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Home , Allochrocebus, Cercopithecini, Guenon, Lesula, Mesopithecus, Old World monkey

Early from the late Miocene Baynunah Formation, Abu Dhabi, with implications for cercopithecoid biogeography and evolution

Christopher C. Gilberta,b,c,1, Faysal Bibid,e,f, Andrew Hillg, and Mark J. Beechh

aDepartment of Anthropology, Hunter College of the City University of New York, New York, NY 10065; bDepartments of Anthropology and , Graduate Center of the City University of New York, New York, NY 10016; cNew York Consortium in Evolutionary , New York, NY; dMuseum für Naturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany; eDepartment of Mammalogy, American Museum of Natural History, New York, NY 10024; fInstitut International de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements, IPHEP UMR CNRS 7262, Université de Poitiers, 86022 Poitiers Cedex, France; gDepartment of Anthropology, Yale University, New Haven, CT 06520-8277; and hCoastal Heritage and Palaeontology Section, Historic Environment Department, Abu Dhabi Tourism and Culture Authority, Abu Dhabi, United Arab Emirates

Edited by Leslea J. Hlusko, University of California, Berkeley, CA, and accepted by the Editorial Board June 2, 2014 (received for review December 21, 2013) A newly discovered fossil (AUH 1321) from the Baynunah (5–9). Until now, no , extant or extinct, have ever been Formation, Emirate of Abu Dhabi, United Arab Emirates, is im- known outside of the African continent. portant in a number of distinct ways. At ∼6.5–8.0 Ma, it represents Three possible routes can be reasonably hypothesized for the earliest known member of the subfamily cercopithecine (and cercopithecoid) dispersal out of and found outside of Africa, and it may also be the earliest cercopithecine into Europe and Asia during the late Miocene: (i) over the in the fossil record. In addition, the fossil appears to represent the Mediterranean Basin or Straits of Gibraltar to the north/north- earliest member of the cercopithecine tribe (gue- west, (ii) across the Arabian Sinai Peninsula to the northeast, or nons) to be found anywhere, adding between 2 and 3.5 million y (iii) across the Arabian Straits of Bab el Mandeb to the east (Fig. ∼ – ( 50 70%) to the previous first-appearance datum of the crown 1). Fossil Macaca specimens from the terminal Miocene of Spain guenon clade. It is the only guenon—fossil or extant—known out- and Italy have been suggested to provide evidence for the use of side the continent of Africa, and it is only the second fossil monkey a route across the Mediterranean Basin or the Straits of Gibral- specimen so far found in the whole of Arabia. This discovery sug- — gests that identifiable crown guenons extend back into the Mio- tar via an ephemeral land bridge either immediately before or — cene epoch, thereby refuting hypotheses that they are a recent perhaps associated with the drop in Mediterranean sea levels radiation first appearing in the Pliocene or Pleistocene. Finally, the during the Messinian (∼6.0–5.3 Ma) (8–19). Paleontological new monkey is a member of a unique fauna that had dispersed from evidence for an Arabian route has been lacking, but paleoge- Africa and southern Asia into Arabia by this time, suggesting that ographic and paleoenvironmental work on circum-Arabia sug- the Arabian Peninsula was a potential filter for cross-continental gests that the region did not present a persistent ecological

