Early guenon from the late Miocene BaynunahFormation, Abu Dhabi, with implications forcercopithecoid biogeography and evolutionChristopher 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 Biology,Graduate Center of the City University of New York, New York, NY 10016; cNew York Consortium in Evolutionary Primatology, New York, NY; dMuseum fürNaturkunde, Leibniz Institute for Evolution and Biodiversity Science, 10115 Berlin, Germany; eDepartment of Mammalogy, American Museum of NaturalHistory, New York, NY 10024; fInstitut International de Paléoprimatologie, Paléontologie Humaine: Evolution et Paléoenvironnements, IPHEP UMR CNRS7262, Université de Poitiers, 86022 Poitiers Cedex, France; gDepartment of Anthropology, Yale University, New Haven, CT 06520-8277; and hCoastal Heritageand 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 monkey (AUH 1321) from the BaynunahFormation, Emirate of Abu Dhabi, United Arab Emirates, is im-portant in a number of distinct ways. At ∼6.5–8.0 Ma, it representsthe earliest knownmember of the primate subfamily Cercopithecinaefound outside of Africa, and it may also be the earliest cercopithecinein the fossil record. In addition, the fossil appears to represent theearliest member of the cercopithecine tribe Cercopithecini (gue-nons) to be found anywhere, adding between 2 and 3.5 million y(∼50–70%) to the previous first-appearance datum of the crownguenon clade. It is the only guenon—fossil or extant—known out-side the continent of Africa, and it is only the second fossil monkeyspecimen so far found in the whole of Arabia. This discovery sug-gests that identifiable crown guenons extend back into the Mio-cene epoch, thereby refuting hypotheses that they are a recentradiation first appearing in the Pliocene or Pleistocene. Finally, thenewmonkey is a member of a unique fauna that had dispersed fromAfrica and southern Asia into Arabia by this time, suggesting thatthe Arabian Peninsula was a potential filter for cross-continentalfaunal exchange. Thus, the presence of early cercopithecines onthe Arabian Peninsula during the late Miocene reinforces the prob-ability of a cercopithecoid dispersal route out of Africa throughsouthwest Asia before Messinian dispersal routes over the Medi-terranean Basin or Straits of Gibraltar.

cercopithecid | Old World monkeys | Bab el Mandeb | Mesopithecus | Sinai

Cercopithecine monkeys (Order Primates, Superfamily Cer-copithecoidea, Family Cercopithecidae, Subfamily Cercopi-

thecinae), also known as cheek-pouch monkeys, are the mostspeciose and widely distributed group of living Old World pri-mates. Recent molecular estimates date the divergence of Cer-copithecinae from Colobinae (leaf-eating monkeys) to between17.6 Ma (range 21.5–13.9 Ma) and 14.5 Ma (range 16.2–12.8 Ma)and the origin of crown Cercopithecinae to around 11.5 Ma (range13.9–9.2 Ma) (1, 2). However, the earliest known fossil cercopi-thecines only appear much later, around 7.4 Ma in the TurkanaBasin of East Africa (3, 4).Cercopithecine monkeys are divided into two tribes: Cerco-

pithecini, including African guenons (Allenopithecus, Miopithecus,Chlorocebus, Erythrocebus, Allochrocebus, Cercopithecus), and Papio-nini, which includes African and Eurasian macaques (Macaca) aswell as African papionins (Papio, Lophocebus, Rungwecebus,Theropithecus, Mandrillus, Cercocebus). Of the living cercopithe-cines, only two genera are known outside of the African continent,both of them papionins: Papio (found on the Arabian Peninsula)andMacaca (found throughout Southern and Southeast Asia, andintroduced inGibraltar). The earliest fossil cercopithecines knownoutside ofAfrica are attributed to the genusMacaca and appear tobe latest Miocene or early Pliocene in age (∼6.0–5.0 Ma) (Fig. 1)

