EARLY PRIMATE EVOLUTIONEARLY PRIMATE EVOLUTIONWhy did the primates appear?Who were their ancestors?Why did primates diversify?

How genes in living primates can help us answer these questions?

How the closest living relatives of primates can help us answer these

questions?

Early Early Primate Primate EvolutiEvoluti

onon•Ancestor of all primates unknown;

•Molecular data indicate an ancient split between strepsirhines and haplorhines probably before 65 Ma

Climate Change and Primate Climate Change and Primate Origins and EvolutionOrigins and Evolution

•How has climate change affected primate evolution over time?

•What factors drive climate change?

Cenozoic Climates: From Greenhouse from Cenozoic Climates: From Greenhouse from IcehouseIcehouse• Past climate change studies shed light on the natural selection factors

which drove primate evolution• During the Cretaceous period (130-65 million years ago), the Earth was

unusually warm (mean temperature = 10 to 15 ºC warmer than today).

Forests spread to latitudes that today are tundra or ice covered. No polar ice caps.

CENOZOICCENOZOICTRENDS INTRENDS INCLIMATECLIMATE

Long-term climatic trends

revealed by oxygen

isotopesOverall cooling since the onset of the Eocene 55 mya.

Foraminifera

Cenozoic climates• Cenozoic period = the age

of mammals: 65 Ma – present

• Appearance of the first mammals, and primates, of modern aspect

• Early Cenozoic global climate = warm, wet and non-seasonal with little difference between the equators and the poles

• No glaciers and ice sheets• High precipitation

forests were the dominant type of vegetation, reached the Arctic and Antarctic

Cenozoic climatesEpochs within the Cenozoic:• Paleocene (65-56 Ma) • Eocene (55-34 Ma) • Oligocene (34-23 Ma)• Miocene (23 – 5 Ma)• Pliocene (5-2.5 Ma)• Pleistocene (2.5 Ma – 10 000 BC) =

The “Ice ages”• Holocene (10 000 BC – present)

World temperatures rose slightly during the Paleocene to peak in the early Eocene

Short-term increase followed by a long-term cooling including at least 5 abrupt downturns:

34 Ma early Oligocene23 Ma terminal Oligocene/early Miocene14 Ma mid-Miocene6-5 Ma late Miocene3.1-2.8 Ma mid-Pliocene

Key tectonic events in the Cenozoic – relevance to climate:

Events which led to continental glaciation in Antarctica and the northern hemisphere:

• During the Cretaceous and early Cenozoic, Antarctica largely ice-free;

• Still connected or at least close to South America and Australia.

Warm ocean currents, deflected by South America and Australia bathed the coast of Antarctica.

• By around 35 million years ago, the last connections with Australia and South America were severed.

Deep water passages surrounded Antarctica formation of a continuous Circum- Antarctic cold current that thermally isolated Antarctica.

Cenozoic climatesCooling events associated with: Continental drift likely played a key role in global

cooling: - redirect oceanic currents, which transfer heat

between latitudes - continental collision results in mountain

building, which alters atmospheric circulation and lead to a decrease in CO2

Cenozoic climates As a result of continental drift, the climate changed

from warm and wet to increasingly cooler and drier. Forests replaced by open savannahs and grasslands.

• How about the Ice Ages? (initiated 2.5 Ma):How about the Ice Ages? (initiated 2.5 Ma): The mechanism that drove late Cenozoic cold-warm

(glacial-interglacial) rapid and intense alternation during the Ice ages:

interaction between astronomical variables, and oceanic and atmospheric circulation•Astronomical variables shown to

influence global climate on Earth are:

•The shape of the earth’s orbit – from elliptical to round (E)

•The tilt of the spin axis (T)

•The wobble of the earth’s spin axis (P)

Ecological Context for Primate origins• The Cretaceous witnessed the

appearance of flowering plants, which became dominant;

• Their success created niches for animals feeding on nectar, flowers, leaf buds, and fruits;

Explosion of insectsBirds and mammals diversified to

exploit the increase of edible plant parts and the insects;

Diversification of placental mammals;

appearance of modern-day orders

• Earliest placental mammals (~ 130 Ma) had diverse adaptations, but all were more or less similar to shrews

• The earliest primates continued to eat insects, but started developing molars with less pointed cusps and blunter ridges started eating fruits and other vegetal matter

Ecological Context of Primate origins

Paleocene Paleocene mammalsmammalsPrimitive

creatures from which the primates sprung surely appeared between 80 to 65 Ma

Plesiadapiformes - the primate ancestors?• Dinosaur extinction opened

ecological opportunities for birds and mammals who burgeoned between 65 and 55 Ma

• One such branch were the Plesiadapiformes, regarded as close to the line producing primates

• Plesoadapiformes known from western North America and western Europe, in subtropical climate

• Small (shrew to cat size), omnivorous

• Some concentrated more on insects, while other more on seeds or fruits

Plesiadapiformes - the primate ancestors?