faunal exchange. Thus, the presence of early cercopithecines on barrier to some amount of intercontinental exchange during the ANTHROPOLOGY the Arabian Peninsula during the late Miocene reinforces the prob- late Miocene (20). In fact, an established land connection through ability of a cercopithecoid dispersal route out of Africa through Sinai was probably present during this time period, and oceanic southwest Asia before Messinian dispersal routes over the Medi- spreading is not estimated to have begun in the southern Red Sea terranean Basin or Straits of Gibraltar. until around 5 Ma, with progressive development of open marine conditions throughout the Pliocene. Thus, before 6.5 Ma, a southern cercopithecid | Old World monkeys | Bab el Mandeb | | Sinai Significance ercopithecine monkeys (Order , Superfamily Cer- Ccopithecoidea, Cercopithecidae, Subfamily Cercopi- The primate subfamily Cercopithecinae represents the most thecinae), also known as cheek-pouch monkeys, are the most diverse and successful living Old World primate group, with speciose and widely distributed group of living Old World pri- a current distribution throughout Africa and Asia. However, mates. Recent molecular estimates date the divergence of Cer- how and when these monkeys dispersed out of Africa is not copithecinae from (leaf-eating monkeys) to between well understood. This paper is significant in its description of 17.6 Ma (range 21.5–13.9 Ma) and 14.5 Ma (range 16.2–12.8 Ma) a ∼6.5–8.0 million-y-old fossil guenon from Arabia represent- and the origin of crown Cercopithecinae to around 11.5 Ma (range ing the earliest cercopithecine (and only guenon) yet known 13.9–9.2 Ma) (1, 2). However, the earliest known fossil cercopi- outside of Africa. Furthermore, this specimen extends the thecines only appear much later, around 7.4 Ma in the Turkana guenon fossil record by at least 2.3 million y and may represent Basin of East Africa (3, 4). the earliest known cercopithecine as well. Because Old World Cercopithecine monkeys are divided into two tribes: Cerco- monkeys appear to have dispersed out of Africa sometime during the Late Miocene, the Arabian fossils also have impli- pithecini, including African guenons (Allenopithecus, Miopithecus, cations for dispersal scenarios in bio- , , , Cercopithecus), and Papio- geography and evolution. nini, which includes African and Eurasian (Macaca)as well as African papionins (Papio, Lophocebus, Rungwecebus, Author contributions: C.C.G., F.B., A.H., and M.J.B. designed research; C.C.G., F.B., A.H., , , Cercocebus). Of the living cercopithe- and M.J.B. performed research; C.C.G., F.B., and A.H. contributed new reagents/analytic tools; C.C.G., F.B., and A.H. analyzed data; and C.C.G., F.B., and A.H. wrote the paper. cines, only two genera are known outside of the African continent, both of them papionins: Papio (found on the Arabian Peninsula) The authors declare no conflict of interest. This article is a PNAS Direct Submission. L.J.H. is a guest editor invited by the Editorial and Macaca (found throughout Southern and Southeast Asia, and Board. introduced in Gibraltar). The earliest fossil cercopithecines known 1To whom correspondence should be addressed. E-mail: [email protected]. outside of Africa are attributed to the Macaca and appear to This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. be latest Miocene or early Pliocene in age (∼6.0–5.0 Ma) (Fig. 1) 1073/pnas.1323888111/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1323888111 PNAS | July 15, 2014 | vol. 111 | no. 28 | 10119–10124 Downloaded by guest on September 29, 2021 Fig. 1. Hypothesized cercopithecoid dispersal routes out of Africa in relation to the known late Miocene fossil record. The oldest cercopithecine, lothagamensis (light blue circles), is known from ∼7.4–6.1 Ma in the Turkana Basin and Tugen Hills, Kenya (3, 4, 41). An unnamed fossil papionin (purple circle) is known from the late Miocene of Ongoliba, Congo (5, 57). Macaca spp. (dark blue circles) are located throughout North Africa at sites ranging in age from ∼6.5–5.5 Ma (5, 8, 58, 59), and Macaca spp. first appear in Europe ∼6.0–5.3 Ma and in China in the early Pliocene (5–9). The oldest colobine outside of Africa, Mesopithecus (green circles), is known from a number of late Miocene sites securely dated between ∼8.5 and 5.3 Ma in Greece, Macedonia, Italy, Ukraine, Iran, Afghanistan, possibly Pakistan, and China (46–48). Three dispersal routes for cercopithecoids can be hypothesized: route 1 imagines a dispersal event over the Straits of Gibraltar or Mediterranean Basin into Europe and Asia; route 2 postulates a dispersal event through the Arabian Sinai Peninsula; and route 3 suggests a migration over the Arabian Straits of Bab el Mandeb. The discovery of AUH 1321 and AUH 35 in Abu Dhabi at >6.5–8 Ma (red circle), con- temporaneous with the first appearance of Mesopithecus sp. in Eurasia and ∼1–2 million y earlier than the appearance of Macaca spp. in Eurasia, suggests scenarios 2 and 3 were possible before scenario 1. None of these scenarios is mutually exclusive and may have occurred in combination or succession.

