8.2: The Origin of Primates

Paleocene: Mammals in the Wake of Dinosaur Extinctions

Placental mammals, including primates, originated in the Mesozoic Era (approximately 251 million to 65.5 million years ago), the Age of Dinosaurs. During this time, most placental mammals were small, probably nocturnal, and probably avoided predators via camouflage and slow, quiet movement. It has been suggested that the success and diversity of the dinosaurs constituted a kind of ecological barrier to Mesozoic mammals. The extinction of the dinosaurs (and many other organisms) at the end of the Cretaceous Period (approximately 145.5–65.5 million years ago) might have opened up these ecological niches, leading to the increased diversity and disparity in mammals of the Tertiary Period (approximately 65.5–2.5 million years ago).

The Paleocene was the first epoch in the Age of Mammals. Soon after the Cretaceous-Tertiary (K-T) extinction event, new groups of placental mammals appear in the fossil record. Many of these groups achieved a broad range of sizes and lifestyles as well as a great number of species before declining sometime in the Eocene (or soon thereafter). These groups were ultimately replaced by the modern orders of placental mammals (Figure 8.3). It is unknown whether these replacements occurred gradually, for example by competitive exclusion, or rapidly, perhaps by sudden geographic dispersals with replacement. In some senses, the Paleocene might have been a time of recovery from the extinction event; it was cooler and more seasonal globally than the subsequent Eocene.

Figure 8.3: A mural of Eocene flora and fauna in North America. Credit: Image from page 27 of “Annual report for the year ended June 30 …” (1951) by Internet Archive Book Images has been designated to the public domain (CC0). This photograph of the mural “Fauna and flora of middle Eocene in the Wyoming area” by Jay Matternes, was originally published by the Smithsonian, and can be viewed in context in the online version of this book.

Plesiadapiforms, the Archaic Primates

The Paleocene epoch saw the emergence of several families of mammals that have been implicated in the origin of primates. These are the plesiadapiforms, which are archaic primates, meaning they possessed some primate features and lacked others. The word plesiadapiform means “almost adapiform,” a reference to some similarities between some plesiadapiforms and some adapiforms (or adapoids; later-appearing true primates)—mainly in the molar teeth. Because enamel fossilizes better than other parts of the body, the molar teeth are the parts most often found and first discovered for any new species. Thus, dental similarities were often the first to be noticed by early mammalian paleontologists, partly explaining why plesiadapiforms were thought to be primates. Major morphological differences between plesidapiforms and euprimates (true primates) were observed later when more parts of plesiadapiform skeletons were discovered. Many plesiadapiforms have unusual anterior teeth and most have digits possessing claws rather than nails. So far, no plesiadapiform ever discovered has a postorbital bar (seen in extant strepsirrhines) or septum (as seen in haplorhines), and whether or not the auditory bulla was formed by the petrosal bone remains unclear for many plesiadapiform specimens. Nevertheless, there are compelling reasons (partly from new skeletal material) for including plesiadapiforms within the Order Primates.

Geographic and Temporal Distribution

Purgatorius is generally considered to be the earliest primate. This Paleocene mammal is known from teeth that are very plesiomorphic for a primate. It has some characteristics that suggest it is a basal plesiadapiform, but there is very little to link it specifically with euprimates (see Clemens 2004). Its ankle bones suggest a high degree of mobility, signaling an arboreal lifestyle (Chester et al. 2015). Purgatorius is plesiomorphic enough to have given rise to all primates, including the plesiadapiforms. However, new finds suggest that this genus was more diverse and had more differing tooth morphologies than previously appreciated (Wilson Mantilla et al. 2021). Plesiadapiform families were numerous and diverse during parts of the Paleocene in western North America and western Europe, with some genera (e.g., Plesiadapis; see Figure 8.4) living on both continents (Figure 8.5). Thus, there were probably corridors for plesiadapiform dispersal between the two continents, and it stands to reason that these mammals were living all across North America, including in the eastern half of the continent and at high latitudes. A few plesiadapiforms have been described from Asia (e.g., Carpocristes), but the affinities of these remain uncertain.

Figure 8.4: Families of plesiadapiforms with example genera and traits: a table. Credit: Plesiadapiforms table original to Explorations: An Open Invitation to Biological Anthropology (2nd ed.) by Jonathan M. G. Perry and Stephanie L. Canington is under a CC BY-NC 4.0 License. Content derived from Fleagle 2013.