(5–9). Until now, no guenons, extant or extinct, have ever beenknown outside of the African continent.Three possible routes can be reasonably hypothesized for

cercopithecine (and cercopithecoid) dispersal out of Africa andinto Europe and Asia during the late Miocene: (i) over theMediterranean Basin or Straits of Gibraltar to the north/north-west, (ii) across the Arabian Sinai Peninsula to the northeast, or(iii) across the Arabian Straits of Bab el Mandeb to the east (Fig.1). Fossil Macaca specimens from the terminal Miocene of Spainand Italy have been suggested to provide evidence for the use ofa route across the Mediterranean Basin or the Straits of Gibral-tar via an ephemeral land bridge either immediately before—orperhaps associated with—the drop in Mediterranean sea levelsduring the Messinian (∼6.0–5.3 Ma) (8–19). Paleontologicalevidence for an Arabian route has been lacking, but paleoge-ographic and paleoenvironmental work on circum-Arabia sug-gests that the region did not present a persistent ecologicalbarrier to some amount of intercontinental exchange during thelate Miocene (20). In fact, an established land connection throughSinai was probably present during this time period, and oceanicspreading is not estimated to have begun in the southern Red Seauntil around 5 Ma, with progressive development of open marineconditions throughout the Pliocene. Thus, before 6.5 Ma, a southern

Significance

The primate subfamily Cercopithecinae represents the mostdiverse and successful living Old World primate group, witha current distribution throughout Africa and Asia. However,how and when these monkeys dispersed out of Africa is notwell understood. This paper is significant in its description ofa ∼6.5–8.0 million-y-old fossil guenon from Arabia represent-ing the earliest cercopithecine (and only guenon) yet knownoutside of Africa. Furthermore, this specimen extends theguenon fossil record by at least 2.3 million y and may representthe earliest known cercopithecine as well. Because Old Worldmonkeys appear to have dispersed out of Africa sometimeduring the Late Miocene, the Arabian fossils also have impli-cations for dispersal scenarios in Old World monkey bio-geography and evolution.

Author contributions: C.C.G., F.B., A.H., and M.J.B. designed research; C.C.G., F.B., A.H.,and M.J.B. performed research; C.C.G., F.B., and A.H. contributed new reagents/analytictools; C.C.G., F.B., and A.H. analyzed data; and C.C.G., F.B., and A.H. wrote the paper.

The authors declare no conflict of interest.

This article is a PNAS Direct Submission. L.J.H. is a guest editor invited by the EditorialBoard.1To whom correspondence should be addressed. E-mail: cgilbert@hunter.cuny.edu.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1323888111/-/DCSupplemental.

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route in the region of the Straits of Bab el Mandeb was also possible(Fig. 1) (21).Although Arabia is a large area of the earth, fossil monkeys

have so far been represented by only a single specimen, an iso-lated male lower canine (AUH 35), discovered in 1989 by A.H.and Peter Whybrow in the late Miocene Baynunah Formation,Abu Dhabi, United Arab Emirates (22–25). The specimen camefrom Jebel Dhanna, site JDH-3 (JD-3 in refs. 24 and 26) (Fig. 2),a locality now lost to industrial development. Because malecercopithecid lower canines are not metrically identifiable be-yond the Family level of classification (23), AUH 35 was de-scribed as a cercopithecid with indeterminate affinities. Here wereport the discovery of a second monkey specimen from theBaynunah Formation in Abu Dhabi (AUH 1321), found almost20 y after the first. AUH 1321 clearly represents a cercopithecineand, because it is dated to between 6.5 and 8.0 Ma, it is the oldestcercopithecine yet known outside of Africa and possibly theoldest cercopithecine in the fossil record. Thus, the discovery ofAUH 1321 provides the earliest paleontological evidence ofcercopithecine dispersal out of continental Africa and possiblyhints at an Arabian cercopithecoid dispersal route into Eurasiaduring the Late Miocene (Fig. 1). Furthermore, we believe AUH1321 can be attributed to the Cercopithecini (guenons) and,therefore, it represents the only record of this tribe, living orfossil, yet known outside of Africa.

Geological and Paleoenvironmental ContextThe Baynunah Formation (27) is a sequence of sandstones andmudstones that are mainly fluvial in origin and that containfossils at several levels. Up to some 60 m thick, the Formation isexposed along more than 200 km of the Abu Dhabi coast in thewestern Al Gharbia region, and extends more than 30 km inland.From 1988 to 1995 a joint research project conducted by A.H.

and Peter Whybrow recovered a diverse fossil fauna from the

Baynunah Formation (24). More recently, a team led by F.B.,A.H., and M.J.B. conducted annual field expeditions from 2006 to2011 (28–30). The Baynunah sediments indicate the presence ofa large meandering river system, with flanking woodlands, pos-sibly tapering off into grasslands and even desert laterally (31).The accompanying fauna is unique, but largely represented bya typical African wooded grassland assemblage with aquaticelements, including hippopotamids, bovids, giraffids, suids, a rangeof carnivores including a mustelid, a large felid, and two hyaenids,equids, a number of rodents, an insectivore, and no less than threeproboscidean taxa. The Baynunah rivers were well populated withdiverse fish, turtles, crocodiles, gavials, and molluscs, and there areinteresting birds and land reptiles as well. For a full current faunallist, see refs. 29 and 30.