route in the region of the Straits of Bab el Mandeb was also possible Baynunah Formation (24). More recently, a team led by F.B., (Fig. 1) (21). A.H., and M.J.B. conducted annual field expeditions from 2006 to Although Arabia is a large area of the earth, fossil monkeys 2011 (28–30). The Baynunah sediments indicate the presence of have so far been represented by only a single specimen, an iso- a large meandering river system, with flanking woodlands, pos- lated male lower canine (AUH 35), discovered in 1989 by A.H. sibly tapering off into grasslands and even desert laterally (31). and Peter Whybrow in the late Miocene Baynunah Formation, The accompanying fauna is unique, but largely represented by Abu Dhabi, United Arab Emirates (22–25). The specimen came a typical African wooded grassland assemblage with aquatic from Jebel Dhanna, site JDH-3 (JD-3 in refs. 24 and 26) (Fig. 2), a locality now lost to industrial development. Because male elements, including hippopotamids, bovids, giraffids, suids, a range cercopithecid lower canines are not metrically identifiable be- of carnivores including a mustelid, a large felid, and two hyaenids, yond the Family level of classification (23), AUH 35 was de- equids, a number of rodents, an insectivore, and no less than three scribed as a cercopithecid with indeterminate affinities. Here we proboscidean taxa. The Baynunah rivers were well populated with report the discovery of a second monkey specimen from the diverse fish, turtles, crocodiles, gavials, and molluscs, and there are Baynunah Formation in Abu Dhabi (AUH 1321), found almost interesting birds and land reptiles as well. For a full current faunal 20 y after the first. AUH 1321 clearly represents a cercopithecine list, see refs. 29 and 30. and, because it is dated to between 6.5 and 8.0 Ma, it is the oldest cercopithecine yet known outside of Africa and possibly the oldest cercopithecine in the fossil record. Thus, the discovery of AUH 1321 provides the earliest paleontological evidence of cercopithecine dispersal out of continental Africa and possibly hints at an Arabian cercopithecoid dispersal route into Eurasia during the Late Miocene (Fig. 1). Furthermore, we believe AUH 1321 can be attributed to the Cercopithecini (guenons) and, therefore, it represents the only record of this tribe, living or fossil, yet known outside of Africa. Geological and Paleoenvironmental Context The Baynunah Formation (27) is a sequence of sandstones and mudstones that are mainly fluvial in origin and that contain fossils at several levels. Up to some 60 m thick, the Formation is exposed along more than 200 km of the Abu Dhabi coast in the western Al Gharbia region, and extends more than 30 km inland. Fig. 2. Map illustrating the location of the two fossil sites in the Baynunah From 1988 to 1995 a joint research project conducted by A.H. Formation that have produced fossil monkeys. Top Right Inset shows the lo- and Peter Whybrow recovered a diverse fossil fauna from the cation of the SHU 2–2 excavation (kite aerial photography by Nathan Craig).

