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PERSPECTIVE

New perspectives on anthropoid origins

Blythe A. Williamsa,1, Richard F. Kaya, and E. Christopher Kirkb aDepartment of Evolutionary Anthropology, Duke University, Durham, NC 27708-0383; and bDepartment of Anthropology, University of Texas, Austin, TX 78712

Edited by Alan Walker, Penn State University, University Park, PA, and approved January 19, 2010 (received for review September 22, 2009)

Adaptive shifts associated with origins are brought to light as we examine the human record and study our own genome and that of our closest relatives. However, the more ancient roots of many human characteristics are revealed through the study of a broader array of living anthropoids and the increasingly dense fossil record of the earliest anthropoid radiations. Genomic data and of early in Asia and clarify relationships among the major of primates. Progress in comparative anatomy, genomics, and molecular biology point to key changes in sensory ecology and brain organization that ultimately set the stage for the emergence of the human lineage.

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uman evolution did not begin primates ( and ) is also well fossil record remains sparse and 6–8 million years ago with the supported by morphological and molecular incomplete. For decades, anthropoid H phylogenetic split between the evidence. However, the question of ancestors were sought in two taxonomically and human line- whether are more closely related diverse radiations of primarily ages. Although the ape–human transition to anthropoids or strepsirrhines has been taxa: Omomyiformes and is of tremendous interest to specialists and less clear. Some classifications united (sometimes identified at the family or the general public, many key genetic tarsiers with strepsirrhines in the suborder superfamily level). Both groups are events and adaptive shifts leading to the Prosimii because they retain primitive common in North American and European origin of had already been set in features such as grooming and an Paleogene faunas and also occur in Africa motion long before this split. The seeds of unfused mandibular symphysis. An and Asia (5). Omomyiforms are fi fi these changes can be identi ed in the alternative phylogenetic classi cation considered haplorhines, and adapiforms earlier branches of the primate family tree, linked tarsiers with anthropoids in the strepsirrhines by most workers (6–8, but many millions of years in the past. semiorder Haplorhini. Evidence for a see ref. 9), although few characters Changes in sensory ecology, increases in haplorhine comes from an unambiguously support omomyiforms as brain size, and reorganization of the increasingly long list of derived hard and ’ haplorhine. The German adapiform brain s components set the stage for the soft tissue morphological features and from was described as having features development of language and for many of molecular features. Molecular phylo- allying it, and by extension, other our other exceptional cognitive abilities. genetic studies using DNA sequence data adapiforms with Haplorhini (10). Recent well-publicized descriptions of generally failed to provide strong support However, Darwinius and other adapiforms fossil primates from Africa and Eurasia for either Haplorhini or Prosimii (1). share derived features with extant have reignited interest in the origins of However, genetic markers called strepsirrhines and lack derived features Anthropoidea—monkeys, , and hu- short interspersed elements (SINEs) offer shared by extant tarsiers and anthropoids mans. Fossil discoveries are expanding our strong evidence in support of both – understanding of the diversity and bio- haplorhine and strepsirrhine . (6, 11 15). geography of this clade. Developments in SINEs are short segments of DNA that Several hypotheses about and molecular phylogenetics are establishing insert into the genome at apparently anthropoid origins have been proposed. a phylogenetic framework of living pri- random positions and are excellent Some researchers argue that anthropoids mates against which hypotheses about re- phylogenetic markers with an extraor- and tarsiers share a common ancestor lationships of fossils can be tested. dinarily low probability of convergent within a paraphyletic Omomyiformes Advances in genomics and the study of evolution (2). Because there are billions of whereas others assert that only tarsiers living primate ecology are enabling us to potential insertion sites in any primate have omomyiform ancestry. An alternative understand key adaptive changes in an- genome, the probability of a SINE hypothesis that we favor is that the tarsier- thropoid evolution and have reframed inserting precisely in the same locus in two anthropoid clade is the sister group of many of our adaptive questions about separate evolutionary lineages is omomyiforms as a whole. This last option human origins in the context of deep time. “exceedingly minute, and for all practical is supported by a comprehensive phylo- Here we review recent fossil discoveries, purposes, can be ignored” (p. 151, ref. 3). genetic analysis (11). The hypothetical developments in the study of the sensory Five SINEs support haplorhine mono- common ancestor of tarsiers, anthro- ecology and neurobiology of anthro- phyly to the exclusion of strepsirrhines and poids, and omomyiforms has yet to be poids, and implications from genetic eight are shared among strepsirrhines (4). identified, but must predate the oldest research that bear on the study of Thus, the haplorhine–strepsirrhine split omomyiform, , from the anthropoid origins. may now be regarded as fact and must earliest Eocene of , underlie any phylogenetic reconstruction Europe, and Asia (16). Phylogenetics of Crown Primates of fossil primates. In the past, separate origins were Identification of which taxa of early considered for the two living clades of primates are haplorhines and which are Author contributions: B.A.W., R.F.K., and E.C.K. analyzed anthropoid primates: the strepsirrhines is an ongoing challenge data and B.A.W., R.F.K., and E.C.K. wrote the paper. platyrrhines and the Old World because homoplasy is common, the The authors declare no conflict of interest. catarrhines. Today, Anthropoidea is evolutionary acquisition of diagnostic This article is a PNAS Direct Submission. accepted universally as a monophyletic haplorhine and anthropoid characters 1To whom