Since it was recognized, the order Primates has been considered especially intelligent in comparison with other animals. Today we recognize in other animals primate-like cognitive capacities, but it is undeniable that primates prioritize cognition and behavioral flexibility over genetically determined behavior.

Euprimate origins

The Plesiadapiformes (65 to 37 Ma) is the oldest fossil taxon attributed to the order Primates, but its members lack most of the attributes that define the Euprimates, primates of modern aspect (Bloch et al., 2007). Some have suggested that Plesiadapiformes are more closely related to the Dermoptera (colugos or flying lemurs) (Beard, 1990; Kay et al., 1990) but the current consensus is that they are primitive primates. This incredibly diverse group persisted for more than 25 Ma and ranged from North America to Asia and Europe. Plesiadapiformes evolved from arboreal mammals and have primate-like grasping feet but teeth that resemble those of the earliest mammals and living insectivores, with pointy cusps and sharp crests to pierce and slice the exoskeletons of the insects they eat (Silcox et al., 2015); their teeth are similar, but slightly broader, with more rounded cusps, which may signal a more diverse diet that included fruit and other plant products (sap, for example) as well as insects. It is a subtle difference, but one that may have put primates on the path toward a more diverse and adaptable diet and lifestyle.

Primate taxonomy. A simplified summary of primate systematics.

Created by the author.

The first described fossil Euprimate (from here on referred to as primates), Adapis parisiensis, was not at first recognized as a primate but as an artiodactyl (even-toed hooved animals like cattle, sheep, and antelopes). Adapids, the family to which Adapis belongs, have slender, flexible limbs and dexterous, gripping hands and feet with nails supporting expanded digital pads, rather than claws. These modern-looking primates appear in the Eocene (56–33.9 Ma) (Godinot, 2015). Early on, once primate fossils were recognized as such, it was noted that, like modern primates, they tend to have relatively large brains, small snouts, and large, convergent eyes. These traits are suggestive of a lower reliance on smell and a higher reliance on vision, compared with other mammals, as well as of enhanced cognitive capacity.

In seeking to explain the tactile and visual emphasis of the sensory systems in primates, theories have focused on diet and ecology (Cartmill, 1992; Sussman, 1991). Like modern primates, early primates were arboreal, spending most of their time in the trees. There are many challenges in an arboreal habitat. Its 3-dimensionality, the importance of not falling while leaping and moving rapidly among the branches, and the ability to hunt or collect food in the most terminal branches. Hunting, in particular the ability to grab insects using the enhanced 3-D vision, is made possible by overlapping visual fields. The earliest primates evolved in the context of the emergence in abundance of angiosperm vegetation (flowering plants), which not only produce fruit in the terminal branches but also attract insects. The earliest primates were nocturnal (deduced from the large size of the orbits or eye sockets), which imposes special challenges for hunting and negotiating an arboreal milieu (Wu et al., 2022).

Ekembo’s skull (in the picture) has an average brain size within the range of present-day monkeys and gibbons. Ekembo is monkey-like in overall adaptation, with subtle but definitive ape attributes. It was likely at least as intelligent as living Old World monkeys, and probably had a similar flexibility of foraging, ranging, and social behaviors.

David R. Begun

These primates already show potential signs of enhanced intelligence in the size and morphology of the brain. Compared with contemporary mammals, the brains of the first primates are absolutely larger with reduced olfactory lobes in relation to overall brain size (Radinsky, 1979). Brain size is generally considered to be a proxy, albeit imperfect, for intelligence (Gibson et al., 2001; Street et al., 2017). Reorganization of cerebral regions often accompanies the attainment of more modern primate grades (strepsirrhine to haplorrhine, basal anthropoid to hominoid, basal hominoid to modern apes, apes to humans), and has also been implicated in the development of enhanced levels of intelligence (Gibson et al., 2001; Radinsky, 1979; Street et al., 2017).

Early primates with well-preserved brain cases include adapids and omomyids, which resemble modern lemurs and lorises, and early tarsiiforms, the ancestors of living tarsiers. The oldest of these skulls have brains that are smaller relative to overall body size than in living prosimians, but toward the end of their geological range early primates had reached the lower ranges of living prosimian relative brain sizes (Godinot, 2015). Increase in brain size over time is common in mammalian lineages and can be explained by what has been called an arms race, in which there is selection for increases in intelligence in predators to outwit their prey and selection in prey species to better detect the presence of predators (Ward et al., 2004). Brain size begins to increase more dramatically with the evolution of anthropoid primates (monkeys, apes, and humans). This is accompanied by a shift to diurnal (daytime) activity and the emergence of social groups (Godinot, 2015). Daytime activity is inferred from the size of the orbits, which are smaller than in nocturnal species, while sociality is inferred from dimorphism in body and canine size. However, as important as social intelligence is in living anthropoids, especially catarrhines (Old world monkeys, apes, and humans), social complexity does not seem to predict brain size so well as diet and socioecology (López-Aguirre et al., 2022).