10120 | www.pnas.org/cgi/doi/10.1073/pnas.1323888111 Gilbert et al. Downloaded by guest on September 29, 2021 Overall, the Baynunah fauna is taxonomically most similar to contemporaneous sites in Libya, Chad, Ethiopia, and Kenya, and very different from those in Greece, Turkey, and Iran (e.g., refs. 24, 29, and 30). Most Baynunah fossil taxa appear African in origin and are not known in Asia. However, there are some southern Asian forms (i.e., Siwaliks) that are never recorded in Africa, such as Propotamochoerus hysudricus (32) and Pachyportax latidens, implying that the Arabian late Miocene fauna was not merely a biogeographic extension of Africa, but was a unique combination of southern Asian and African elements, possibly reflecting an intermittent and not totally permeable corridor of faunal exchange between these neighboring continents. Very few Baynunah are shared with Europe and Asia north of the Himalayan-Zagros- Tauride mountain belt, although Prostrepsiceros aff. vinayaki and possibly some rodents may be examples (33, 34). Thus, given the evidence at hand, Arabia in the late Miocene appears to have served as a cross-continental corridor for only a few taxa, but for the majority it was a filter through which only those taxa with suitable adaptations were occasionally able to disperse into, although not always beyond. The fossil tooth AUH 1321 was found in 2009 at site SHU 2-2 [24.1148N 52.4320E (WGS84)], a sublocality of SHU 2 (S2 in refs. 24 and 26) on the island of Shuwaihat (Fig. 2). The fossil came from a small area (∼4 × 4 m) of sedimentary exposure that has produced a large number of microvertebrate fossils through dry sieving. The specimen was spotted by F.B. on a surface that had been scooped and sieved the previous day. The color and relatively good preservation of the specimen—in a coastal area where sun, humidity, gypsum, and halite quickly attack fossil specimens as they approach the surface—attests to very recent surface exposure and negligible postexposure transport. Site SHU 2-2 has also produced a diverse microvertebrate fauna, including new specimens of the murid rodent Abudhabia baynunensis (35), a new thryonomyid rodent, Protohummus dango (33), and several fish and squamate taxa currently under study. ANTHROPOLOGY Geological Age Radiometric dates are not available for the Baynunah Forma- Fig. 3. Photographs of AUH 1321 in (A) occlusal, (B) mesial, (C) distal, (D) tion, and paleomagnetic estimates are not well resolved (22, 36). buccal, and (E) lingual views. Mesial is to the right in A and E; mesial is to the Biochronological comparisons with African and Asian faunas in- left in D. (Scale bars, ∼1 mm) (photos by Eric Lazo-Wasem). dicate an age between 8 Ma and 6.5 Ma, and most probably around 7 Ma (29, 30, 37, 38). The upper limit is suggested by the suid from the late Miocene of Africa or the Miocene-Pliocene of P. hysudricus (32), which is not known from the Siwaliks in Pakistan Eurasia (Table 2). later than 6.8 Ma, with an estimated last appearance datum of 6.5 The crown of AUH 1321 is moderately worn and in good Ma (39). The presence of the hippopotamid Archaeopotamus and condition overall, although it is slightly damaged and abraded in the ratite Diamantornis laini in both the Baynunah and the Lower Member of the Nawata Formation (7.4–6.54 Ma) at Lothagam, places (Fig. 3 and Fig. S1). The crown is high relative to the low Kenya also indicates an age greater than 6.5 Ma (38, 40, 41). The cusps, as is typical of cercopithecines (Fig. 3, Fig. S1, and Table lower limit is not so well resolved, but is unlikely to be greater than S1). A mesial contact facet is present at the mesial end of the 8 Ma. This age estimate puts the Baynunah specimens in the time tooth. The mesial shelf is relatively elongated and slightly larger range of the earliest known cercopithecine fossils in Africa, all than the distal shelf/fovea, another feature shared with extant from Kenya: Parapapio lothagamensis, known to occur in the Lower cercopithecines (43). The median buccal cleft is relatively wide Nawata Formation at Lothagam (3, 4) and also at around 6.1 Ma and of moderate depth, not nearly as deep as typically seen in in the Lukeino Formation, Tugen Hills (42). colobines. There is a very small and shallow mesial buccal cleft present, but no visible distal buccal cleft. However, because the Description and Comparison of AUH 1321 distobuccal portion of the enamel is damaged, it is impossible to

AUH 1321 is a small lower left molar, most likely an M1, pre- say with certainty whether a distal buccal cleft or distal contact serving the majority of the crown and the distal root; the mesial facet was present or absent (Fig. 3 and Fig. S1). root is broken off (Fig. 3 and Fig. S1). The mesial and distal The tooth is relatively narrow, as shown by the mesiodistal lophids are complete and transversely oriented with the distal length divided by the mesial or distal width (Table 1), but not as lophid being slightly wider than the mesial lophid. Comparisons narrow as is typically seen in cercopithecine dP4s, confirming with extant and late Miocene cercopithecoids are given in Table 1 that the specimen most likely represents an adult molar (Tables and Tables S1 and S2. Given available M1 crown measure- S1 and S2). The preserved distal root is moderate in length and ments, AUH 1321 represents a small cercopithecine, similar in robust at its proximal and distal ends, also indicating a perma- size to extant vervet monkeys or blue monkeys, (estimated body nent rather than deciduous tooth. The distal root appears slightly mass ∼3.9–5.8 kg, based on cercopithecine regressions of female broken at the apex, exposing a small opening. An alternative ’ M1 mesial buccolingual width and male M1 mesiodistal length explanation might be that the root s apex was still slightly open; from ref. 7), but much smaller than any known cercopithecine however, given the moderate wear of the tooth combined with an