correspondence should be addressed. E-mail: group. The monophyly of the strepsirrhine occurred in mosaic fashion, and the [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.0908320107 PNAS | March 16, 2010 | vol. 107 | no. 11 | 4797–4804 Downloaded by guest on September 28, 2021 What Is an Anthropoid? features found in living anthropoids, as have given rise to catarrhines, platyrrhines, By definition, crown Anthropoidea includes discussed below. We do not know the both, or neither (13). all , living and fossil, descended character states for many of the presumed Propliopithecids ( and from the last common ancestor of extant Eocene anthropoids from Asia because ) are widely accepted as the anthropoids. Stem Anthropoidea includes they are not yet known from adequate earliest definitive representatives of the all fossil taxa that are more closely related cranial materials. Postcranial materials of catarrhine primates because of their to crown anthropoids than they are to putative Asian stem anthropoids have been dental formula (two premolars) and tarsiers, but are outside the anthropoid found in isolation, complicating their details of anatomy greatly fi . Crown anthropoids share a speci c attribution. resembling early catarrhines number of important features. On the from east Africa (37). Oligopithecids may basis of evidence from comprehensive Anthropoid Fossils and be catarrhines. They retain some primitive phylogenetic analyses (11, 13, 17, 18), Revised Dates characteristics (small brain and unfused many of these features are considered Afro-Arabian Anthropoids. In the past mandibular symphysis), yet the dental synapomorphies. Four peculiarities of decade, finds of fossil primates have formula, large ascending process of the embryonic implantation have been augmented our picture of early premaxilla, and several features of the described (19). Extant anthropoids share talus, , and femur all support anthropoids and broadened the fi 27 Alu-SINE markers (4). Most biogeographic focus of studies of catarrhine af nities (33). anthropoids have orbits that are relatively anthropoid origins (Fig. 1 and Fig. 2). Other poorly known African Paleogene small, forward facing, and convergent (20). Early anthropoids are best known from primates may be anthropoids. A bony lamina posterior to the orbit the phylogenetically diverse faunas of (late , Morocco) was described completely separates the eyes from the Afro-Arabia, especially those of the as an omomyiform (38) but may be a stem chewing muscles in the temporal fossa Fayum Depression in Egypt. The youngest anthropoid (11, 38, 39) or a stem (21). A number of other soft-tissue of the Fayum primate-bearing deposits euprimate (40). , from the features of the visual system (e.g., an all- date to the , ∼30 Ma, whereas Egyptian Oligocene, resembles stem cone retinal fovea) are anthropoid the oldest are late Eocene, ∼37 Ma (29). anthropoids (41), but also tarsiids (13, 42). synapomorphies (22). Anthropoid features There are 15 known Fayum anthropoid Algeripithecus (early to middle Eocene, of the auditory region include a distinctive genera from four clades: parapithecoids, Algeria) was commonly recognized as an configuration of the internal carotid proteopithecids, oligopithecids, anthropoid (39), but recent discoveries of arterial system that supplies the orbit and and propliopithecids. more complete specimens suggest that it much of the cerebrum (23). The middle Parapithecoids (e.g., Simonsius, is not anthropoid but instead may belong ear cavity of the temporal bone extends , Parapithecus, and ) are to the Azibiidae (43). Azibiids are argued forward into an air-filled accessory thought by some researchers to be stem to be adapiforms, early euprimates, chamber containing a network of bony catarrhines (30), but cranial and plesiadapiforms (possible stem primates), trabeculae (24). The tympanic bone that postcranial evidence suggests that they are or even nonprimates (14, 44, 45), and supports the eardrum is fused to the bony stem anthropoids (13). Proteopithecids there is no consensus on their sidewall of the middle ear. Early fusion (Proteopithecus, and possibly Serapia) have phylogenetic position. However, the occurs in both the frontal metopic suture been linked with the oligopithecids oblique orientation of the lacrimal canal and the mandibular symphysis (25). The and (8), but relative to the infraorbital canal indicates body of the mandible is relatively deep postcranial evidence (31–33) does not that they are not crown haplorhines (26). Other anthropoid dental features support this link. Proteopithecids also ( and anthropoids have more include small, vertically implanted and exhibit some resemblance to platyrrhines vertically oriented lacrimal canals) (43). spatulate lower incisors, simplified molar (34), but a close phylogenetic relationship Specimens attributed to another supposed trigonids, and lower third molars with between these two groups is supported anthropoid from Algeria, Tabelia, are short heels (8). neither by character distribution (35) nor probably specimens of Algeripithecus or The bony anatomy of the crown phylogenetic analyses (36). The most that Azibius (43). This leaves Altiatlasius as the anthropoid foot is distinctive: the facet can be said is that proteopithecids are only potentially anthropoid African taxon between the talus and fibula is steep-sided, stem anthropoids sufficiently primitive to from earlier than ∼37 Ma. and the groove for the tendon of the flexor fibularis muscle is in a midtrochlear position (6). The calcaneus is wide with a shortened heel and a distinctive calcaneocuboid joint shape (27). The peroneal tubercle on the first metatarsal that receives the tendon of the peroneus longus muscle is reduced in size (28). We do not know the in which most of these crown anthropoid features evolved. Most features probably appeared in a mosaic fashion in stem anthropoids. Some features may be primitive for Anthropoidea or Primates as a whole and others may have evolved in parallel in multiple crown anthropoid clades. We do know that most of the hard tissue features mentioned above are evident in Afro- Fig. 1. Map showing localities containing Paleogene anthropoids. Coastlines and continental positions Arabian fossils of late Eocene age, represent roughly the situation in the early Eocene to early Oligocene. Modified from refs. 8 and 119 although several taxa lack some derived with a more northerly position of India.

