, L. de, and G. Koufos1997 The phylogenetic and functional implications

of Ouranopithecus macedoniensis. In Function,Phylogeny, and Fossils: Miocene HominoidEvolution and Adaptations, edited by D. R.Begun, C. V. Ward and M. D. Rose,pp. 317–326. Plenum Press, New York.

Bonis, L. de, and J. Melentis 1987 Intérêt de l’anatomie nasomaxillaire pour la

phylogénie de Hominoidea. Comptes Rendus del’Académie des Sciences de Paris 304:767–769.

Brunet, M., F. Guy, D. Pilbeam, H. T. Mackaye,A. Likius, D. Ahounta, A. Beauvillain, C. Blondel,H. Bocherens, J. R. Boisserie, L. De Bonis, Y. Coppens,J. Dejax, C. Denys, P. Duringer, V. Eisenmann,G. Fanone, P. Fronty, D. Geraads, T. Lehmann,F. Lihoreau, A. Louchart, A. Mahamat, G. Merceron,G. Mouchelin, O. Otero, P. Campomanes, M. Ponce deLeon, J. C. Rage, M. Sapanet, M. Schuster, J. Sudre,P. Tassy, X. Valentin, P. Vignaud, L. Viriot, A. Zazzo,and C. Zollikofer

2002 A new hominid from the Upper Miocene ofChad, Central Africa. Nature 418:145–151.

Cameron, D. W.1997 A revised systematic scheme for the Eurasian

Miocene fossil Hominidae. Journal of HumanEvolution 33:449–477.


Delson, E.1977 Catarrhine phylogeny and classification:

Principles, methods and comments. Journal ofHuman Evolution 6:433–459.

1987 An anthropoid enigma: Historical introduc-tion to the study of Oreopithecus bambolii.Journal of Human Evolution 15:523–531.

Delson, E., and P. J. Andrews1975 Evolution and interrelationships of the

catarrhine primates. In Phylogeny of thePrimates: A Multidisciplinary Approach, editedby W. P. Luckett and F. S. Szalay, pp. 405–446.Plenum Press, New York.

Delson, E., N. Eldredge, and I. Tattersall1977 Reconstruction of hominid phylogeny: A

testable framework based on cladistic analysis.Journal of Human Evolution 6:263–278.

Delson, E., I. Tattersall, J. Van Couvering, andA. S. Brooks

2000 Encyclopedia of Human Evolution andPrehistory, 2nd Edition. Garland, New York.

Eldredge, N., and J. Cracraft1980 Phylogenetic Patterns and the Evolutionary

Process. Columbia University Press, New York.

Fleagle, J. G. 1999 Primate Adaptation and Evolution. 2nd

Edition. Academic Press, New York.

Galik, K., B. Senut, M. Pickford, D. Gommery, J. Treil,A. J. Kupervage, and R. B. Eckhardt

2004 External and internal morphology of the BAR1002’00 Orrorin tugenensis femur. Science305:1450–1453.

Gebo, D. L., L. MacLatchy, R. Kitiyo, A. Deino,J. Kingston, and D. Pilbeam

1997 A hominoid genus from the early Miocene ofUganda. Science 276:401–404.

Gibbons, A.2004 Oldest human femur wades into controversy.

Science 305:1885.

Goodman, M. 1963 Man’s place in the phylogeny of the primates

as reflected in serum proteins. In Classificationand Human Evolution, edited by S. L.Washburn, pp. 204–234. Aldine, Chicago.

1975 Protein sequence and immunological specificity:Their role in phylogenetic studies of primates. InPhylogeny of the Primates: A MultidisciplinaryApproach, edited by W. P. Luckett and F. S.Szalay, pp. 219–248. Plenum Press, New York.

Goodman, M., C. A. Porter, J. Czelusniak, S. L. Page,H. Schneider, J. Shoshani, G. Gunnell, and C. P. Groves

1998 Toward a phylogenetic classification of pri-mates based on DNA evidence complemented byfossil evidence. Molecular Phylogenetics andEvolution 9:585–598.

Goodman, M., D. A. Tagle, D. H. A. Fitch, W. Bailey,J. Czelusniak, B. F. Koop, P. Benson, and J. L. Slightom

1990 Primate evolution at the DNA level and aclassification of the hominoids. Journal ofMolecular Evolution 30:260–266.

Groves, C. P.2001 Primate Taxonomy. Smithsonian Institution

Press, Washington D.C.