Anthropoids

Anthropoids, a primate suborder, include Old and New World monkeys, apes, humans, and their fossil relatives. Most fossil strepsirrhines are extinct by the time anthropoids become common in the fossil record (the earliest anthropoids are very rare before about 40 Ma). The best samples of early anthropoids come from the Fayum deposits in Egypt. Several early anthropoid genera are known with relatively well-preserved crania (Godinot, 2015).

The Fayum anthropoids include a diversity of primitive haplorrhines and catarrhines (Godinot, 2015). They were arboreal, some being primarily frugivorous and others more insectivorous. Most appear to have been diurnal and sexually dimorphic in body and canine size, suggestive of extant anthropoid-like social complexity. They are generally larger than most Eocene prosimians. We have endocasts of the primitive anthropoids Proteopithecus and Parapithecus and the primitive catarrhines Catopithecus and Aegyptopithecus (Godinot, 2015). The more primitive taxa have small brains and large olfactory lobes, while Aegyptopithecus, which is younger and more modern-looking in cranial morphology, has reduced olfactory lobes but brains at the low end of the modern prosimian range. In sum, the earliest anthropoids retain the ancient and current primate pattern of arboreality and frugivory and signal a change toward diurnal and social behavior with subtle changes in brain size and morphology that may be suggestive of some enhancements in intelligence.

Hominoids

The Hominoidea, a superfamily of the Anthropoidea, includes apes, humans and their fossil relatives. While not the oldest hominoid, our knowledge of ape evolution really begins with Ekembo, a primitive hominoid known from localities in Kenya ranging in age from about 19 to 17 Ma (McNulty et al., 2015). Ekembo is the first fully modern catarrhine. Most of the bones of its skeleton are known, revealing a body-plan much like that of living monkeys with one major exception, a coccyx in the place of a tail. Tailessness is a derived character that is considered a hallmark of the Hominoidea, possibly forcing hominoids into greater degrees of manual dexterity to compensate for the absence of the tail as a balancing mechanism in the trees. The skull of Ekembo has a relative brain size within the range of living monkeys and gibbons (Begun & Kordos, 2004). Overall, Ekembo is monkey-like in overall adaptation, with subtle but definitive ape attributes. It was likely at least as intelligent as living Old World monkeys, and probably had a similar flexibility of foraging, ranging, and social behaviors.

Afropithecus overlaps with the latter part of the temporal range of Ekembo (Leakey & Walker, 1997). Postcranially Afropithecus is indistinguishable from Ekembo. Craniodentally Afropithecus is distinct in having a massive face associated with large chewing muscles indicating a powerfully developed set of jaws and teeth for crushing and grinding. Afropithecus also has specializations of its front teeth that probably allowed it to tear through any protective covering. Afropithecus was likely capable of exploiting a wider variety of resources than Ekembo, which may have allowed its descendants to disperse north into Saudi Arabia and then Europe (Begun, 2015a, 2015b). It is in Eurasia that modern hominids (great apes and humans) evolve.

Craniodentally, Afropithecus (in the picture) is distinct in having a massive face associated with large chewing muscles indicating a powerfully developed set of jaws and teeth for crushing and grinding.

David R. Begun

The oldest hominoids from Europe are hominids (orangutans, chimpanzees, bonobos, gorillas, humans, and their fossil relatives), with modern-looking thickly enameled teeth with broad flat cusps. Like Afropithecus, European apes such as Griphopithecus had broad diets and were able to exploit resources ranging from soft fruits to more embedded foods with outer coverings such as shells or tough peels, as well as buried foods such as roots. Dietary breadth was probably the key to the success of the hominids that first dispersed into Eurasia. Dietary breadth, enabled by masticatory adaptations, may have been accompanied by changes in cognition related to ecological and dietary flexibility. Once in Eurasia, middle Miocene hominids disperse widely, occupying the region between Central Europe and the equator. Multiple taxa arise with various adaptations, but they are all united by enhanced attributes for food processing. Where known, middle Miocene apes show adaptations toward a shift to more forelimb dominated positional behavior, but they were not yet suspensory or orthograde (see below) (Nakatsukasa & Kunimatsu, 2009). They may have been engaged in more vertical climbing and hoisting activities but not suspension below branches, as in extant non-human hominoids. There are no crania known for middle Miocene apes, but by the late Miocene there is evidence of modern great ape brain sizes and developmental biology.