4798 | www.pnas.org/cgi/doi/10.1073/pnas.0908320107 Williams et al. Downloaded by guest on September 28, 2021 to the correct taxon has been particularly vexing. Cranial fragments from Burma that were attributed to (60) and indicated the lack of postorbital Adapiformes MiMiocene closure may not belong to that taxon (61). However, a newly reconstructed face of Oligocene Siamopithecus displays the highly convergent and frontated orbits and relatively short face typical of anthropoids Eocene (62). Tarsal elements thought to belong to Amphipithecus also show anthropoid features (63), and most phylogenetic Paleocene analyses link amphipithecids with anthropoids (11, 13, 18).

Strepsirrhini Haplorhini Adaptations in Anthropoidea Fig. 2. A dendrogram of primate phylogeny with Eocene families represented based on cladograms Body Mass. With the exception of the of refs. 11, 13, and 18. Paleocene through Miocene is proportionally scaled; post Miocene time is not Neotropical , , and to scale. squirrel monkeys, most extant anthropoids weigh more than 1 kg. By contrast, early and middle Eocene anthropoids were all Stem Anthropoids of Asia. was have the other crown anthropoid small-bodied, and no major size increases described in 1994 on the basis of hallmarks (23, 24, 55). in anthropoids are detected until the late fragmentary dental remains from the The phylogenetic position of Asian Eocene or early Oligocene (Table 1). All middle Eocene of China (46) and was eosimiids is more controversial. known eosimiid primates weighed less placed in a previously undescribed Comprehensive phylogenetic analyses than a few hundred grams. Some eosimiids anthropoid family, . To date, as place eosimiids within the anthropoid were extremely small (11, 47, 64)—the size many as 11 species in six genera are radiation (11–13), and the majority of of the dwarf —or even smaller if attributed to the Eosimiidae. Eosimias and specialists agree that eosimiids are stem some isolated middle Eocene foot bones Phenacopithecus are known from the anthropoids. Nevertheless, some from anthropoids are considered (65). middle Eocene of China (e.g., 46, 47). researchers continue to question the Amphipithecids ranged from a few Outside of China, Bahinia and another anthropoid status of some or all eosimiids hundred grams up to 6 kg or more. Body eosimiid have been recovered from the (42, 51, 56, 57). Although eosimiids retain mass estimates for Fayum anthropoids late middle Eocene of Burma (48, 49), and many primitive dental features (e.g., ranged from a few hundred grams for Phileosimias is known from the Oligocene paraconid on lower molars, an unfused smaller parapithecoids up to 5–6 kg for of Pakistan (50). mandibular symphysis), they also propliopithecids (66, 67). The fossil record for eosimiids was demonstrate key anthropoid The small size of the earliest anthropoids synapomorphies, including tarsal features has important implications for extended to the Indian subcontinent by the fl discovery of fragmentary dental remains of (midtrochlear position of the exor reconstructing the feeding ecology of the fi ∼ Anthrasimias (11) from the early Eocene bularis, a wide calcaneus with a earliest anthropoids. Primates over 500 g shortened heel, and a reduced peroneal fi of India. Some researchers have argued are able to use leaves to ful ll their protein tubercle of the first metatarsal), a deep that Anthrasimias is an adapiform (12, 51), requirements, whereas those less than mandible, various dental features (absence ∼ although a calcaneus from the same 500 g rely on insects. Leaf consumption of a Nannopithex-fold on the upper and insect predation require very different locality is eosimiid-like in its proportions molars, transverse lower molar and morphology (12). digestive and sensory specializations, some protocristid, and the lower third molar of which are described below. Southeast Asian Amphipithecidae were with a weak heel), and a deep suborbital first described from fragments of upper and part of the maxilla (27, 47, 49, 58). To Diet. The dietary adaptations of fossil lower jaws (Amphipithecus, Pondaungia) date, however, no eosimiid crania preserve anthropoids have been reconstructed using from the late middle Eocene of Burma. In the diagnostically haplorhine or dental and mandibular structure, the past decade, much amphipithecid anthropoid anatomy of the orbit or ear microwear analysis, and estimations of material has been recovered from Burma region. Cranial resemblances between the body mass (11, 25, 53, 67–69). Asian (Myanmarpithecus, ) (52, 53), the eosimiid Bahinia and adapiforms have eosimiids and most of the late Eocene and late Eocene of Thailand (Siamopithecus) been proposed (56), but the specimen in Oligocene anthropoids of Egypt show (54), and the early Oligocene of Pakistan question is too crushed and distorted to dental adaptations for eating primarily (Bugtipithecus) (50). make such claims reliable. The mounting fruits. The majority of the smaller-bodied evidence is persuasive in favor of a stem taxa would have relied on insects for their Relationships of North African Anthropoids, anthropoid position for eosimiids. More source of protein, as do extant small- Eosimiids, and Amphipithecids. The complete cranial material may resolve bodied primates (70), but were not anthropoid status of the late Eocene to this issue. primarily insectivorous. The larger-bodied early Oligocene Afro-Arabian taxa is The anthropoid status of amphipithecids taxa would have used leaves as their undisputed because they are known from also is controversial. Their status as protein source, although they were not crania that possess the above-mentioned anthropoids has long been disputed committed folivores. A few Afro-Arabian derived anthropoid features of the orbit because they resemble various taxa might have been more predominantly and ear region, mandible, and teeth. Some omomyiforms, catarrhines, and (especially) folivorous. The amphipithecids appear to taxa (Catopithecus and Proteopithecus) lack adapiforms (30, 59). Difficulty in have had more divergent diets. Although a few features found in extant anthropoids attributing isolated postcranial elements fruit was a major food source, the larger (e.g., fused mandibular symphysis), but (some of which show adapiform features) taxa show massive jaws, deep faces, large