Hacia, J. G.2001 Genome of the apes. Trends in Genetics

17:637–645.

Haile-Selassie, Y.2001 Late Miocene hominids from the Middle

Awash. Nature 412:178–181.

2004 Late Miocene teeth from Middle Awash,Ethiopia, and early hominid dental evolution.Science 303:1503–1505.


Harrison, T. 1982 Small-bodied apes from the Miocene of East

Africa. Ph.D. Dissertation, University ofLondon.

1987 A reassessment of the phylogenetic relation-ships of Oreopithecus bambolii Gervais. Journalof Human Evolution 15:541–583.

1991 The implications of Oreopithecus for the ori-gins of bipedalism. In Origine(s) de la BipédieChez les Hominidés, edited by Y. Coppens andB. Senut, pp. 235–244. Cahiers de Paléoanthro-pologie, CNRS, Paris.

1992 A reassessment of the taxonomic and phylo-genetic affinities of the fossil catarrhines fromFort Ternan, Kenya. Primates 33:501–522.

2002 Late Oligocene to middle Miocene catarrhinesfrom Afro-Arabia. In The Primate Fossil Record,edited by W. C. Hartwig, pp. 311–338.Cambridge University Press, Cambridge.

Harrison, T. S., and T. Harrison1989 Palynology of the late Miocene Oreopithecus-

bearing lignite from Baccinello, Italy.Palaeogeography, Palaeoclimatology,Palaeoecology 76:45–65.

Harrison, T., and L. Rook 1997 Enigmatic anthropoid or misunderstood ape?

The phylogenetic status of Oreopithecus bam-bolii reconsidered. In Function, Phylogeny, andFossils: Miocene Hominoid Evolution andAdaptations, edited by D. R. Begun, C. V. Wardand M. D. Rose, pp. 327–362. Plenum Press,New York.

Heizmann, E.1992 Das Tertiär in Südwestdeutschland.

Stuttgarter Beiträge zur Naturkunde, Serie C39:1–60.

Heizmann, E., and D. R. Begun2001 The oldest Eurasian hominoid. Journal of

Human Evolution 41:463–481.

Hürzeler, J.1958 Oreopithecus bambolii Gervais: A preliminary

report. Verhandlungen der naturforschendenGesellschaft, Basel 69:1–47.

1968 Questions et réflexions sur l’histoire desanthropomorphes. Annales de Paléontologie44:13–233.

Hürzeler, J., and B. Engesser1976 Les faunes de mammiferes néogènes du basin

de Baccinello (Grosseto, Italie). Comptes Rendusde l’Académie des Sciences de Paris283:333–336.

Huxley, J. S.1958 Evolutionary processes and taxonomy with

special reference to grades. Upsala Universitetsårsskrift 6:21–39.

Ishida, H., Y. Kunimatsu, M. Nakatsukasa, andY. Nakano

1997 New hominoid genus from the middleMiocene of Nachola, Kenya. AnthropologicalScience 107:189–191.

Ishida, H., Y. Kunimatsu, T. Takano, Y. Nakano, andM. Nakatsukasa

2004 Nacholapithecus skeleton from the MiddleMiocene of Kenya. Journal of Human Evolution46:69–103.

Kappelman, J., B. G. Richmond, E. R. Seiffert,A. M. Maga, and T. M. Ryan

2003 Hominoidea (Primates). In Geology andPaleontology of the Miocene Sinap Formation,Turkey, edited by M. Fortelius and J. Kappelman,pp. 90–124. Columbia University Press, New York.


Kelley, J.2002 The hominoid radiation in Asia. In The

Primate Fossil Record, edited by W. C. Hartwig,pp. 369–384. Cambridge University Press,Cambridge.

Kelley, J., and P. Andrews2005 A new species of hominid from the Miocene

site at Pasalar, Turkey. Journal of HumanEvolution, in press.

Kelley, J., S. Ward, B. Brown, A. Hill, and W. Downs2000 Middle Miocene hominoid origins: Response.

Science 287:2375a.

Kelley, J., S. Ward, B. Brown, A. Hill, and D. L. Duren2002 Dental remains of Equatorius africanus from

Kipsaramon, Tugen Hills, Baringo District,Kenya. Journal of Human Evolution 42:39–62.

Köhler, M., and S. Moyà-Solà1997 Ape-like or hominid-like? The positional

behavior of Oreopithecus bambolii reconsid-ered. Proceedings of the National Academy ofSciences of the United States of America94:11747–11750.