Fig. 1. Hypothesized cercopithecoid dispersal routes out of Africa in relation to the known late Miocene fossil record. The oldest cercopithecine, Parapapiolothagamensis (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 eventover the Straits of Gibraltar or Mediterranean Basin into Europe and Asia; route 2 postulates a dispersal event through the Arabian Sinai Peninsula; and route3 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, suggestsscenarios 2 and 3 were possible before scenario 1. None of these scenarios is mutually exclusive and may have occurred in combination or succession.

Fig. 2. Map illustrating the location of the two fossil sites in the BaynunahFormation that have produced fossil monkeys. Top Right Inset shows the lo-cation of the SHU 2–2 excavation (kite aerial photography by Nathan Craig).

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Overall, the Baynunah fauna is taxonomically most similar tocontemporaneous sites in Libya, Chad, Ethiopia, and Kenya, andvery different from those in Greece, Turkey, and Iran (e.g., refs. 24,29, and 30). Most Baynunah fossil taxa appear African in originand are not known in Asia. However, there are some southernAsian forms (i.e., Siwaliks) that are never recorded in Africa, suchas Propotamochoerus hysudricus (32) and Pachyportax latidens,implying that the Arabian late Miocene fauna was not merelya biogeographic extension of Africa, but was a unique combinationof southern Asian and African elements, possibly reflecting anintermittent and not totally permeable corridor of faunal exchangebetween these neighboring continents. Very few Baynunah speciesare shared with Europe and Asia north of the Himalayan-Zagros-Tauride mountain belt, although Prostrepsiceros aff. vinayaki andpossibly some rodents may be examples (33, 34). Thus, given theevidence at hand, Arabia in the late Miocene appears to haveserved as a cross-continental corridor for only a few taxa, but for themajority it was a filter through which only those taxa with suitableadaptations were occasionally able to disperse into, although notalways 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 inrefs. 24 and 26) on the island of Shuwaihat (Fig. 2). The fossilcame from a small area (∼4 × 4 m) of sedimentary exposure thathas produced a large number of microvertebrate fossils throughdry sieving. The specimen was spotted by F.B. on a surface thathad been scooped and sieved the previous day. The color andrelatively good preservation of the specimen—in a coastal areawhere sun, humidity, gypsum, and halite quickly attack fossilspecimens as they approach the surface—attests to very recentsurface exposure and negligible postexposure transport. Site SHU2-2 has also produced a diverse microvertebrate fauna, includingnew specimens of the murid rodent Abudhabia baynunensis (35),a new thryonomyid rodent, Protohummus dango (33), and severalfish and squamate taxa currently under study.

Geological AgeRadiometric dates are not available for the Baynunah Forma-tion, and paleomagnetic estimates are not well resolved (22, 36).Biochronological comparisons with African and Asian faunas in-dicate an age between 8 Ma and 6.5 Ma, and most probably around7 Ma (29, 30, 37, 38). The upper limit is suggested by the suidP. hysudricus (32), which is not known from the Siwaliks in Pakistanlater than 6.8 Ma, with an estimated last appearance datum of 6.5Ma (39). The presence of the hippopotamid Archaeopotamus andthe ratite Diamantornis laini in both the Baynunah and the LowerMember of the Nawata Formation (7.4–6.54 Ma) at Lothagam,Kenya also indicates an age greater than 6.5 Ma (38, 40, 41). Thelower limit is not so well resolved, but is unlikely to be greater than8 Ma. This age estimate puts the Baynunah specimens in the timerange of the earliest known cercopithecine fossils in Africa, allfrom Kenya: Parapapio lothagamensis, known to occur in the LowerNawata Formation at Lothagam (3, 4) and also at around 6.1 Main the Lukeino Formation, Tugen Hills (42).