At about 12.5 Ma, more modern apes appear in Europe. The best known is Pierolapithecus, from an 11.9 Ma site near Barcelona (Alba, 2012). Pierolapithecus was orthograde (having a more vertically oriented backbone, as in living apes, as opposed to the more horizontally oriented backbones of monkeys and most early and middle Miocene apes (Moyà-Solà et al., 2004). Its hands are large, with long, curved fingers, suggestive of some degree of suspension. Pierolapithecus and other late middle Miocene apes from Europe have teeth closely resembling those of living chimpanzees and probably had a similar diet, heavy in soft fruits but with sufficient breadth to weather lean periods by exploiting other resources. In the late Miocene, more modern-looking apes appear, the best known of which is Danuvius, from the earliest late Miocene (Böhme et al., 2019). Danuvius differs from Pierolapithecus in having thick enamel, but like Pierolapithecus, it was orthograde, with evidence of powerfully grasping hands. The hindlimbs of Danuvius indicate that it was bipedal in the trees, with powerfully grasping feet. Bipedalism in Danuvius may be a precursor to human bipedalism (Böhme et al., 2019).

A simplified phylogeny of the Primates with a focus on the Hominoidea.

R=Rudapithecus, K= Kenyapithecus

Created by the author.

We know little about the brains of middle Miocene apes. Late Miocene apes from Europe such as Rudapithecus in Hungary and Hispanopithecus in Spain are known from partial skeletons that reveal a modern, orthograde and fully suspensory body plan. Rudapithecus is also known from three partial crania including two with braincases. From these we know that Rudapithecus had a brain within the range of living chimpanzees after accounting for the differences in body size between the two (Begun & Kordos, 2004; Gunz et al., 2020). Since brain tissue is among the most metabolically expensive, expanded brain size is very likely to be associated with selection for multiple behaviors and abilities that enhance survival and reproductive success. That Rudapithecus had achieved this level of encephalization, which is difficult to explain in the absence of a survival and reproductive benefit, suggests a pattern of behavior approaching the level of complexity of modern great apes. Indirect evidence of the evolution of enhanced cognitive capacity in apes comes from body size and especially dental development (Kelley, 2004; Ward et al., 2004). In Sivapithecus (a South Asian great ape related to orangutans) and Rudapithecus, dental evidence indicates that both taxa developed at rates comparable with living great apes, which take longer to reach maturity than do living Old World monkeys (Kelley, 2004; Smith et al., 2019). The fossil ape Afropithecus also appears to be characterized by slower growth, though not to the degree seen in the late Miocene taxa (Smith et al., 2003).

Rudapithecus is known from three partial crania including two with braincases. From these we know that Rudapithecus had a brain within the range of living chimpanzees after accounting for the differences in body size between the two. That Rudapithecus had achieved this level of encephalization suggests a pattern of behavior approaching the level of complexity of modern great apes. In the picture, a female Rudapithecus skull.

David R. Begun

Conclusions

The evolutionary history of the primates is characterized by a diversity of adaptations to an arboreal lifestyle, increasing reliance on visual cues over olfaction and an ever greater dependance on enhanced cognitive capabilities related to resource acquisition and processing, social interactions, and ecological diversity. All extant primates, but especially anthropoids, are exceptional in their levels of intelligence in comparison with most mammals. Impressive cognitive achievements characterize various branches of all anthropoids, including tool use in Cebus monkeys and the extraordinary exploits of many Old World monkeys (food washing, stream-baths, incredible behavior flexibility, and their ability to adapt to the presence of humans). Different primates have evolved their own versions of cognitive exceptionalism. But the fossil record of attributes related to intelligence reaches its pinnacle in late Miocene apes, which had achieved modern great ape body plan, reproductive biology, and probably cognition. These apes, broadly ancestral to hominins, set the stage for cognitive evolution in humans. The hominin fossil record shows consistent increases in brain size over time, correlated with the development of progressively more complex and elaborate extra-somatic survival strategies, human culture.

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