Gilbert et al. PNAS | July 15, 2014 | vol. 111 | no. 28 | 10121 Downloaded by guest on September 29, 2021 Table 1. Selected comparative measurements (mm) of the in the Abu Dhabi cercopithecines and other Old World monkeys

M1 M1 M1

Taxon Source Specimen no. M1 MD M1 MBL M1 DBL M1 NH/NR M1 Flare (MD/MBL) (MD/DBL) (MBL/DBL)

Cercopithecini Present study AUH 1321 6.2 4.5 4.6 67 66 138 135 98 sp. indet. Late Miocene fossil macaques Macaca libyca (59) Average 7.6 7.5 7.3 — 53* 101.0 103.8 102.7 Macaca sp. Menacer (59) Average 9.1 7.6 6.8 — 65* 120.5 133.8 111.0 Macaca sp. Almenara (8) IPMC 11676 8.0 6.2 6.1 ——129.0 131.1 101.6 As Sahabi (59) Average 7.6 6.4 6.3 — 51* 119.0 121.2 101.9 (8, 59) Fossil 8.1 6.9 6.6 — 57 117 122 104 average (8, 59) Fossil macaque 7.6–9.1 6.2–7.6 6.1–7.3 — 51–65 101–129 104–134 102–111 species range Extant macaques Macaca (45, 60) Extant macaque 7.0 5.4 5.3 49 68 129 130 101 average (45, 60) Extant macaque 6.4–7.5 4.9–5.8 4.7–5.8 44–61 66–71 120–137 119–140 98–104 species range Extant guenons Cercopithecus/ (60, PRIMO, Extant guenon 5.6 4.0 4.2 61 61 139 133 96 Chlorocebus present study) average (60, PRIMO, Extant guenon 5.0–6.3 3.6–4.4 3.8–4.7 39–77 55–63 130–144 130–137 89–100 present study) species range

In addition to measurements collected during the course of this study, comparative measurements are derived from refs. 8, 43, 45, 59, and 60, as well as

from the PRIMO (Primate Morphology) database, access courtesy of E. Delson. —, unavailable measurement; *, estimated from M2 values in ref. 59; DBL, maximum distal buccolingual width measured across the distal lophid; MBL, maximum mesial buccolingual width measured across the mesial lophid; MD, maximum mesiodistal length; NH/NR, notch height/crown height below the notch [see Benefit (43, 45, 61) for details]; species range, range of values among species averages within a given group. Flare measured as in Benefit (43, 45, 61) and lower values indicate higher degrees of flare. Note that AUH 1321 is most

similar to extant small-bodied guenons in M1 size and shape. See also Table 2 and Fig. S4. For a more complete list of taxa, see Tables S1–S3.