Description and Comparison of AUH 1321AUH 1321 is a small lower left molar, most likely an M1, pre-serving the majority of the crown and the distal root; the mesialroot is broken off (Fig. 3 and Fig. S1). The mesial and distallophids are complete and transversely oriented with the distallophid being slightly wider than the mesial lophid. Comparisonswith extant and late Miocene cercopithecoids are given in Table 1and Tables S1 and S2. Given available M1 crown measure-ments, AUH 1321 represents a small cercopithecine, similar insize to extant vervet monkeys or blue monkeys, (estimated bodymass ∼3.9–5.8 kg, based on cercopithecine regressions of femaleM1 mesial buccolingual width and male M1 mesiodistal lengthfrom ref. 7), but much smaller than any known cercopithecine

from the late Miocene of Africa or the Miocene-Pliocene ofEurasia (Table 2).The crown of AUH 1321 is moderately worn and in good

condition overall, although it is slightly damaged and abraded inplaces (Fig. 3 and Fig. S1). The crown is high relative to the lowcusps, as is typical of cercopithecines (Fig. 3, Fig. S1, and TableS1). A mesial contact facet is present at the mesial end of thetooth. The mesial shelf is relatively elongated and slightly largerthan the distal shelf/fovea, another feature shared with extantcercopithecines (43). The median buccal cleft is relatively wideand of moderate depth, not nearly as deep as typically seen incolobines. There is a very small and shallow mesial buccal cleftpresent, but no visible distal buccal cleft. However, because thedistobuccal portion of the enamel is damaged, it is impossible tosay with certainty whether a distal buccal cleft or distal contactfacet was present or absent (Fig. 3 and Fig. S1).The tooth is relatively narrow, as shown by the mesiodistal

length divided by the mesial or distal width (Table 1), but not asnarrow as is typically seen in cercopithecine dP4s, confirmingthat the specimen most likely represents an adult molar (TablesS1 and S2). The preserved distal root is moderate in length androbust at its proximal and distal ends, also indicating a perma-nent rather than deciduous tooth. The distal root appears slightlybroken at the apex, exposing a small opening. An alternativeexplanation might be that the root’s apex was still slightly open;however, given the moderate wear of the tooth combined with an

Fig. 3. Photographs of AUH 1321 in (A) occlusal, (B) mesial, (C) distal, (D)buccal, and (E) lingual views. Mesial is to the right in A and E; mesial is to theleft in D. (Scale bars, ∼1 mm) (photos by Eric Lazo-Wasem).

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irregular shaped opening (Fig. 3 and Fig. S1), we believe that theformer is more likely. In either case, the distal root would havebeen even longer than is preserved, and long robust roots with nosign of lingual resorption are typical of permanent rather thandeciduous teeth (Figs. S2 and S3 and Tables S2 and S3). Al-though the distal root of AUH 1321 is angled posteriorly, rem-iniscent of a deciduous premolar, it is within the variation seenamong M1s of living cercopithecines, and a discriminant func-tions analysis of five crown and root shape variables demon-strates that AUH 1321 is most likely an M1 rather than a dP4,with a >99% probability (more specifically a guenon M1, witha >97% probability) (Figs. S2 and S3 and Tables S1–S3).AUH 1321 displays low-to-moderate flare, in contrast to most

papionin permanent molars and cercopithecine dP4s, and ismore similar to the condition seen in the permanent molars ofcolobines, some extant macaques, and some cercopithecin taxa(Table 1 and Tables S1–S3) (44, 45). The overall size and shapeof the tooth—small, narrow, low-to-moderately flaring, elon-gated basin, and a distally expanded lophid—is differentiatedfrom extant small-bodied and fossil macaques and is most similarto non-Allenopithecus cercopithecins among extant cercopithe-cine taxa. A phylogenetic analysis of 13 dental characters con-firms that AUH 1321 is most similar to the tribe Cercopitheciniamong extant cercopithecine taxa (Fig. S4 and Tables S4 andS5). Thus, we assign AUH 1321 to Cercopithecini sp. indet untilmore material becomes available. Although it appears that AUH1321 most probably represents a new taxon, we refrain fromnaming a new genus and species in the absence of a more di-agnostic type specimen. The size of the lower male canine AUH35, the only other fossil monkey known from Abu Dhabi, is alsosmaller than any known fossil cercopithecine from North Africaand within the range of living guenons, being closest in size toCercopithecus mitis among extant Cercopithecus taxa and makingit possible that AUH 1321 and AUH 35 represent the same

taxon (Table S6). However, AUH 35 is also within the size rangeof modern macaques and the fossil colobine Mesopithecus,making it equally possible that multiple cercopithecoid taxa andsubfamilies are being sampled (Table S6).