Family	Genera	Morphology	Location	Age^1
Paromomyidae	Ignacius	Long, dagger-like, lower incisor.	North America and Europe	Early Paleocene to Late Eocene
Carpolestidae	Carpolestes	Plagiaulacoid dentition. Limb adaptations to terminal branch feeding. Grasping big toe.	North America, Europe, and Asia	Middle Paleocene to Early Eocene
Plesiadapidae	Plesiadapis	Mitten-like upper incisor. Diastema. Large body size for group.	North America and Europe	Middle Paleocene to Early Eocene
^1 Derived from Fleagle 2013.

Figure 8.5: Map of the world in the Paleocene, highlighting plesiadapiform localities on lands that would become North America, southern Europe, and eastern Asia. Credit: Paleocene Map with Plesiadapiform Localities (Figure 8.4) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License. Localities based on Fleagle 2013, 211.

General Morphological Features

Although there is much morphological variation among the families of plesiadapiforms, some common features unite the group. Most plesiadapiforms were small, the largest being about three kilograms (approximately 7 lbs.; Plesiadapis cookei). They had small brains and fairly large snouts, with eyes that faced more laterally than in euprimates. Many species show reduction and/or loss of the canine and anterior premolars, with the resulting formation of a rodent-like diastema (a pronounced gap between the premolars and the incisors, with loss of at least the canine); this probably implies a herbivorous diet. Some families appear to have had very specialized diets, as suggested by unusual tooth and jaw shapes.

Arguably the most interesting and unusual family of plesiadapiforms is the Carpolestidae. They are almost exclusively from North America (with a couple of possible members from Asia), and mainly from the Middle and Late Paleocene. Their molars are not very remarkable, being quite similar to those of some other plesiadapiforms (e.g., Plesiadapidae). However, their lower posterior premolars (p4) are laterally compressed and blade-like with vertical serrations topped by tiny cuspules. This unusual dental morphology is termed plagiaulacoid (Simpson 1933). The upper premolar occlusal surfaces are broad and are covered with many small cuspules; the blade-like lower premolar might have cut across these cuspules, between them, or both.

Figure 8.6: An artistic rendition of Carpolestes simpsoni moving along a small diameter support. Credit: CarpolestesCL by Sisyphos23 is under a CC BY-SA 3.0 License.

Many plesiadapiforms have robust limb bones with hallmarks of arboreality. Instead of having nails, most taxa had sharp claws on most or all of the digits. The extremities show grasping abilities comparable to those of primates and some arboreal marsupials. Nearly complete skeletons have yielded a tremendous wealth of information on locomotor and foraging habits. Many plesiadapiforms appear to have been able to cling to vertical substrates (like a broad tree trunk) using their sharp claws, propelling themselves upward using powerful hindlimbs, bounding along horizontal supports, grasping smaller branches, and moving head-first down tree trunks. In carpolestids in particular, the skeleton appears to have been especially well adapted to moving slowly and carefully in small terminal branches (Figure 8.6).

Debate: Relationship of Plesiadapiforms to True Primates

In the middle of the twentieth century, treeshrews (Order Scandentia) were often considered part of the Order Primates, based on anatomical similarities between some treeshrews and primates. For many people, plesiadapiforms represented intermediates between primates and treeshrews, so plesiadapiforms were included in Primates as well.

Studies of reproduction and brain anatomy in treeshrews and lemurs suggested that treeshrews are not primates (e.g., Martin 1968). This was soon followed by the suggestion to also expel plesiadapiforms (Martin 1972) from the Order Primates. Like treeshrews, plesiadapiforms lack a postorbital bar, nails, and details of the ear region that characterize true primates. Many paleoanthropologists were reluctant to accept this move to banish plesiadapiforms (e.g., F. S. Szalay, P. D. Gingerich).

Later, K. Christopher Beard (1990) found that in some ways, the digits of paromomyid plesiadapiforms are actually more similar to those of dermopterans (Order Dermoptera), the closest living relatives of primates, than they are to those of primates themselves (but see Krause 1991). At the same time, Richard Kay and colleagues (1990) found that cranial circulation patterns and auditory bulla morphology in the paromomyid, Ignacius (see Figure 8.4), are more like those of dermopterans than of primates.

For many anthropologists, this one-two punch effectively removed plesiadapiforms from the Order Primates. In the last two decades, the tide of opinion has turned again, with many researchers reinstating plesiadapiforms as members of the Order Primates. New and more complete specimens demonstrate that the postcranial skeletons of plesiadapiforms, including the hands and feet, were primate-like, not dermorpteran-like (Bloch and Boyer 2002, 2007). New fine-grained CT scans of relatively complete plesiadapiform skulls revealed that they share some key traits with primates to the exclusion of other placental mammals (Bloch and Silcox 2006). Most significant was the suggestion that Carpolestes simpsoni possessed an auditory bulla formed by the petrosal bone, like in all living primates.