• Primitive skulls: - large snouts with

laterally-placed eyes (well-developed sense of smell and limited overlap of the fields of vision)

- eye sockets open to the sides rather than surrounded by postorbital bars.

• In most species, the pointed terminal phalanges indicate that all digits retained claws: no grasping hands and feet

Exception: genus Carpolestes at 55 Ma: big toe had a nail and could have been opposable

Plesiadapiformes - the primate ancestors?

-- No forward-facing eyes-- tiny – 100 g, 35 cm long with the tail-- Evolved to exploit the diversity of fruits, flowers, leaf buds increased in the Paleocene took to the trees to exploit this new food source and avoid competition with rodents.

Plesiadapiformes - the primate Plesiadapiformes - the primate ancestors?ancestors?

Nail on big toe

The dentition of The dentition of CarpolestesCarpolestes

too specialized

• Plesiadapiformes linked to primates by: - shape of their molars and premolars - by possible presence of auditory bulla

Plesiadapiformes - primate ancestors?

• Yet, Plesiadapiformes resemble living tropical squirrels: - anterior teeth too specialized (large procumbent

incisors, reduced number of teeth) - cannot have given the generalized, primitive incisors and

canines and the large number of premolars of the first primates of modern

aspect. Plesiadapiformes likely a side branch, closely related to

primates, but not directly ancestral

Plesiadapiformes - primate ancestors?

Plesiadapiformes: likely side branch

Didn’t give rise toprimates

Gave adapids

and modern lemurs/lor

ises

Two hypotheses about the fate of the Plesiadapiformes

The First Primates of modern Aspect: Euprimates

What happened to the Plesiadapiformes if they did not give rise to the Primates?

became extinct in the late Paleocene or the early Eocene (56 - 54 Ma), likely because of unsuccessful competition with evolving primates of modern aspect.

The earliest fossils to be widely recognized as primates of modern aspect – jaws and teeth dated at 55 Ma.

Exhibit the suite of derived primate characteristics: - auditory bulla, - postorbital bar, - orbital convergence, - large brains relative to body size, - expanded visual areas of the brain - reduced olfactory bulbs, - grasping hands and feet, and nails on most if not all

digits.

The First Primates of Modern Aspect: Euprimates• Early Eocene: geographically and climatically similar to

the Paleocene• North America and western Europe connected by forested

land bridge, with subtropical climate• Early true primates (Euprimates) widely dispersed, and

similar between the two continents• Continental drift disrupted land connection between

Europe and N. America ~ 50 Ma

Distribution and Classification of the Euprimates• In the Eocene (55

to 34 Ma):• Very abundant Euro-American

fossils commonly divided between two groups: more lemur- like and more tarsier-like

• Both groups existed at the same time in southern and eastern Asia, northern Africa, and even India

Two diverse groups:

• Adapiformes, lemur-like (with large snouts), basal to the Strepsirhini (more closely related to Strepsirhini than to Haplorhini yet may not be directly ancestral)

• Omomyiformes, tarsier-like, basal to the Haplorhini (more closely related to Haplorhini than to Strepsirhini, yet may not be directly ancestral)

• Adapiformes were larger than omomyiformes, with body plan similar to larger extant lemurs

Distribution and Classification of Distribution and Classification of the Euprimatesthe Euprimates

Adapiformes had small orbit size: diurnal;

Omomyiformes had large orbital size: nocturnal

Euprimates: Adapiformes and Euprimates: Adapiformes and OmomyiformesOmomyiformes• Diet: most species in both groups focused on fruits,

although the really small ones ate insects while the larger ones focused on leaves

Euprimates: Adapiformes and Euprimates: Adapiformes and OmomyiformesOmomyiformes• Locomotion: in both groups:

- some hindlimb-dominated active arboreal quadrupeds like lemurs

- some slow arboreal quadrupeds like lorises

- some with elongated feet indicative of galago or tarsier-like ability to leap

• Adapiformes shared unique derived ear structure with lemurs and lorises (Ear ring), while omomyiformes – with tarsiers (Ear tube)

• Omomyiformes had more globular brains with more developed visual areas and smaller olfactory bulbs

• Adapiformes and Omomyiformes differed from living forms by being more primitive:

Adapiformes relative to lemurs/lorises: - 4 premolars on each side of the jaw (instead

of 2), - no tooth comb, - fused two halves of the lower jaw, like modern

haplorhines! - might have had sexually dimorphic canines as

anthropoids!

