9 Early Primate Evolution

Mr. Vijit Deepani and Prof. A.K. Kapoor

Contents:

• Fossil Primates: Introduction
• Theories of primate origin
• Primates: Pre- Pleistocene Period

a.     Palaeocene epoch

b.     Eocene epoch

c.     Oligocene epoch

d.    Miocene – Pliocene epoch

• Summary

Learning outcomes:

The learner will be able to develop:

• an understanding about fossil primates and theories of primate origin.
• an insight about the extinct primate types of Pre-Pleistocene Period.

Fossil Primates: Introduction

In modern time, the living primates are graded in four principle domains – Prosimian, Monkey, Ape and man. On the basis of examination of fossil evidences, it has been established that all the living primates have evolved and ‘adaptively radiated’ from a common ancestor. Fossil primates exhibit a palaeontological record of evolutionary processes that occurred over the last 65 to 80 million years. Crucial evidence of intermediate forms, that bridge the gap between extinct and extant taxa, is yielded by the macroevolutionary study of the primate fossil evidences.

The paleoanthropologists often utilize the comparative anatomical method to develop insight about morphological adaptations in fossil primates. Crucial insight into the diet and behaviour of fossil primates is exhibited by comparing their dentition and skeletal traits with those of living primates. The examination of dental fossil material (such as teeth) could yield crucial information about the climate conditions of the period when the animal existed, if the geological structure in which the teeth were found is known. The primate fossil records and evidences provide crucial information on evolutionary trend of primate diversity over tens of millions of years.

The geological time scale provides crucial evidences related to appearance and dominance of ancestral primate forms. The Cenozoic Era is characterized by the end of the “Age of the Dinosaurs” and the beginning of the “Age of the Mammals”. This geological era witnessed significant climate and topographic changes on earth and held utmost importance in relation to primate origins and evolution. There were considerable geological and climatic changes during the Cenozoic era.

The Cenozoic is further ramified into seven epochs – Palaeocene, Eocene, Oligocene, Miocene, Pliocene, Pleistocene, and Holocene. During the Cenozoic era, primates appeared and adaptively radiated into all the various species living today. It has been emphasized that earliest primates of Palaeocene epoch were small prosimians (like tree shrews). During the Eocene epoch, lemurs and tarsiers of various kinds were distributed across North America and parts of Europe and Asia. But gradually with time, their number declined. In subsequent periods, in the new world, prosimian forms lead to development of the platyrrhine monkeys and in the Old World, these forms eventually evolved and led to emergence of catarrhine moneys, apes and man.

Fig I: Geological time scale

(Source: Lambert, 1985)

Fig II: A possible hypothesis of relationships among extant and extinct primates. (Source:Masters, 2009)

PP  CENE = Plio-Pleistocene epoch; dotted lines and question marks represent inferred relationships and uncertainties respectively.

Theories of primate origin

Scientists have proposed several theories in relation to primate origin and evolution, and the following three theories have gained recognition and acceptance – arboreality, predation, and ecology (Lehman, 2009).

Fred Szalay (1972) proposed the arboreal theory of primate origins and emphasized that primate origins represent an adaptive radiation of new species from early arboreal ancestral mammals. A change in dietary pattern from insectivory to herbivory was the impulse for this evolutionary shift. In order to ease out locomotion and movement in the complex web of flexible tree branches, grasping hands and feet also evolved in these early mammals. Although the theory throws light upon modification in dentition and limb morphology, it could not explain certain aspects of the primate visual system.

Mart Cartmill (1992) developed an alternative idea on primate origins, which is known as the visual predation theory. Cartmill emphasized that primate origins can be traced back to visual adaptations and modifications for hunting prey in arboreal dwellings. He further opined that arboreal hunting lead to evolution of grasping hands and nails which could facilitate primates to capture and hold prey in small and terminal branches. But the detailed ecological examination of insectivorous primates showed significant flaws in Cartmill’s theory. Wright et al. (2003) suggested that nocturnal insectivores are more likely to hunt using smell and sound rather than relying upon visual system and Garber (1980) suggested that tamarins, characterized with claw-like nails, exhibit adaptation in both hunting for insects in terminal branches and clinging to tree trunks to feed on exudates.

These observations led, in part, to Robert Sussman’s (1991) more ecologically based idea on primate origins, called the angiosperm co-evolution theory. He suggested that the prime impulse behind primate origins and adaptations was the roughly coeval evolution of angiosperm plants. The evolution of angiosperm plants formulated a new set of ecological niche for animals. The former lured animals to disperse their seeds and in turn provided tasty and nutritious fruit to them. Primates were one of the principle taxonomic groups that evolved to take advantage of this scenario. But it was emphasized that the field studies of living mammals similar to those that led to the first primates did not provide crucial evidence in support of either Sussman’s or Cartmill’s theories singly but provided support for aspects of both theories.