Williams et al. PNAS | March 16, 2010 | vol. 107 | no. 11 | 4799 Downloaded by guest on September 28, 2021 Table 1. Glossary of time periods and adaptive profiles of primates discussed in text

Adapiformes Clade of North American, Eurasian, and African Eocene to Miocene stem strepsirrhines: >90 species. Body mass: 100–7,000 g; most >1 kg. Mostly diurnal. Diet: leaves and fruit, a few specialized in insects. Active arboreal quadrupeds, some deliberate slow-climbing quadrupeds. Amphipithecidae Clade of Asian Eocene to Oligocene stem anthropoids: six species. Body mass: 130–5,900 g. Siamopithecus diurnal; activity pattern for other taxa unknown. Diet: fruit, nuts, seeds. Slow or active arboreal quadrupeds.* Clade of Old World monkeys and apes and all extinct species more closely related to this clade than to living New World monkeys (Platyrrhini), their sister group. Eocene ∼56 and ∼34 Ma. Early Eocene, ∼56 to ∼49 Ma; middle Eocene, ∼49 to ∼37 Ma; late: ∼37 to ∼34 Ma. † Eosimiidae Clade of Asian and African Eocene to Oligocene stem anthropoids: 11 species. Body mass: 30–280 g. Bahinia and Phenacopithecus diurnal; activity pattern for other taxa unknown. Diet: fruit and insects. Active arboreal quadrupeds.* Haplorhini Clade of tarsiers and anthropoids and all extinct species more closely related to this clade than to Strepsirrhini, their sister group. Miocene Epoch ∼23 to ∼5Ma Oligocene Epoch ∼34 to ∼23 Ma Oligopithecidae Clade of African late Eocene to Oligocene stem anthropoids or stem catarrhines: three species. Body mass: 770-1,200 g. Catopithecus diurnal; activity pattern of Oligopithecus unknown. Diet: leaves, fruit. Catopithecus was a slow-climbing arboreal quadruped. Omomyiformes Clade of North American, Eurasian, and African Eocene stem haplorhines: >95 species. Body mass: 35–1775 g; most <400 g. Most nocturnal. Diet: fruit and insects. Arboreal quadrupeds, some with a significant leaping component. Paleocene Epoch ∼66 to ∼56 Ma Paleogene Period Paleocene–Oligocene Epochs. Parapithecoidea Clade of African Eocene to Oligocene stem anthropoids (or stem catarrhines): 12 species. Body mass: 140–1,800 g. Most diurnal, but earliest (Biretia) nocturnal. Diet: fruit; Simonsius grangeri more folivorous. Active arboreal quadrupeds. Platyrrhini Clade of Neotropical monkeys and all extinct species more closely related to this clade than they are to living Catarrhini, their sister group. Prosimii Paraphyletic group that includes tarsiers and strepsirrhines. Propliopithecidae Clade of African Oligocene stem catarrhines: five species. Body mass: 2-4 kg,. Diurnal. Diet: fruit. Arboreal quadrupeds. Proteopithecidae Extinct clade of African late Eocene stem anthropoids: of two species. Body mass: 500-720 g. Diurnal. Diet: fruit, insects. Proteopithecus engaged in agile above-branch quadrupedalism and pronograde leaping. Strepsirrhini Clade of lemurs of Madagascar (Lemuroidea) and lorises of Africa and Asia (Lorisoidea) and all extinct species (Adapiformes) more closely related to this clade than they are to Haplorhini, their sister group. Tarsier A small, nocturnal, and insectivorous primate from Asia. The sister group of anthropoids.