• Adapiformes and Omomyiformes differed from living forms by being more primitive:

Omomyiformes relative to tarsiers: - had a rhinarium (indicated by large gap between

the upper incisors)

Anthropoid OriginsAnthropoid OriginsOn anatomical grounds, which group is closer to the ancestry of

anthropoids (monkeys and apes)? Contentious!

Omomyiform teeth and skulls similar to modern anthropoid ones in some respects (smaller snouts and larger brains), but adapiformes share features with EARLY anthropoids that neither share with omomyiforms, such as:

- relatively long snout

- fusion of the two halves of the mandible in the midline in several

adapiform species and all anthropoids but no omomyiformes

- short, vertical and wide incisors versus more procumbent and sharply-

pointed ones in omomyiformes

- large, sexually-dimorphic canines in some adapiformes and in anthropoids

- lack of external auditory tube in adapiformes and early anthropoids

(presence in omomyiformes)

Anthropoid OriginsAnthropoid Origins Impossibility to distinguish between derived

similarity due to common descent (synapomorphy) and similarities that evolved in parallel (convergence) due to common adaptation

BUT, IF the tarsiers evolved from omomyiformes and IF tarsiers and anthropoids are sister taxa (more closely related to each other than either

is to lemurs/lorises)

Then probably omomyiformes were closer to the anthropoid ancestry

Then similarities between adapiforms and early anthropoids were convergences.

Theories of Primate OriginsTheories of Primate Origins• Why did the Primate pattern appear?1)Arboreal theory: the primate pattern resulted from natural selection

for features that permitted life in the trees: - collarbones providing stability of shoulder, - increased mobility of arm, - grasping hands and feet – good manipulative ability. - stereoscopic (3D) vision, - good eye to hand coordination

• Arboreal theory is criticized non-primate arboreal animals such as opossums, tree-

shrews and squirrels do not possess these characteristics;

2) Visual/Predation Hypothesis (“bug-snatching” theory):

• Grasping and visual abilities of the first primates were selected for seeing and catching insects in the understory of tropical forests.

Why did the Primate pattern Why did the Primate pattern appear?appear?

3) Extension and Update of the Arboreal theory: “Angiosperm radiation hypothesis”:

• The appearance and spread of flowering plants paved the way for a shift from an insectivorous diet to reliance on edible plant parts In the primate ancestors

• Natural selection enhanced the efficiency for foraging and harvesting flowering plants.

• Evolution in the locomotor, grasping, manipulative, cognitive, visual abilities

• Primitive primates had to : remember sites where patches of fruits are available,

when they will be ripe,

distinguish them from leaves, be able to reach them and snatch them and to remove any

inedible tissues.

Why did the Primate pattern Why did the Primate pattern appear?appear?

The Closest Living Relatives of The Closest Living Relatives of PrimatesPrimates The tree shrews (order Scandentia)• a variety of species living in the forests of Southern

Asia• Squirrel-sized, highly active, diurnal, largely

terrestrial living in the forest undergrowth• Long body, tail and muzzle, eyes on the side of the

head, claws

• One genus is arboreal and nocturnal - eats insects, vegetal material and small vertebrates

The Closest Living Relatives of The Closest Living Relatives of PrimatesPrimates•Primate-like characters of tree shrews:

- postorbital bar - enlarged visual areas of the brain - partial mobility of the big toe and thumb•Dermoptera (flying lemurs) might be more closely related to Primates than Scandentia

Flying lemurs

Inferring phylogenetic relationships and split times from the genes of living taxa• DNA sequences for phylogenetic reconstruction are powerful:

unlike anatomical differences, the likelihood that the nucleotide was changed with exactly the same other nucleotide and at exactly the same spot in the huge genome in two separate species or even individuals is minuscule.

This advantage is used in the technique known as

“ Molecular Clock”

Inferring phylogenetic relationships and split times from the genes of living taxaMolecular clock: • Allows determining the split patterns in an evolutionary tree, and even associated split dates

• Assumes that mutations in certain non-functional DNA regions have occurred randomly and at constant rates over long periods of time

Accumulation of more differences between two species implies a more ancient split, than would be the case if they differ by fewer mutations

• Powerful method: succeeds where the fossil record has not due to incompleteness

Molecular Clock cont’d

Ramapithecus