Pre-Pleistocene epoch

In order to develop understanding about early primate evolution, primate fossil remains from the different strata of pre-Pleistocene period deposits are discussed and dealt with.

Paleocene primates

The Paleocene epoch was characterized by warm climatic conditions with savannas and woodlands dominating the geographic domain in North America and Europe (Swindler, 2004). The mountainous regions of North America and France in Europe yielded fossil remains of several varieties of the primate – like taxa and most of the remains consisted of teeth and fragments of Jaw. The deposit of the middle Paleocene epoch yielded the fossil evidence of existence of the earliest primates (Das, 2008). The transition from Cretaceous to Palaeocene epoch was noted by appearance of small and primitive insectivorous mammal called Purgatorius ceratops. The late Cretaceous deposit yielded a single lower molar tooth which is linked to Purgatorius ceratops (Valen and Sloan, 1965). This genus along with other species of primitive primates is grouped under the infraorder Plesiadapiformes (Clemens, 1974). Plesiadapiformes encompasses three major families namely Carpolestidae, Phenacolemuridae and Plesiadapidae. On the basis of fossil evidences it is emphasized that most of these genera existed in North America and a few in Europe. The Family Carpolestidae is defined by certain typical fossil evidences such as jaws, both maxillae and mandibles, and teeth. Phenacolemuridae group represents the earliest of the primate forms but there is a lack of fossil evidences related to this group. Among the three groups, Plesiadapidae represent the best known family. The fossil remains of Plesiadapidae were constituted by a complete fossil skull and other parts of the skeletons. The members of this family were devoid of stereoscopic vision.

Swindler (2004) suggested that members of Plesiadapiformes were characterized by an auditory bulla formed by the petrosal portion of the temporal bone (a hallmark of living primates) and a dental formula (in most species) of 2.1.3.3, for both upper and lower jaws, indicating a reduction from the basic eutherian 3.1.4.3 dental formula.

Several scientific investigation have emphasized that Plesiadapis are unlikely to be members of the Primate Order. Plesiadapis – a prominent archaic under Plesiadapiformes – possessed primitive mammalian features such as claws instead of nails, rodent-like jaws and teeth, eyes at the side of the head, greatly enlarged incisors, a long snout and no postorbital bar (Fig III).

Fig III: Reconstruction of Plesiadapis – a prominent archaic under Plesiadapiformes (Source:

Lambert, 1987)

The Plesiadapiformes is traditionally different from Prosimii and Anthropoidea and it can be argued that the former are not ancestral to modern primates but represent an early offshoot from the primate family tree that does not lead to modern primates (Sellers, 2000).

Fig IV: Major anatomical differences between archaic Plesiadapiformes and early fossil primates

(Source: Fleagle, 2013)

Eocene primates

Several evidences from palaeoclimatology, paleaobotany and biogeography indicate that Eocene epoch represented maximum warming during the Cenozoic era. The primates of the Eocene epoch are often categorized as Euprimates. Euprimates (true primates) resemble modern day primates in various aspects such as presence of forwardly facing orbits, post-orbital bar, an opposable first toe and grasping hands and feet. Most Eocene primates are typically divided into two major families – the Adapidae and the Omomyidae (Swindler, 2004). The former and the latter are more lemur like and tarsier like in their morphology respectively. The Adapidae members inhabited North America, Europe and Asia and were further ramified into sub–families, namely, the Notharctinae and the Adapinae. The omomyids were categorized into three subfamilies, namely, Anaptomorphinae, Omomyinae and Microchoerinae.

Fig V: Reconstruction of Notharctus –an adapid

(Source: Lambert, 1987)

The adapids, with dental formula 2.1.4.3, were characterized by primitive dental traits and their canines were projecting and displayed sexual dimorphism. Based on the examination of postcranial bones it was suggested that they were mostly diurnal in their activity pattern and vertical clinger and leaper in their locomotion. The dental formula of omomyids was 2.1.3.3 but there was no evidence of sexual dimorphism in their dentition and body weight. They were arboreal and preferred nocturnal lifestyle. All omomyids possessed unfused mandibular symphysis and tubular ectotympanic bone. Adapids had a fused mandibular symphysis and ring-shaped ectotympanic bone.