Kunimatsu, Y., H. Ishida, M. Nakatsukasa, Y. Nakano,Y. Sawada, and K. Nakayama

2004 Maxillae and associated gnathodental speci-mens of Nacholapithecus kerioi, a large-bodiedhominoid from Nachola, northern Kenya.Journal of Human Evolution 46:365–400.

Larson, S. G. 1989 Parallel evolution in the hominoid trunk and

forelimb. Evolutionary Anthropology 6:87–99.

Le Gros Clark, W. E.1964 The Fossil Evidence for Human Evolution.

2nd Edition. University of Chicago Press,Chicago.

1971 The Antecedents of Man. Third Edition.Edinburgh University Press, Edinburgh.

MacLatchy, L., D. Gebo, R. Kityo, and D. Pilbeam2000 Postcranial functional morphology of

Morotopithecus bishopi, with implications forthe evolution of modern ape locomotion.Journal of Human Evolution 39:159–183.

Madar S. I., M. D. Rose, J. Kelley, L. MacLatchy, andD. Pilbeam

2002 New Sivapithecus postcranial specimens fromthe Siwaliks of Pakistan. Journal of HumanEvolution 42:705–752.

Martin L., and P. Andrews1993 Species recognition in Middle Miocene homi-

noids. In Species, Species Concepts, and PrimateEvolution, edited by W. H. Kimbel and L. B.Martin, pp. 393–427. Plenum Press, New York.

Martin, R. D.1990 Primate Origins and Evolution: A

Phylogenetic Reconstruction. PrincetonUniversity Press, Princeton.

Mayr, E.1969 Principles of Systematic Zoology. McGraw-

Hill, New York.

McCrossin, M. L., and B. R. Benefit1994 Maboko Island and the evolutionary history

of Old World monkeys and apes. In IntegrativePaths to the Past: Paleoanthropological Advancesin Honor of F. C. Howell, edited by R. S.Corruccini and R. L. Ciochon, pp. 95–122.Prentice-Hall, Englewood Cliffs, NJ.

McCrossin, M. L., B. R. Benefit, S. Gitau, and K. T. Blue1998 Fossil evidence for the origins of terrestriality

among Old World higher primates. In PrimateLocomotion: Recent Advances, edited by E. L.Strasser, J. G. Fleagle, A. L. Rosenberger, andH. M. McHenry, pp. 353–396. Plenum Press,New York.


Miyamoto, M. M., and M. Goodman1990 DNA systematics and evolution of primates.

Annual Review of Ecology and Systematics2:197–220.

Miyamoto, M. M., J. L. Slightom, and M. Goodman1987 Phylogenetic relationships of humans and

African apes from DNA sequences in the Ψηglobin region. Science 238:369–373.

Moyà-Solà S., and M. Köhler1993 Recent discoveries of Dryopithecus shed new

light on evolution of Great Apes. Nature365:543–545.

1995 New partial cranium of Dryopithecus Lartet,1863 (Hominoidea, Primates) from the upperMiocene of Can Llobateres, Barcelona, Spain.Journal of Human Evolution 29: 101–139.

1996 The first Dryopithecus skeleton: Origins ofgreat ape locomotion. Nature 379:156–159.

1997 The phylogenetic relationships ofOreopithecus bambolii Gervais, 1872. ComptesRendus de l’Académie des Sciences de Paris324:141–148.

Moyà-Solà S., M. Köhler, and L. Rook 1999 Evidence of hominid-like precision grip capa-

bility in the hand of the Miocene apeOreopithecus. Proceedings of the NationalAcademy of Sciences of the United States ofAmerica 96:313–317

Ohman, J.C., T. J. Krochta, C. O. Lovejoy,R. P. Mensforth, and B. Latimer

1997 Cortical bone distribution in the femoral neckof hominoids: Implications for the locomotionof Australopithecus afarensis. American Journalof Physical Anthropology 104:117–131.

Paabo, S.2003 The mosaic that is our genome. Nature

421:409–412.

Pickford, M.1985 A new look at Kenyapithecus based on recent

discoveries in western Kenya. Journal of HumanEvolution 14:113–143.

Pickford, M., B. Senut, and D. Gommery1999 Sexual dimorphism in Morotopithecus bishopi,

an early Middle Miocene hominoid fromUganda, and a reassessment of its geological anbiological contexts. In Late Cenozoic Environmentsand Hominid Evolution: A Tribute to Bill Bishop,edited by P. Andrews and P. Banham, pp. 27–38.Geological Society, London.