*Isolated postcrania make attribution of locomotor patterns uncertain. †Includes Altiatlasius and Anthrasimias, whose status as eosimiids is controversial.

canines, and blunt cheek teeth with heavy lemurs (suggesting more leaping in focal length and an increased size of the apical wear indicating that they ingested omomyiforms). Likewise, the anterior retinal image. This eye morphology is one hard objects such as nuts and seeds. bowing and prominent third trochanter of of several derived features supporting very The dietary patterns of the earliest the femur and the morphology of the os high visual acuity in anthropoids (74). anthropoids broadly overlapped those of coxa attributed to eosimiids are similar to Furthermore, because cornea size places sympatric omomyiform and adapiform taxa late Eocene African anthropoids that are an upper limit on the amount of light that (11, 67), suggesting that gross dietary most often compared to living squirrel may be admitted to the eye, the derived changes were not important selective monkeys (31, 33). Allocation of postcrania eye morphologies shared by most living factors in the origin of anthropoids. The to the Amphipithecidae has been anthropoids almost certainly evolved in a fossil record suggests that relatively late- contested. A humerus attributed to common ancestor that was diurnal. occurring increases in body size led to Amphipithecus suggests that it was a slow- Consistent with their nocturnal habits, increased reliance on foods that are tough moving arboreal quadruped (69), but a tarsiers and owl monkeys exhibit large and/or hard or brittle (unripe fruits, nuts, talus allocated to the same taxon indicates corneas relative to eye size and thus lack leaves), which in turn probably selected for more active arboreal quadrupedal habits the characteristic eye morphology of (63). Late Eocene parapithecoids and stronger and more stable jaws (25). diurnal anthropoids (75). However, Proteopithecus often are compared to tarsiers exhibit highly unusual features for Locomotion. Several limb bones from the squirrel monkeys. Catopithecus differs nocturnally adapted species (76). Like Chinese middle Eocene have been from stem anthropoids in features of the attributed to eosimiids (27, 71). In the talus, suggesting that it was a slower, more anthropoids, but unlike all other eosimiid foot, the calcaneus is short and deliberate climber that may have used , tarsiers possess a retinal fovea broad, but the midcalcaneal portion is hind-limb suspensory postures (33). (a pit in the central retina) and a macula relatively long. This calcaneal morphology lutea (produced by a high concentration of is similar to that of the platyrrhine Saimiri, Eye. Most anthropoids differ from other carotenoid pigments around the fovea). the squirrel , and implies agile, primates and nonprimate mammals in Both features are best interpreted as above-branch quadrupedalism and having small corneas relative to eye size adaptations for enhanced visual acuity that pronograde leaping. The shorter, broader (72, 73). Reduction of cornea size in initially evolved in a diurnal setting. calcanei of eosimiids differ from those of anthropoids reflects a reconfiguration of Furthermore, the tarsier central retina has omomyiforms, which generally are the eye’s focusing apparatus (including the surprisingly high densities of cones. In this moderately elongated like those of mouse lens and cornea) that results in a greater respect, tarsiers resemble diurnal squirrels