Many primate palaeontologists supported the view that members of infaorder adapiforms were close relatives of the ancestor of the modern-day tooth-combed primates, while at least some omomyiforms exhibited resemblance to tarsiers (e.g., Shoshonius). Although adapiforms were devoid of tooth-combs but they shared various aspects of their wrist and ankle morphology with the living strepsirrhines. Several modern taxonomic classifications support the idea that omomyiforms are located on the haplorhine side of the subordinal divide, while adapiforms are placed with the strepsirrhines, however, whether similarities exhibited between tarsiers and omomyiforms represent close evolutionary relationship is a debatable issue (Masters, 2009).

Fig VI: Comparison of Adapoids and Omomyoids

(Source: Fleagle, 2013)

Oligocene primates

The Eocene/ Oligocene transition (33.9–23.0 MYA) is marked by continued modifications in global geography, climate, and primate habitats. This transition is also referred to as Grande Coupure (the ‘great break’ in continuity) because vast majority of mammals became extinct during this transition. The earliest fossil primates were discovered in the late Oligocene and all these primate fossils were anthropoids. Although several ‘Euprimates’ became extinct in North America and Europe but new primate taxa evolved in Asia, Africa, and South America.

Most Oligocene primates can be categorized into three principle taxonomic groups within the Haplorhini suborder – Parapithecidae, Propliopithecidae, and Platyrrhini. The parapithecids, which include the smallest anthropoid primate called Qatrania, are the most common primate fossils recovered from the Fayum (Cairo in Eygpt) deposits. Most parapithecid members possess a primitive dental formula (2.1.3.3) and have retained the third premolars, a common feature found among all modern platyrrhines (Swindler, 2004). It is likely that parapithecids were polygynous as they had sexually dimorphic canines. The postcranial anatomy of parapithecids, in several features, exhibits more resemblance to New World Monkeys than to Old World Monkeys or apes.

Fleagle (1988) emphasized that the members of propliopithecidae are comparatively larger than the parapithecids (with Aegyptopithecus being the largest Fayum primate). These early Fayum primates are often ape-like and exhibit an array of both ape and monkey traits. The propliopithecids represent primitive catarrhines before the split into apes and Old World Monkeys (Swindler, 2004).

The lower Oligocene deposits of Fayum yielded an incomplete lower jaw (with teeth but without the ascending ramii) and this fossil evidence is attributed to Propliopithecus which is considered to be a primitive anthropoid ape and to be very closely linked with gibbon. In comparison to the jaw of modern gibbon, the recovered jaw was somewhat deeper, shorter and more pointed. Although Propliopithecus is considered to be the ancestral of the modern day gibbons but Aegyptopithecus – another African variety of the Oligocene primates – exhibited much more close resemblances to the modern gibbon (Das, 2008).

Miocene-Pliocene primates

Das (2008) reported that as there seems to be continuity of certain lineages of Anthropoidea during the Miocene and Pliocene epochs, therefore, the fossil primates of the Miocene and Pliocene epochs can be examined together. This period yielded fossil remains of various Hominoid forms (besides that of Cebidae, Cercopithecidae and Lorisidae) from different locations of Asia, Europe and Africa.

In late Miocene, the hominoid forms spread from Spain (Dryopithecus) east through Europe (Oreopithecus and Ouranopithecus) to Pakistan (Sivapithecus), across the Tibetan plateau to China (Lufengpithecus) and several species were left in Africa (such as Kenyapithecus) (Swindler, 2004). The old world monkeys continued to radiate through the Plio-Pleistocene into many new econiches, particularly in Africa and Asia.

The late Miocene hominoids exhibited resemblances in certain traits, such as: (Swindler, 2004)

• They inhabited forested or wooded regions
• Many appear to have been quadrupedal climbers and walkers, but some forms may have also employed suspensory activities;
• They exhibited sexual dimorphism and were moderately large to quite large (large monkeys to small gorillas).

Table I: Principle morphological differences between Miocene and Extant apes

(Source: Begun, 2003).

Pliopithecus

Pliopithecus fossil remains were discovered from early Pliocene (late Miocene) deposits of Europe. The fossil specimen was represented by an incomplete mandible. It exhibited resemblance with gibbon (in having characters such as wide-set eyes, narrow snout portion) and monkeys (with reference to upper limb, spinal column and general body proportions). At propliopithecus stage, in Oligocene epoch, a bifurcation of gibbon line was observed (Das, 2008).

Dryopithecus

Dryopithecus (probably quite ape-like) primate fossils were represented by some teeth and jaw bone excavated from Miocene and Pliocene deposits of Europe and the Siwalik Hills of India. It has been opined that Dryopithecus are most likely ancestors of the modern Pongidae members, i.e., gorilla and chimpanzee. The cusps of the lower molar teeth of Dryopithecus exhibit a ‘Y-5’ arrangement.