DiscussionAlthough sparse, the cercopithecoids of the Baynunah Forma-tion in Arabia are both chronologically and biogeographicallyhighly significant. AUH 1321 represents the earliest appearanceof the subfamily Cercopithecinae outside of Africa and, together,AUH 1321 and AUH 35 provide tantalizing evidence for a po-tential primate dispersal route through Arabia and into southernAsia and Europe during the latest Miocene (Fig. 1). Althoughguenons do not appear to have ever dispersed into Europe andAsia, it is clear that other cercopithecines (and colobines) did,and the presence of two monkey specimens in the Late Mioceneof Arabia suggests that Arabia provided suitable environments forcercopithecoid primates dispersing out of Africa (see reconstructedwoodlands, above) (23, 29–30). Thus, although the appearance ofthese monkeys in the Arabian Peninsula does not refute a Gibraltaror Mediterranean dispersal route for cercopithecoids during theMessinian Crisis, it does suggest that an Arabian dispersal route forOld World monkeys was possible earlier, in pre-Messinian times(Fig. 1). In fact, the earliest securely dated cercopithecoids knownfrom Europe and Asia are late Miocene specimens placed in thecolobine genus Mesopithecus, ∼8.5–5.3 Ma (46–48), roughly con-temporaneous with the Baynunah Formation and consistent witha pre-Messinian route through Arabia in the Late Miocene (Fig. 1).Because AUH 35 is within the size range ofMesopithecus pentelicuslower canines (Table S6), it is possible that the Baynunah Formationcaptures a snapshot of both cercopithecines and colobines exitingAfrica during the late Miocene. Additional evidence of limited lateMiocene cross-continental faunal exchange between Africa, Arabia,and Asia may also be provided by the bovid Prostrepsiceros cf.

Table 1. Selected comparative measurements (mm) of the dentition in the Abu Dhabi cercopithecines and other Old World monkeys

Taxon Source Specimen no. M1 MD M1 MBL M1 DBL M1 NH/NR M1 FlareM1

(MD/MBL)M1

(MD/DBL)M1

(MBL/DBL)

Cercopithecinisp. indet.

Present study AUH 1321 6.2 4.5 4.6 67 66 138 135 98

Late Miocenefossil macaquesMacaca libyca (59) Average 7.6 7.5 7.3 — 53* 101.0 103.8 102.7Macaca sp. Menacer (59) Average 9.1 7.6 6.8 — 65* 120.5 133.8 111.0Macaca sp. Almenara (8) IPMC 11676 8.0 6.2 6.1 — — 129.0 131.1 101.6As Sahabi (59) Average 7.6 6.4 6.3 — 51* 119.0 121.2 101.9

(8, 59) Fossil macaqueaverage

8.1 6.9 6.6 — 57 117 122 104

(8, 59) Fossil macaquespecies range

7.6–9.1 6.2–7.6 6.1–7.3 — 51–65 101–129 104–134 102–111

Extant macaquesMacaca (45, 60) Extant macaque

average7.0 5.4 5.3 49 68 129 130 101

(45, 60) Extant macaquespecies range

6.4–7.5 4.9–5.8 4.7–5.8 44–61 66–71 120–137 119–140 98–104

Extant guenonsCercopithecus/Chlorocebus

(60, PRIMO,present study)

Extant guenonaverage

5.6 4.0 4.2 61 61 139 133 96

(60, PRIMO,present study)

Extant guenonspecies range

5.0–6.3 3.6–4.4 3.8–4.7 39–77 55–63 130–144 130–137 89–100

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 asfrom 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 amongspecies 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 mostsimilar 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.

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vinayaki, the fish Clarias sp., the carnivore genus Plesiogulo, and therodent genera Myocricetodon and Abudhabia (30, 33–35).A phylogenetic analysis of 13 cercopithecine dental characters

demonstrates the affinities of AUH 1321 to Cercopithecini, es-tablishing its position as the earliest known guenon in the fossilrecord by at least 2.3 million y (49), and the only guenon yetknown outside of Africa (Fig. S4 and Tables S4 and S5). On bothmolecular and morphological grounds, nearly all authorities rec-ognize Allenopithecus as the most basal extant member of theCercopithecini (e.g., refs. 1, 44, 50–54). Allenopithecus is primi-tive relative to other cercopithecin taxa in that it retains basallyflaring molars, a feature shared with both papionins and moreprimitive cercopithecoids, such as Victoriapithecus. In contrast,AUH 1321 clearly displays relatively nonflaring molars, a distinctivefeature shared exclusively with non-Allenopithecus guenons amongmodern cercopithecins. Thus, the available morphological evi-dence suggests that AUH 1321 is a crown guenon nested withinthe modern non-Allenopithecus radiation (Fig. S4). Among non-Allenopithecus guenons, molecular estimates place the divergencebetween the terrestrial Chlorocebus/Erythrocebus/Allochrocebusclade and the arboreal Cercopithecus clade between 8.8 and7.6 Ma (55), making it possible that AUH 1321 is an earlymember of one of these two clades as suggested by our phylo-genetic analysis of cercopithecine dental characters (Fig. S4).In any case, the fact that the Baynunah Formation predates theestimated appearance of the Cercopithecus common ancestor (4.9–4.3 Ma) and the Chlorocebus/Erythrocebus/Allochrocebus commonancestor (5.5–5.0 Ma) (55) suggests that the Arabian specimenbelongs to a distinct genus. In addition, to our knowledge, it