4800 | www.pnas.org/cgi/doi/10.1073/pnas.0908320107 Williams et al. Downloaded by guest on September 28, 2021 and tree shrews and differ markedly from the tarsier septum represents a convergent genetic data suggest that such other nocturnal mammals (74). In total, adaptation necessitated by the evolution of “polymorphic ” has evolved these derived retinal features provide extremely large eyes (82, 83). Owls are multiple times among diurnal and support for the hypothesis that tarsiers are similar to tarsiers in having postorbital cathemeral lemuriform primates as well secondarily nocturnal and share a diurnal processes that are less extensive than (86, 87), although the functionality of common ancestor with anthropoids. It is anthropoid septa, in having rod- in lemurs needs to be more probable that most visual adaptations for dominated retinal foveae (lost in tytonid fully explored (88). Similarly, studies of high acuity found in anthropoids evolved owls), and in being predominantly Australian marsupials suggest that many initially in the haplorhine stem lineage and nocturnal (81). As a result, the common are routine trichromats like catarrhine that this heritage is partly obscured in occurrence of orbital insulating structures primates (89). These data reveal that tarsiers through a secondary adaptation to in owls, tarsiers, and anthropoids suggests excellent color vision based on the nocturnality. Middle Eocene tarsiers from that such structures theoretically could presence of three cone types is not as rare China have large orbits, suggesting that have evolved in either a nocturnal or a among mammals as was recently thought. tarsiers are genuine “living fossils” that diurnal setting, provided that eye size, eye have persisted more or less in their current and orbit orientation, and selection to Olfaction. As with color vision, studies of form for millions of years (77). maintain high acuity were contributing the primate olfactory system have been factors. At present, however, it is most revolutionized by the study of genes that Orbit. Anthropoids are unique among parsimonious to conclude that some kind code for olfactory receptor proteins mammals in having a thin bony partition of postorbital septum was present in a (ORPs) and vomeronasal receptor that isolates the orbit from the temporal diurnal common ancestor of tarsiers and proteins. These proteins are expressed in fossa. This partition, or postorbital septum, anthropoids because this ancestor specialized sensory epithelia and initiate a is formed chiefly by varying contributions presumably had large and convergent eyes transduction cascade when they bind with from the frontal, zygomatic, and (73, 81, 84) as well as the shared target molecules (odorants). Like most alisphenoid bones. Tarsiers resemble haplorhine features supporting very high mammals, many primates have both a anthropoids in exhibiting a partial visual acuity (74). “main” olfactory system (MOS) and an postorbital septum with contact between “accessory” olfactory system (AOS), with the zygomatic and alisphenoid bones, but Color Vision. Over the last two decades, receptors localized in the nasal mucosa unlike anthropoids, tarsiers retain broad studies of opsin genes and the and (VNO), confluence between the orbit and temporal photopigments that they encode have respectively. The MOS is often fossa inferior to the septum (21). revealed that most mammals, including characterized as detecting odors Observational and experimental data tarsiers and some lemurs, have color vision associated with a wide range of stimuli suggest that the postorbital septum is an that is based on two cone types (85). This such as food or predators, whereas the adaptation for preventing mechanical of color vision—in which one cone AOS is more narrowly specialized to disturbance of the eyes by contractions of class is maximally sensitive to blue-violet detect pheromones or other sociosexual the anterior temporalis muscle (78, 79). light and another to red-green light—is odors (90). The functional roles of the According to this “insulation hypothesis,” called “.” Dichromats are able MOS and AOS, however, are probably far haplorhines require postorbital septa to use these two cone types to discriminate more complex than this generalization because they evolved large and convergent between short and long wavelength light implies (90, 91). (i.e., forward-facing) eyes and orbits, thus and thus differ from a smaller assortment Living haplorhines have small olfactory bringing the eyes and temporalis muscles of mammals (including lorises, bushbabies, bulbs compared with most mammals and into close proximity. Maintaining and owl monkeys among primates) that lack the primitive “olfactory recess” in mechanical stability of the eyes is also are truly color-blind because they possess which olfactory mucosa is separated from particularly important for haplorhines, only one cone type (“monochromacy”). the main respiratory airway. As a result, given their high visual acuity (74, 80). Anthropoids are not uniform in their color haplorhines have generally been The fact that no other mammals have vision, but all diverge somewhat from the characterized as lacking well-developed postorbital septa has hindered comparative typical mammalian pattern of dichromacy olfactory abilities. However, recent tests of the insulation hypothesis. However, (85). Due to an ancient gene duplication comparative studies of the MOS suggest owls resemble tarsiers and anthropoids in event, catarrhines have three cone types that platyrrhines resemble strepsirrhines having a bony lamina (an expanded that are each maximally sensitive to and many other mammals in retaining a “postorbital process”) that shields the eye different regions of the visible spectrum. large proportion of functional ORP genes and redirects a key jaw adductor muscle This type of color vision (“routine (92–94). Because the olfactory bulb is posterior to the orbit (81). Owls also trichromacy”) is rare among mammals and primarily a relay between MOS receptors possess relatively large and convergent gives catarrhines the ability to discriminate in the nasal fossa and olfactory centers orbits, bringing the eyes and jaw adductors between short, middle, and long in the brain, the small size of the into close proximity, as in haplorhines. wavelengths of light. With the exception of platyrrhine olfactory bulb probably reflects These findings lend crucial comparative howler monkeys, platyrrhines lack the key a decrease in the total number of MOS support to the insulation hypothesis and gene duplication that confers routine receptor cells rather than a decrease in the suggest that haplorhines and owls evolved trichromacy on catarrhines. However, number of distinct ORP types. These analogous morphological solutions to the most platyrrhines do exhibit considerations suggest that although shared problem of mechanical polymorphism in the opsin gene expressed platyrrhines may not be able to detect interference between the eyes and jaw in the class of cones that is maximally volatile odorants at very low adductor muscles. sensitive to red-green light. Because this concentrations, they probably resemble One key question that remains gene is on the X chromosome, most strepsirrhines in retaining a keen ability to unresolved is how to account for the female platyrrhines inherit different alleles discriminate between families of odorants. distinctive circum-orbital morphology of for the red-green opsin locus and are As with color vision, it is mainly tarsiers. Although most researchers have functionally trichromats. Males, by catarrhines that stand out as unusual argued for homology between anthropoid contrast, receive only one red-green allele among primates in terms of their ORP and tarsier septa, others have argued that and are dichromats. The most recent gene complement. Up to 50% of the ORP