The debate about the status of plesiadapiforms continues, owing to a persistent lack of key bones in some species and owing to genuine complexity of the anatomical traits involved. Maybe plesiadapiforms were the ancestral stock from which all primates arose, with some plesiadapiforms (e.g., carpolestids) nearer to the primate stem than others.

Adapoids and Omomyoids, the First True Primates

Geographic and Temporal Distribution

The first universally accepted fossil primates are the adapoids (Superfamily Adapoidea) and the omomyoids (Superfamily Omomyoidea). These groups become quite distinct over evolutionary time, filling mutually exclusive niches for the most part. However, the earliest adapoids are very similar to the earliest omomyoids.

The adapoids were mainly diurnal and herbivorous, with some achieving larger sizes than any plesiadapiforms (10 kg; 22 lbs.). By contrast, the omomyoids were mainly nocturnal, insectivorous and frugivorous, and small.

Both groups appear suddenly at the start of the Eocene, where they are present in western North America, western Europe, and India (Figure 8.7). This wide dispersal of early primates was probably due to the presence of rainforest corridors extending far into northern latitudes.

Figure 8.7: Map of the world in the Eocene, highlighting adapoid and omomyoid localities on lands that would become North America, southern Europe, Africa, and Asia. Credit: Eocene Map with Adapoid and Omomyoid Localities (Figure 8.6) original to Explorations: An Open Invitation to Biological Anthropology by Elyssa Ebding at GeoPlace, California State University, Chico is under a CC BY-NC 4.0 License. Localities based on Fleagle 2013, 229.

In North America and Europe, both groups achieved considerable diversity in the Middle Eocene, then mostly died out at the end of that epoch (Figure 8.8). In some Eocene rock formations in the western United States, adapoids and omomyoids make up a major part of the mammalian fauna. The Eocene of India has yielded a modest diversity of euprimates, some of which are so plesiomorphic that it is difficult to know whether they are adapoids or omomyoids (or even early anthropoids).

Figure 8.8: Families of adapoids and omomyoids with example genera and traits: a table. Credit: Adapoids and omomyoids table original to Explorations: An Open Invitation to Biological Anthropology (2nd ed.) by Jonathan M. G. Perry and Stephanie L. Canington is under a CC BY-NC 4.0 License. Content derived from Fleagle 2013.

Family	Genera	Morphology	Location	Age^1
Cercamoniidae	Donrussellia	Variable in tooth number and jaw shape.	Europe and Asia	Early to Late Eocene
Asiadapidae^2	Asiadapis	Plesiomorphic teeth and jaw resemble early Omomyids.	Asia	Early Eocene
Caenopithecidae^3	Darwinius	Robust jaws with crested molars. Fewer premolars.	Europe, Africa, North America, and Asia	Middle to Late Eocene
Adapidae	Adapis	Fused mandible. Long molar crests. Large size and large chewing muscles.	Europe	Late Eocene to Early Oligocene
Sivaladapidae	Sivaladapis	Some large with robust jaws.	Asia	Middle Eocene to Late Miocene
Notharctidae^4	Notharctus	Canine sexual dimorphism. Lemur-like skull. Clinging and leaping adaptations.	North America and Europe	Early to Middle Eocene
Omomyidae^5	Teilhardina	Small, nocturnal, frugivorous or insectivorous. Tarsier-like skull in some.	North America, Europe, and Asia	Early Eocene to Early Miocene
Microchoeridae^6	Necrolemur	Long bony ear tubes. Tarsier-like lower limb adaptations for leaping.	Europe and Asia	Early Eocene to Early Oligocene
^1 Derived from Fleagle 2013. ^2 See Dunn et al. 2016 and Rose et al. 2018. ^3 See Kirk and Williams 2011 and Seiffert et al. 2009. ^4 See Gregory 1920. ^5 See Beard and MacPhee 1994 and Strait 2001. ^6 See Schmid 1979.

Adapoids and omomyoids barely survived the Eocene-Oligocene extinctions, when colder temperatures, increased seasonality, and the retreat of rainforests to lower latitudes led to changes in mammalian biogeography. In North America, one genus (originally considered an omomyoid but recently reclassified as Adapoidea) persisted until the Miocene: Ekgmowechashala (Rose and Rensberger 1983). This taxon has highly unusual teeth and might have been a late immigrant to North America from Asia. In Asia, one family of adapoids, the Sivaladapidae, retained considerable diversity as late as the Late Miocene.

