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What is a primate?
The first problem that one inevitably faces in thinking about primate origins is where to draw the line between primates and other types of mammals. If one considers only living primates (i.e., monkeys, apes, lemurs, lorises, and humans), then the Order Primates is not that difficult to define. Living primates are unusual in relying very heavily on vision — this is reflected in the skull by orbits that are close together (convergent) and bounded by a postorbital bar (Figure 1a). Primates also typically have hands and feet that are well designed for grasping (with long fingers, opposable thumbs and big toes, and nails rather than claws on most digits), and other skeletal traits that are beneficial for moving around in the trees. Finally, living primates eat a lot of fruit, and members of the order generally have features of the teeth that reflect this, including fat, round (bunodont) cusps and broad talonid basins, for squishing fruit in a mortar-and-pestle type arrangement.
Species in the fossil record that exhibit all these features will be easy to recognize as primates. However, at some point primates must have evolved from ancestors that lacked these characteristics. And unless all of these features evolved in an evolutionary instant (which seems unlikely), there must have been some species more closely related to living primates than to any other mammalian group that nonetheless lacked some of these traits. Recognizing such forms as being related to primates is a much more difficult problem, but is critical to understanding where, when, and why primates branched off from the rest of Mammalia.
Plesiadapiforms share some traits with living primates, including long fingers well designed for grasping, and other features of the skeleton that are related to arboreality (Bloch & Boyer, 2002). One species, Carpolestes simpsoni, even had a divergent big toe with a nail (Bloch & Boyer, 2002). Dentally, plesiadapiforms look quite similar to definitive primates, with broad talonid basins and a similar pattern of cusps and crests. However, no known plesiadapiform exhibits the features of living primates associated with specialized vision, such as the postorbital bar or convergent orbits. Even though they exhibit some features for primate-like grasping, known plesiadapiforms still retain claws on most of their digits. These contrasts have led some workers (e.g., Martin, 1968; Cartmill, 1974) to suggest that plesiadapiforms do not belong in the Order Primates. Others (e.g., Kay et al., 1990; Beard, 1990) have further argued that plesiadapiforms are not most closely related to primates, but instead are closer kin to another order, Dermoptera.
Figure 1: Crania of a euprimate (a,b Lemur catta, FMNH 23977) and a plesiadapiform (c,d Ignacius graybullianus, USNM 421608) in rostral (a,c) and dorsal (b,d) views.
Note the presence of the postorbital bar (red asterisk) and convergent orbits in the euprimate, missing in the plesiadapiform. Image of Ignacius graybullianus is based on a 3D reconstruction using high resolution X-ray computed tomography data (see Silcox, 2003). Scales = 1cm.
© 2013 Nature Education (a,b) Photos courtesy of Zachary Randall. All rights reserved. 
The group of fossils that is the focus of debates over primate origins is called the plesiadapiforms. This is an incredibly diverse group including more than 140 named species arranged into 11 different families. The first record of plesiadapiforms appears just as the non-avian dinosaurs were going extinct about 65 million years ago, near the beginning of the Paleocene. Some plesiadapiforms persist well into the Eocene, with the last species going extinct around 37 million years ago (Silcox & Gunnell, 2008). Over the course of its more than 25-million-year history, the group underwent an impressive adaptive radiation, producing forms with very distinctive dental adaptations including weird, multi-cusped upper incisors, and a diversity of very specialized lower premolars (Figure 2).
Figure 2: Scanning electron micrographs of plesiadapiform P4s and M1s in occlusal view: a) Purgatorius janisae (UCMP 107406, image reversed); b) Elphidotarsius florencae (USNM 9411); c) Tinimomys graybulliensis (YPM 33895); d) Picrodus silberlingi (AMNH 35456).
Note the wide range of different P4 morphologies, reflecting the adaptive diversity of plesiadapiforms. The white asterisk indicates the broad talonid basin in Purgatorius. Scales = 1 mm.
© 2013 Nature Education All rights reserved.
The most comprehensive analysis to date of the relationships among plesiadapiforms, primates, and closely related mammals is by Bloch and colleagues (2007; Figure 3). The results of this analysis support the idea that plesiadapiforms are more closely related to primates than to any other group. These authors argued that plesiadapiforms should therefore be considered stem primates; they adopted the name Euprimates (Hofstetter, 1977) for living primates and any fossil forms that exhibit all of the features of modern primates listed above. It is worth noting, however, that not all researchers are convinced by Bloch et al.'s (2007) results. These workers generally equate the Order Primates with Euprimates, excluding plesiadapiforms from the order. This leads to a very different conception of what constitutes primate origins than discussed here (e.g., Soligo & Martin, 2007), with the order not appearing until nearly 10 million years later, when the first forms that share traits such as the postorbital bar and nails on most digits (e.g., adapoids and omomyoids) are first found in the fossil record (e.g., Rose et al., 2012).