irregular shaped opening (Fig. 3 and Fig. S1), we believe that the taxon (Table S6). However, AUH 35 is also within the size range former is more likely. In either case, the distal root would have of modern macaques and the fossil colobine Mesopithecus, been even longer than is preserved, and long robust roots with no making it equally possible that multiple cercopithecoid taxa and sign of lingual resorption are typical of permanent rather than subfamilies are being sampled (Table S6). deciduous teeth (Figs. S2 and S3 and Tables S2 and S3). Al- though the distal root of AUH 1321 is angled posteriorly, rem- Discussion iniscent of a deciduous premolar, it is within the variation seen Although sparse, the cercopithecoids of the Baynunah Forma- among M1s of living cercopithecines, and a discriminant func- tion in Arabia are both chronologically and biogeographically tions analysis of five crown and root shape variables demon- highly significant. AUH 1321 represents the earliest appearance strates that AUH 1321 is most likely an M1 rather than a dP4, of the subfamily Cercopithecinae outside of Africa and, together, with a >99% probability (more specifically a guenon M1, with AUH 1321 and AUH 35 provide tantalizing evidence for a po- a >97% probability) (Figs. S2 and S3 and Tables S1–S3). tential primate dispersal route through Arabia and into southern AUH 1321 displays low-to-moderate flare, in contrast to most Asia and Europe during the latest Miocene (Fig. 1). Although papionin permanent molars and cercopithecine dP4s, and is guenons do not appear to have ever dispersed into Europe and more similar to the condition seen in the permanent molars of Asia, it is clear that other cercopithecines (and colobines) did, colobines, some extant macaques, and some cercopithecin taxa and the presence of two monkey specimens in the Late Miocene (Table 1 and Tables S1–S3) (44, 45). The overall size and shape of Arabia suggests that Arabia provided suitable environments for of the tooth—small, narrow, low-to-moderately flaring, elon- cercopithecoid primates dispersing out of Africa (see reconstructed gated basin, and a distally expanded lophid—is differentiated woodlands, above) (23, 29–30). Thus, although the appearance of from extant small-bodied and fossil macaques and is most similar these monkeys in the Arabian Peninsula does not refute a Gibraltar to non-Allenopithecus cercopithecins among extant cercopithe- or Mediterranean dispersal route for cercopithecoids during the cine taxa. A phylogenetic analysis of 13 dental characters con- Messinian Crisis, it does suggest that an Arabian dispersal route for firms that AUH 1321 is most similar to the tribe Cercopithecini Old World monkeys was possible earlier, in pre-Messinian times among extant cercopithecine taxa (Fig. S4 and Tables S4 and (Fig. 1). In fact, the earliest securely dated cercopithecoids known S5). Thus, we assign AUH 1321 to Cercopithecini sp. indet until from Europe and Asia are late Miocene specimens placed in the more material becomes available. Although it appears that AUH colobine genus Mesopithecus, ∼8.5–5.3 Ma (46–48), roughly con- 1321 most probably represents a new taxon, we refrain from temporaneous with the Baynunah Formation and consistent with naming a new genus and species in the absence of a more di- a pre-Messinian route through Arabia in the Late Miocene (Fig. 1). agnostic type specimen. The size of the lower male canine AUH Because AUH 35 is within the size range of Mesopithecus pentelicus 35, the only other fossil monkey known from Abu Dhabi, is also lower canines (Table S6), it is possible that the Baynunah Formation smaller than any known fossil cercopithecine from North Africa captures a snapshot of both cercopithecines and colobines exiting and within the range of living guenons, being closest in size to Africa during the late Miocene. Additional evidence of limited late Cercopithecus mitis among extant Cercopithecus taxa and making Miocene cross-continental faunal exchange between Africa, Arabia, it possible that AUH 1321 and AUH 35 represent the same and Asia may also be provided by the bovid Prostrepsiceros cf.

10122 | www.pnas.org/cgi/doi/10.1073/pnas.1323888111 Gilbert et al. Downloaded by guest on September 29, 2021 Table 2. Body mass estimates (kg) for selected extant and fossil cercopithecine taxa Taxon Average male mass Average female mass

Cercopithecini sp. indet. AUH 1321 5.8 3.9 Late Miocene/Plio-Pleistocene Cercopithecines Parapapio lothagamensis 10.5 8.0 Papionin sp. indet., Ongoliba 9.5 6.5 Macaca libyca 10.0 9.5 As Sahabi papionin 11.0 8.5 Macaca sp., Menacer 10.0 7.0 Macaca sp., Almenara 11.5 8.0 cf Macaca sp., Moncucco 12.0 8.0 9.5 6.0 Macaca sylvanus ?prisca 12.0 — Macaca sylvanus ?florentina 13.0 10.5 Macaca palaeindica 13.0 — Macaca sylvanus ?pliocena 14.0 7.5 Macaca anderssoni 14.0–17.0 10.5 Procynocephalus subhimalayanus 13.0 24.0 avernensis 31.0 19.0 Paradolichopithecus sushkini 36.0 35.0 Extant small cercopithecines Cercopithecus cephus 3.8 2.7 Macaca fascicularis 5.0 3.0 Chlorocebus aethiops 5.1 3.6 Cercopithecus ascanius 5.5 2.5 Macaca mulatta 6.2 — Cercopithecus neglectus 6.9 4.2 Macaca nigra 7.5 4.7 Cercopithecus mitis 8.0 3.9 Macaca nemestrina 8.0–11.5 5.0–6.5 Macaca sylvanus 15.0 10.0