Adapoid Diversity

Adapoids were very diverse, particularly in the Eocene of North America and Europe. They can be divided into six families, with a few species of uncertain familial relationship. As a group, adapoids have some features in common, although much of what they share is plesiomorphic. Important features include the hallmarks of euprimates: postorbital bar, flattened nails, grasping extremities, and a petrosal bulla (Figures 8.9 and 8.10). In addition, some adapoids retain the ancestral dental formula of 2.1.4.3; that is, in each quadrant of the mouth, there are two incisors, one canine, four premolars, and three molars. In general, the incisors are small compared to the molars, but the canines are relatively large, with sexual dimorphism in some species. Cutting crests on the molars are well developed in some species, and the two halves of the mandible were fused at the midline in some species. Some adapoids were quite small (Anchomomys at a little over 100 g), and some were quite large (Magnadapis at 10 kg; 22 lbs.). Furthermore, the spaces and attachment features for the chewing muscles were truly enormous in some species, suggesting that these muscles were very large and powerful. Taken together, this suggests an overall adaptive profile of diurnal herbivory. The canine sexual dimorphism in some species suggests a possible mating pattern of polygyny, as males in polygynous primate species often compete with each other for mates and have especially large canine teeth.

Figure 8.9: Representative crania of Adapidae from Museum d’Histoire Naturelle Victor Brun, a natural history museum in Montauban, France. The white scale bar is 1 cm long. Credit: Representative crania of adapids (European adapoids, (Figure 8.7) from the Museum d’Histoire Naturelle Victor Brun in Montauban, France original to Explorations: An Open Invitation to Biological Anthropology by Jonathan M. G. Perry is under a CC BY-NC 4.0 License.

Figure 8.10: Darwinius masillae, a member of the Caenopithecidae. The slab on the left is Plate A and the slab on the right is Plate B. The parts of the skeleton in B that are outside of the dashed lines were fabricated. Credit: Darwinius masillae holotype slabs by Jens L. Franzen, Philip D. Gingerich, Jörg Habersetzer1, Jørn H. Hurum, Wighart von Koenigswald, B. Holly Smith is under a CC BY 2.5 License. Originally from Franzen et al. 2009.

Omomyoid Diversity

Like adapoids, omomyoids appeared suddenly at the start of the Eocene and then became very diverse with most species dying out before the Oligocene. Omomyoids are known from thousands of jaws with teeth, relatively complete skulls for about a half-dozen species, and very little postcranial material. Omomyoids were relatively small primates, with the largest being less than three kilograms (approximately 7 lbs.; Macrotarsius montanus). All known crania possess a postorbital bar, which in some has been described as “incipient closure.” Some—but not all—known crania have an elongated bony ear tube extending lateral to the location of the eardrum, a feature seen in living tarsiers and catarrhines. The anterior teeth tend to be large, with canines that are usually not much larger than the incisors. Often it is difficult to distinguish closely related species using molar morphology, but the premolars tend to be distinct from one species to another. The postcranial skeleton of most omomyoids shows hallmarks of leaping behavior reminiscent of that of tarsiers. In North America, omomyoids became very diverse and abundant. In fact, omomyoids from Wyoming are sufficiently abundant and from such stratigraphically controlled conditions that they have served as strong evidence for the gradual evolution of anatomical traits over time (Rose and Bown 1984).

Teilhardina (Figure 8.11; see Figure 8.2) is one of the earliest and arguably the most plesiomorphic of omomyoids. Teilhardina has several species, most of which are from North America, with one from Europe (T. belgica) and one from Asia (T. asiatica). The species of this genus are anatomically similar and the deposits from which they are derived are roughly contemporaneous. Thus, this small primate likely dispersed across the northern continents very rapidly (Smith et al. 2006).

Figure 8.11: A map of the world during the early Eocene showing one hypothesis for the direction of dispersal of the omomyoid Teilhardina. The map depicts primates hopping from continent to continent (East to West) via the forest corridors at high latitudes. Credit: Paleogeographic map showing hypothetical migration routes of Teilhardina (Figure 1) by Thierry Smith, Kenneth D. Rose, and Philip D. Gingerich. 2006. Proceedings of the National Academy of Sciences of the United States of America 103 (30): 11223–11227. Copyright (2006) National Academy of Sciences. Image is used for non-commercial and educational purposes as outlined by PNAS.