Pilbeam, D. R. 1969 Tertiary Pongidae of East Africa: Evolutionary

relationships and taxonomy. Bulletin of thePeabody Museum of Natural History 31:1–185.

1982 New hominoid skull material from theMiocene of Pakistan. Nature 295:232–234.

1996 Genetic and morphological records of theHominoidea and hominid origins: A synthesis.Molecular Phylogenetics and Evolution5:155–168.

2002 Perspectives on the Miocene Hominoidea. InThe Primate Fossil Record, edited by W. C.Hartwig, pp. 303–310. Cambridge UniversityPress, Cambridge.

Pilbeam, D., and N. Young2004 Hominoid evolution: synthesizing disparate

data. Comptes Rendus Palevol 3:303–319.

Pilbeam, D. R., M. D. Rose, C. Badgley, andB. Lipschutz

1980 Miocene hominoids from Pakistan. Postilla181:1–94.


Pilbeam, D. R., G. E. Meyer, C. Badgley, M. D. Rose,M. Pickford, A. K. Behrensmeyer, and S. M. I. Shah

1977 New hominoid primates from the Siwaliks ofPakistan and their bearing on hominoid evolution.Nature 270:689–695.

Rafferty, K.L.1998 Structural design of the femoral neck in pri-

mates. Journal of Human Evolution 34:361–383.

Rook, L., L. Bondioli, M. Köhler, S. Moyà-Solà, andR. Macchiarelli

1999 Oreopithecus was a bipedal ape after all:Evidence from the iliac cancellous architecture.Proceedings of the National Academy ofSciences of the United States of America96:8795–8799.

Rose, M. D.1983 Miocene hominoid postcranial morphology:

Monkey-like, ape-like, neither, or both? In NewInterpretations of Ape and Human Ancestry,edited by R. L. Ciochon and R. S. Corruccini,pp. 405–420. Plenum Press: New York.

1986 Further hominoid postcranial specimens fromthe late Miocene Nagri Formation of Pakistan.Journal of Human Evolution 15:333–367.

1989 New postcranial specimens of catarrhinesfrom the middle Miocene Chinji Formation,Pakistan: Descriptions and a discussion of prox-imal humeral functional morphology in anthro-poids. Journal of Human Evolution18:131–162.

1994 Quadrupedalism in some Miocenecatarrhines. Journal of Human Evolution26:387–411.

1997 Functional and phylogenetic features of theforelimb in Miocene hominoids. In Function,Phylogeny, and Fossils: Miocene HominoidEvolution and Adaptations, editors D. R. Begun,C. V. Ward and M. D. Rose, pp. 79–100.Plenum Press, New York.

Ruvolo, M.1997 Molecular phylogeny of the hominoids:

Inference from multiple independent DNAsequence data sets. Molecular Biology andEvolution 14:248–265.

Sanders, W. J., and B. E. Bodenbender 1994 Morphometric analysis of lumbar vertebra

UMP 67–28: Implications for spinal functionand phylogeny of the Miocene Moroto homi-noid. Journal of Human Evolution 26:203–237.

Sarmiento, E. E. 1987 The phylogenetic position of Oreopithecus

and its significance in the origin of theHominoidea. American Museum Novitates2881:1–44.

Sawada, Y., M. Pickford, B. Senut, T. Itaya, M. Hyodo,T. Miura, C. Kashine, T. Chujo, and H. Fujii

2002 The age of Orrorin tugenensis, an earlyhominid from the Tugen Hills, Kenya. ComptesRendus Palevol 1:293–303.

Senut, B., M. Pickford, D. Gommery, P. Mein,K. Cheboi, and Y. Coppens

2001 First hominid from the Miocene (LukeinoFormation, Kenya). Comptes Rendus del’Académie des Sciences de Paris 332:137–144.

Sherwood, R. J., S. Ward, A. Hill, D. L. Duren,B. Brown, and W. Downs

2002 Preliminary description of the Equatoriusafricanus partial skeleton (KNM-TH 28860)from Kipsaramon, Tugen Hills, Baringo District,Kenya. Journal of Human Evolution 42:63–73.


Simons, E. L., and D. R. Pilbeam 1965 Preliminary revision of the Dryopithecinae

(Pongidae, Anthropoidea). Folia Primatologica3:81–152.

Simpson, G. G.1961 Principles of Animal Taxonomy. Columbia

University Press, New York.