Williams et al. PNAS | March 16, 2010 | vol. 107 | no. 11 | 4801 Downloaded by guest on September 28, 2021 genes in Old World monkeys, apes, and of pheromonal communication that are anthropoid evolution accords well with the humans no longer code for functional commonly found in other primates and underlying genetic mechanisms that may receptor proteins (92–95). Apparently, nonprimate mammals. In light of these be associated with anthropoid brain loss of olfactory discriminative ability is distinct changes in their olfactory systems, evolution. The anthropoid clade has not an anthropoid characteristic generally it is intriguing that catarrhines, including experienced positive selection in genes that but is instead restricted mainly to humans, are known to respond to certain have a strong phenotypic effect on brain catarrhines. However, we still know very sociosexual odor cues and to exhibit a anatomy. For example, phylogenetically little about the precise relationship limited repertoire of pheromonal independent increases in anthropoid between olfactory bulb size and olfactory responses (101, 102). The mechanisms neocortex size are positively correlated abilities in primates. Likewise, the specific through which catarrhines sense these with increases in amino acid substitution in odorants detected by individual ORPs cues are not yet well understood but may the ASPM gene in a broad array of remain unknown in most cases, and thus partly involve trace-amine–associated primates (110). Differences in gene we do not yet fully understand the receptors expressed in the main olfactory expression or enzyme function in ASPM functionality of ORP genes. epithelium (103). remain to be demonstrated directly among As with variation in the MOS, the state species examined (111), but the ASPM of the anthropoid AOS is more Brain Size. Extant anthropoids exhibit an work highlights the need to extend complicated than might be expected on the upward “grade shift” in relative brain size comparisons beyond simply those within basis of the evident gross reductions of the compared to tarsiers and living humans or between humans and olfactory periphery. The VNO is the strepsirrhines (104). A number of adaptive (112). primary receptor organ of the AOS, and explanations have been proposed for this Genes that affect proteins important in accordingly much attention recently has shift, including enhanced environmental the machinery of aerobic energy been devoted to the presence or absence of mapping, dietary shifts, changes in the production also experienced positive this structure among primates. Catarrhines visual system, changes in social structure, selection in the anthropoid stem and its are unique among primates in lacking and enhanced domain–general cognition. descendant clades, whereas these genes are functional VNOs (91, 96). Early reports of Most of these proposals are bolstered by highly conserved in tarsiers, strepsirrhines, a functional VNO in humans are correlative distributions of brain size and mammals generally (1). It has been controversial and have not been supported versus behavioral traits in living species. hypothesized that changes to genes by subsequent anatomical research (97, The emergence of a more detailed fossil influencing aerobic metabolism may have 98). Although some adult catarrhines record is beginning to serve as an fueled the emergence of an enlarged, (including humans) may express a important test of these hypotheses. For energetically expensive anthropoid rudimentary VNO, such structures do not example, we now know that relative neocortex (1, 113). Another proposed contain a sensory epithelium, often do not increases in brain size occurred explanation for these changes involves communicate with the nasal fossa, and independently in catarrhines and provision of more energy for prolongation lack vomeronasal nerves to transmit platyrrhines (8, 105, 106) and that stem of the time to reach maturity or reductions information to the brain. More anthropoids (e.g., Simonsius) and even in the release of free radicals in aerobic importantly, the gene coding for the TRP2 stem catarrhines (Aegyptopithecus) and metabolic processes that may reduce tissue ion channel (which is critical for stem platyrrhines ( and damage and prolong life span (114). transduction by V1R receptor cells in the Homunculus) had brains broadly VNO) is nonfunctional in extant comparable in size to living strepsirrhines Biogeography catarrhines (99). (105, 107, 108). Thus, the larger brains of The continent of origin of anthropoid Together with data on the MOS, these living anthropoids evolved gradually and primates remains uncertain because early findings suggest that the reduced emphasis potentially could have been influenced by fossil occurrences are documented in both on olfaction that is generally characteristic different selective factors in platyrrhines Afro-Arabia and Asia and because the of anthropoids evolved in two major steps. and catarrhines. We can now also Tethys seaway between the two continents First, the complexity of the nasal cavity and establish that high visual acuity was well was evidently a permeable barrier to the size of the main olfactory epithelium developed in early anthropoids before a mammalian dispersal at various times were reduced in the haplorhine stem large brain evolved (109). during the Paleogene. The limited state of lineage. This anatomical reorganization Overall increase in brain size is, of our current knowledge about anthropoids was correlated with a reduction in the size course, not the whole story. The from the Paleocene and Eocene also of the MOS receptor cell population, a anthropoid brain also has been contributes to our uncertainty about where reduction in the size of the central targets reorganized, although only the outlines of various anthropoid groups originated. The of olfactory input in the brain (e.g., main this story have been gleaned from fossil strongest evidence for stem anthropoid olfactory bulb and olfactory cortex), and a . Reduction in the size of the origins is documented from middle Eocene corresponding reduction in olfactory olfactory bulb has already been mentioned. deposits in China and Southeast Asia, but sensitivity. Second, stem catarrhines lost a The size of the neocortex also has eosimiids may also be known from the early functional VNO as well as the ability to increased. Although the size of the brain of Eocene of India. Crown anthropoids produce a large fraction of their ORPs. Aegyptopithecus was smaller than that of certainly were present in Africa by the Although it is unclear why catarrhines living anthropoids, the area of the visual late Eocene. became less dependent on olfactory stimuli cortex exhibited an anthropoid-like Biogeographic hypotheses must be than other primates, some researchers expansion (106). Homunculus had an tempered by the discrepancy between have suggested that this de-emphasis on enlarged optic canal, indicating improved molecular and fossil-based estimates of olfaction was tied to the evolution of visual acuity in the small-brained stem branch times for the divergence of primates routine trichromacy (93, 99; but see ref. platyrrhine (107). Aegyptopithecus and from other mammals, haplorhines from 100). Irrespective of the causal agent, Simonsius (108) appear to have had strepsirrhines, and tarsiers from these findings provide further evidence smaller frontal neocortexes than do anthropoids. All molecularly based that catarrhine primates are highly derived living anthropoids. estimates for primate origins fall in the late in lacking the well-developed olfactory These independent increases in brain (83.3–70.6 Ma) and those for apparatus and sophisticated mechanisms size documented in the fossil record of the haplorhine–strepsirrhine split and