Proconsul

The early Miocene deposits in Kenya (East Africa) yielded fossil remains of Proconsul. Leakey discovered majority of the Proconsul fossil remains and the remains exhibited significant variation in size and other traits. Proconsul africanus, Proconsul major and Proconsul nyanzae represent three principle species. The limb bone structure revealed that Proconsul was not adapted to arboreal brachiation.

Ramapithecus

Genus Ramapithecus represents some crucial hominid forms from Miocene period. The fossil evidence of the genus is mostly represented by teeth and jaw specimen which are mainly obtained from two regions – the Siwalik Hills in India and Fort Ternan in Kenya. G.E. Lewis, in 1932, was the first person to discover Ramapithecus fossils in the Siwalik hill regions of India. Simon, on the basis of examination of fossil evidences of the Miocene to early Pliocene period, suggested that there were two genera at that time, namely, Ramapithecus and Dryopithecus. He emphasized that Ramapithecus represented the initial step in the evolutionary divergence of humans from the common hominoid stock (which led to the development of modern apes and humans). The dental features of Ramapithecus were different from Dryopithecus as in the former genus the incisors and canines are smaller in relation to molar, but it is not so in the latter and the Dryopithecus pattern of molar cusps was not observed in Ramapithecus dental specimens. The upper jaw of Ramapithecus is shortened and the palate is arched and it bears more resemblance to man than to Dryopithecus. The members of the genus Ramapithecus was probably erect biped with hands free. Some scholars suggested that Ramapithecus is most likely the ancestor of Homo sapiens. Das (2008) even opined that Ramapithecus line was separated from the Dryopithecus lineage in the Miocene epoch and the separation was complete by the Pliocene epoch.

Oreopithecus

In 1870, the fossil remains of Oreopithecus were discovered from Tuscan, Northern Italy and later, in 1972, the remains were described by Gervais (Das, 2008). It was regarded as a cercopithecoid monkey, but in 1948 suggested that Oreopithecus is a hominid not a cercopithecoid monkey. Hurzeler gave an account of certain hominid traits such as small size of teeth, absence of premolar and diastema, small canine, short and not so prognathous face and higher positioning of mental foramen (as found in man).

Pleistocene epoch

The Quaternary period is bifurcated into two epochs – Pleistocene and Holocene (Recent). Pleistocene epoch marked the beginning of the Quaternary period and the Tertiary period ended with Pliocene epoch. The genus – Australopithecus and Homo appeared during Pliocene period and both these genera represent the first members of family Hominidae. The Pleistocene epoch witnessed the evolution of man from an ape like creature– Australopithecus – to Homo sapiens. Pleistocene deposits have yielded numerous fossil remains of ancestral hominid forms. Three principle phases have been emphasized and highlighted in the course of Hominid evolution. In chronological sequence, these include – the stage of Australopithecine, the stage of Homo erectus and the stage of Neanderthal man (Das, 2008). The Late Pleistocene deposits yielded crucial fossil evidences related to the Cro-Magnon (Aurignacian time of Upper palaeolithic period), Grimaldi and Chancelade.

Fig VII: Hominid Evolution with time

(Source link : https://s-media-cache-

ak0.pinimg.com/originals/01/a3/86/01a386cb04a6fa5c4d22ebd1c4117c1e.jpg)

Summary

Early primate evolution is a complex phenomenon and in order to understand this phenomenon, one should be acquainted with extinct and extant primate species. Dental remains forms the most frequent fossil evidence related to ancestral primate species. The approach of comparative anatomy helps primate palaeontologists to develop an understanding about morphological adaptations and general patterns of diet, locomotion, activity patterns, and even social organization which helped the ancestral primate species to survive in archaic-climatic conditions.

Several theories related to primate origin have been developed but three prominent hypotheses namely: arboreality, predation, and ecology gained recognition. The principle morphological adaptations, that helped the early primate forms to successfully inhabit their particular environments, were prehensile fingers and toes and binocular visual system. It is suggested that the first ancestral mammalian forms (infraorder Plesiadapiformes) related to true primates (but were not their direct ancestors) evolved prior to or during the Palaeocene epoch. But the Palaeocene and Eocene transition witnessed that the earliest true primate radiations and the first ‘euprimates’ or definitive primates lived in the Eocene epoch. Eocene and Oligocene transition witnessed a massive extinction event called as Grande Coupure. This event marked the disappearance of two prominent Eocene primate families – Adapidae and the Omomyidae from Europe. Fossil evidences of extinct primates obtained from Oligocene epoch indicated morphological resemblances (in several aspects) to some modern monkeys.

The Miocene epoch experienced an extensive radiation of ape-like primate species, which gradually disappeared during the Pliocene epoch and the early hominids belonging to the genus Australopithecus, which appeared during Pliocene epoch, paved the way for the evolution of modern humans.

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