1963 The meaning of taxonomic statements. InClassification and Human Evolution, edited byS. L. Washburn, pp. 1–31. Aldine, Chicago.

Skelton R. R., H. M. McHenry, and G. M. Drawhorn1986 Phylogenetic analysis of early hominids.

Current Anthropology 27:21–43.

Spoor, C. F., P. Y. Sondaar, and S. T. Hussain1991 A hominoid hamate and first metacarpal

from the Late Miocene Nagri Formation ofPakistan. Journal of Human Evolution21:413–424.

Straus, W. L.1963 The classification of Oreopithecus. In

Classification and Human Evolution, edited byS. L. Washburn, pp. 146–177. Aldine, Chicago.

Stringer, C. B., and P. J. Andrews2005 The Complete World of Human Evolution.

Thames and Hudson, London.

Szalay, F. S., and E. Delson1979 Evolutionary History of the Primates.

Academic Press, New York.

Vignaud, P., P. Duringer, H. T. Mackaye, A. Likius,C. Blondel, J.-R. Boisserie, L. de Bonis, V. Eisenmann,M.-E. Etienne, D. Geraads, F. Guy, T. Lehmann,F. Lihoreau, N. Lopez-Martinez, C. Mourer-Chauviré,O. Otero, J.-C. Rage, M. Schuster, L. Viriot, A. Zazzo,and M. Brunet

2002 Geology and palaeontology of the UpperMiocene Toros-Menalla hominid locality, Chad.Nature 418:152–155.

Walker, A., and M. D. Rose1968 Fossil hominoid vertebra from the Miocene of

Uganda. Nature 217:980–981.

Ward, C. V.1993 Torso morphology and locomotion in

Proconsul nyanzae. American Journal ofPhysical Anthropology 92:291–328.

1997 Functional anatomy and phyletic implicationsof the hominoid trunk and hindlimb. InFunction, Phylogeny, and Fossils: MioceneHominoid Evolution and Adaptations, edited byD. R. Begun, C. V. Ward and M. D. Rose, pp.101–130. Plenum Press, New York.

Ward, S. C., and B. Brown1986 The facial skeleton of Sivapithecus indicus. In

Comparative Primate Biology, Vol 1,Systematics, Evolution and Anatomy, edited byD. Swindler and S. Erwin, pp. 413–452. Alan R.Liss, New York.

Ward, S., and D. L. Duren2002 Middle and late Miocene African hominoids.

In The Primate Fossil Record, edited by W. C.Hartwig, pp. 385–397. Cambridge UniversityPress, Cambridge.

Ward, S. C., and W. H. Kimbel1983 Subnasal morphology and the systematic posi-

tion of Sivapithecus. American Journal ofPhysical Anthropology 61:157–171.

Ward, S. C., and D. R. Pilbeam1983 Maxillofacial morphology of Miocene homi-

noids from Africa and Indo-Pakistan. In NewInterpretations of Ape and Human Ancestry,edited by R. L. Ciochon and R. S. Corruccini,pp. 211–238. Plenum Press, New York.

Ward, S., B. Brown, A. Hill, J. Kelley, and W. Downs 1999 Equatorius: A new hominoid genus from the

middle Miocene of Kenya. Science285:1382–1386.


White, T. D., G. Suwa, and B. Asfaw 1994 Australopithecus ramidus: A new species of

early hominid from Aramis, Ethiopia. Nature371:306–312.

Woldegabriel, G., T. D. White, G. Suwa, P. Renne,J. De Heinzelin, W. K. Hart, and G. Heiken

1994 Ecological and temporal placement of earlyPliocene hominids at Aramis, Ethiopia. Nature371:330–333.

Woldegabriel, G., Y. Haile-Selassie, P. R. Renne, W. K.Hart, S. H. Ambrose, B. Asfaw, G. Heiken, and T. White

2001 Geology and palaeontology of the LateMiocene Middle Awash valley, Afar Rift,Ethiopia. Nature 412:175–181.

Wolpoff, M. H., B. Senut, M. Pickford, and J. Hawks2002 Sahelanthropus or “Sahelpithecus”? Nature

419:581–582

Wood, B. A., and M. Collard 1999 The human genus. Science 284:65–71.

Young, N. M., and L. McLatchy2004 The phylogenetic position of Morotopithecus.

Journal of Human Evolution 46:163–184.

2005 Andrews & Harrison - Last Common Ancestor Apes and Humans

Documents

Transcript of 2005 Andrews & Harrison - Last Common Ancestor Apes and Humans