Fossil cercopithecine and body mass estimates from Delson et al. (7) or derived from equations therein. Note that AUH 1321 is much smaller than any known Late Miocene cercopithecine and most similar in size to small-bodied guenons among living taxa. Taxa in bold are most similar in size to AUH 1321. ANTHROPOLOGY

vinayaki,thefishClarias sp., the carnivore genus Plesiogulo,andthe provides the first paleontological evidence refuting the hypoth- rodent genera Myocricetodon and Abudhabia (30, 33–35). esis that the crown guenons are only a recent Pliocene-Pleis- A phylogenetic analysis of 13 cercopithecine dental characters tocene radiation (56). demonstrates the affinities of AUH 1321 to Cercopithecini, es- The discovery of AUH 1321, in addition to AUH 35, em- tablishing its position as the earliest known guenon in the fossil phasizes the problem of determining the existence of rare taxa in record by at least 2.3 million y (49), and the only guenon yet geographically isolated fossil situations, and making paleoge- known outside of Africa (Fig. S4 and Tables S4 and S5). On both ographical inferences in the absence of more comprehensive molecular and morphological grounds, nearly all authorities rec- fossil data. If it were not for these two teeth we would not know ognize Allenopithecus as the most basal extant member of the that monkeys existed in the late Miocene of Arabia. Perhaps for Cercopithecini (e.g., refs. 1, 44, 50–54). Allenopithecus is primi- similar reasons we are currently ignorant of other possible im- tive relative to other cercopithecin taxa in that it retains basally portant yet rare elements of the fauna, including other primates flaring molars, a feature shared with both papionins and more (e.g., other monkeys, , and early hominins). Further sus- primitive cercopithecoids, such as . In contrast, tained paleontological exploration of Arabia and northern Africa AUH 1321 clearly displays relatively nonflaring molars, a distinctive is necessary if we are to clarify primate and mammalian evolu- feature shared exclusively with non-Allenopithecus guenons among tion and biogeography during the late Miocene. modern cercopithecins. Thus, the available morphological evi- ACKNOWLEDGMENTS. We thank the American Museum of Natural History dence suggests that AUH 1321 is a crown guenon nested within for the use of CT Scan imaging equipment; Eric Delson, Steve Frost, John the modern non-Allenopithecus radiation (Fig. S4). Among non- Fleagle, Peter Ungar, and Mike Plavcan for their assistance and advice; Sarah Allenopithecus guenons, molecular estimates place the divergence Elton, two anonymous reviewers, and the editor for their helpful comments; between the terrestrial Chlorocebus/Erythrocebus/Allochrocebus Eileen Westwig for access to primate specimens at the American Museum of Natural History; Darrin Lunde and Nicole Edmison for access to primate clade and the arboreal Cercopithecus clade between 8.8 and specimens at the Smithsonian National Museum of Natural History; Andrea 7.6 Ma (55), making it possible that AUH 1321 is an early Baden for help with Fig. 1; Eric Lazo-Wasem for the photographs forming member of one of these two clades as suggested by our phylo- Fig. 3; Emily Goble for biostratigraphical discussions; and B. Kraatz, E. Moacdieh, M. Al Neyadi, and staff from the Historic Environment De- genetic analysis of cercopithecine dental characters (Fig. S4). partment at the Abu Dhabi Tourism and Culture Authority, who participated In any case, the fact that the Baynunah Formation predates the in fieldwork efforts. Our research in Abu Dhabi has been supported by the estimated appearance of the Cercopithecus common ancestor (4.9– Historic Environment Department of the Abu Dhabi Tourism and Culture 4.3 Ma) and the Chlorocebus/Erythrocebus/Allochrocebus common Authority (formerly Abu Dhabi Authority for Culture and Heritage); an – International Research Fellowship Award (National Science Foundation ancestor (5.5 5.0 Ma) (55) suggests that the Arabian specimen Grant 0852975) (to F.B); the Revealing Hominid Origins Initiative (National belongs to a distinct genus. In addition, to our knowledge, it Science Foundation Grant BCS-0321893); the Institute International de

Gilbert et al. PNAS | July 15, 2014 | vol. 111 | no. 28 | 10123 Downloaded by guest on September 29, 2021 Paléoprimatologie et Paléontologie humaine; the Agence Nationale de la Gilder Graduate School and the Gerstner Scholars Program; and a grant from Recherche (ANR-09-BLAN-0238); the Yale Peabody Museum; the Richard the Yale University President’s Office (to A.H.).

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