provides the first paleontological evidence refuting the hypoth-esis that the crown guenons are only a recent Pliocene-Pleis-tocene radiation (56).The discovery of AUH 1321, in addition to AUH 35, em-

phasizes the problem of determining the existence of rare taxa ingeographically isolated fossil situations, and making paleoge-ographical inferences in the absence of more comprehensivefossil data. If it were not for these two teeth we would not knowthat monkeys existed in the late Miocene of Arabia. Perhaps forsimilar reasons we are currently ignorant of other possible im-portant yet rare elements of the fauna, including other primates(e.g., other monkeys, apes, and early hominins). Further sus-tained paleontological exploration of Arabia and northern Africais necessary if we are to clarify primate and mammalian evolu-tion and biogeography during the late Miocene.

ACKNOWLEDGMENTS. We thank the American Museum of Natural Historyfor the use of CT Scan imaging equipment; Eric Delson, Steve Frost, JohnFleagle, Peter Ungar, and Mike Plavcan for their assistance and advice; SarahElton, two anonymous reviewers, and the editor for their helpful comments;Eileen Westwig for access to primate specimens at the American Museum ofNatural History; Darrin Lunde and Nicole Edmison for access to primatespecimens at the Smithsonian National Museum of Natural History; AndreaBaden for help with Fig. 1; Eric Lazo-Wasem for the photographs formingFig. 3; Emily Goble for biostratigraphical discussions; and B. Kraatz,E. Moacdieh, M. Al Neyadi, and staff from the Historic Environment De-partment at the Abu Dhabi Tourism and Culture Authority, who participatedin fieldwork efforts. Our research in Abu Dhabi has been supported by theHistoric Environment Department of the Abu Dhabi Tourism and CultureAuthority (formerly Abu Dhabi Authority for Culture and Heritage); anInternational Research Fellowship Award (National Science FoundationGrant 0852975) (to F.B); the Revealing Hominid Origins Initiative (NationalScience Foundation Grant BCS-0321893); the Institute International de

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 CercopithecinesParapapio lothagamensis 10.5 8.0Papionin sp. indet., Ongoliba 9.5 6.5Macaca libyca 10.0 9.5As Sahabi papionin 11.0 8.5Macaca sp., Menacer 10.0 7.0Macaca sp., Almenara 11.5 8.0cf Macaca sp., Moncucco 12.0 8.0Macaca majori 9.5 6.0Macaca sylvanus ?prisca 12.0 —

Macaca sylvanus ?florentina 13.0 10.5Macaca palaeindica 13.0 —

Macaca sylvanus ?pliocena 14.0 7.5Macaca anderssoni 14.0–17.0 10.5Procynocephalus subhimalayanus 13.0 24.0Paradolichopithecus avernensis 31.0 19.0Paradolichopithecus sushkini 36.0 35.0

Extant small cercopithecinesCercopithecus cephus 3.8 2.7Macaca fascicularis 5.0 3.0Chlorocebus aethiops 5.1 3.6Cercopithecus ascanius 5.5 2.5Macaca mulatta 6.2 —

Cercopithecus neglectus 6.9 4.2Macaca nigra 7.5 4.7Cercopithecus mitis 8.0 3.9Macaca nemestrina 8.0–11.5 5.0–6.5Macaca sylvanus 15.0 10.0

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

Gilbert et al. PNAS | July 15, 2014 | vol. 111 | no. 28 | 10123

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Paléoprimatologie et Paléontologie humaine; the Agence Nationale de laRecherche (ANR-09-BLAN-0238); the Yale Peabody Museum; the Richard

Gilder Graduate School and the Gerstner Scholars Program; and a grant fromthe Yale University President’s Office (to A.H.).

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