4802 | www.pnas.org/cgi/doi/10.1073/pnas.0908320107 Williams et al. Downloaded by guest on September 28, 2021 anthropoid–tarsier split are older than ∼56 will extend our understanding of the characteristic mainly of a more restricted Ma (115–118). In contrast, the oldest earliest branches of the anthropoid group—the catarrhines. Similarly, known fossil evidence for a “primate of radiation. Discordance between the fossil postorbital septa (found in all modern aspect” is early Eocene (∼55.8 record and molecular divergence estimates haplorhines) and routine trichromacy Ma) or late Paleocene if Altiatlasius is a is likely to decrease as we focus our efforts (characteristic of catarrhines) are known euprimate. The great antiquity of these on the Asian and African Paleocene to have evolutionary analogs among other molecular branch times is discordant with deposits. In the meantime, data vertebrates. Finally, fossil evidence reveals the evidence of the fossil record (14). accumulated over the last 15 years reveal that major increases in brain size occurred Molecular clock estimates of the many details about the early origins of independently in New World and Old splits among the major lineages of living monkeys, apes, and humans. Africa no World anthropoids. These revelations primates predates all known primates of longer holds the distinction of being the hold the key to understanding the initial modern aspect by up to 25 million years. only likely center for anthropoid origins, evolution of many distinctive human This discrepancy has given rise to and a diverse assemblage of early fossil characteristics—from our keen eyesight to suggestions that anthropoids had an anthropoids are now known from China, our poor sense of smell and large brain. African or Indo-Madagascan origin (57). India, and Southeast Asia. Like many human features, the first So far this hypothesis, like many others, All of the available fossil evidence adaptive shifts responsible for the lacks concrete support. Recent fossils suggests that anthropoids originated at very emergence of these characteristics are supporting the extension of the stem small size. Many of the key features of truly ancient, substantially predating the primate lineage to 65 million years (40) anthropoid sensory ecology and anatomy, appearance of a human evolutionary lessen this discrepancy. such as highly acute diurnal vision and lineage distinct from other primates. retinal foveae, are best interpreted as Summing Up having first evolved in stem haplorhines ACKNOWLEDGMENTS. We thank Kari Allen, Nate In the next decade, paleontological rather than in stem anthropoids. Other Dominy, Christine Drea, Daniel Gebo, Yasuhoro Go, Laurent Marivaux, Erik Seiffert, Mary Silcox, exploration in late Paleocene and early sensory features long thought to Derek Wildman, Greg Wray, and an anonymous Eocene deposits in Asia and Africa will characterize all anthropoids, such as an reviewer for advice, helpful conversations, and/or likely produce important new fossils that extreme reduction of olfactory abilities, are suggestions on the manuscript.

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