The broader relationships of Primates in Mammalia
Although there are continuing disagreements about where to draw the primate/non-primate line in the fossil record, more consensus exists about the identity of the closest living relatives of primates. Molecular analyses of mammalian relationships have fairly consistently placed primates in a group called Euarchonta with two other living orders: Scandentia and Dermoptera (Springer et al., 2004). Scandentians are small, quadrupedal animals that live in Southeast Asia. They are more commonly referred to as treeshrews, although not all of them live in the trees, and taxonomically they are not shrews. From 1922 (Carlsson, 1922) until 1980, treeshrews were often classified as primates. This idea was effectively refuted in a landmark edited volume (Luckett, 1980) that assessed the primate hypothesis using multiple lines of evidence. Even though trees shrews are no longer considered to be primates, familiarity with them is very important for researchers interested in primate origins because they provide the best living models for the earliest members of the Order. Indeed, the most primitive plesiadapiform known from a reasonably complete skeleton (Dryomomys szalayi) closely resembles the pen-tailed treeshrew, Ptilocercus lowii (Figure 4), below the head (Bloch et al., 2007). These similarities suggest that the first primate probably looked quite a bit like Ptilocercus, and supports the idea (Szalay & Drawhorn, 1980) that primates evolved from an already arboreal ancestor.
Figure 4: Ptilocercus lowii (the pen-tailed treeshrew).
Ptilocercus is the most primitive living treeshrew (Sargis, 2004) and represents the best extant model for the common ancestor of all Primates (including plesiadapiforms).
© 2013 Public Domain Zoological Society of London, 1848 Some rights reserved.
Figure 5: Labial view of the mandible of a dermopteran, Galeopterus variegatus (AMNH/Mammalogy: 106628).
Note the distinctive, comb-like morphology of the first two lower incisors. Scale = 2 mm.
© 2013 Nature Education Photo courtesy of Zachary Randall. All rights reserved.
Where, when, and why did primates evolve?
The earliest known plesiadapiforms are placed in the genus Purgatorius. Although there is a fragment of a tooth for this genus that has been described as coming from the same deposit as a Triceratops skeleton (Van Valen & Sloan, 1965), this deposit includes a mixture of material of different ages (Clemens, 2004). More firmly dated specimens are known from the earliest part of the Paleocene, however, so it is clear that even if Purgatorius did not overlap in time with the non-avian dinosaurs, it was one of the first groups to exploit the new opportunities created by their extinction (Johnston & Fox, 1984; Clemens, 2004).
Although the age and primitive morphology of Purgatorius would suggest an origin of primates around 65 million years ago, molecular dates for the origin of the order are generally at least 10 million years earlier, well before the Cretaceous-Tertiary boundary (Springer et al., 2003). If this is the case, we may be missing or not recognizing a significant part of the early history of the order. Alternatively, this discrepancy could reflect problems with the assumptions underlying molecular clock models, such as constancy of evolutionary rate (Ho, 2008), and the difficulty of calibrating the clock (e.g., see discussion in Stauffer et al., 2001).
While the Southeast Asian location of the closest living relatives of primates might suggest an Asian origin for the order (Beard, 2004), the North American location of most primitive plesiadapiforms supports a North American origin instead (Bloch et al., 2007). This may be a product, however, of much greater sampling of the fossil record in North America. Indeed, there is now a relatively primitive plesiadapiform known from Asia (Asioplesiadapis youngi Fu et al., 2002; see discussion in Silcox, 2008), which suggests that further discoveries on that continent may make it seem a more plausible place of origin for Primates.
In terms of why primates evolved, most of the scenarios for primate origins that discuss plesiadapiforms (rather than those restricted to Euprimates) suggest a relationship to diet. Szalay, in his landmark 1968 paper, "The beginnings of Primates," wrote: "It is only an increasing occupation of feeding on fruits, leaves, and other herbaceous matter that explains the first radiation of primates" (p. 32), and Sussman and Raven (1978) included plesiadapiforms in their proposed co-evolutionary scenario between primates and flowering plants. Eriksson et al. (2000) document an increase in the volume of fruit and proportion of animal-dispersed flowering plants through the late Cretaceous into the Paleocene; early primates may have been one of the forces driving this change. These suggestions may seem surprising in light of the small, rather pointy teeth of Purgatorius (Figure 2a). Certainly in comparisons with modern primates this morphology would suggest a diet richer in insects than in plant materials (Kay & Cartmill, 1977). However, it is important to note that the features we use to differentiate Purgatorius and the other early plesiadapiforms from contemporaneous small mammals (e.g., broad talonid basins) are precisely those which can be related to a more diverse diet. So while we still have much to learn about the ecological profile of the earliest primates, a shift to a more omnivorous diet may have been one part of their success. A diffuse co-evolutionary relationship with flowering plants may have subsequently played a critical role in shaping the diversification of plesiadapiforms throughout the Paleocene (Sussman, 1991; Bloch et al., 2007).References and Recommended Reading
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