Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage

Journal of Human Evolution xxx (2014) 1e15

Contents lists available at ScienceDirect

Journal of Human Evolution journal homepage: www.elsevier.com/locate/jhevol

Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage Stephen R. Frost a, *, Nina G. Jablonski b, Yohannes Haile-Selassie c a

Department of Anthropology, University of Oregon, Eugene, OR 97403-1218, USA Department of Anthropology, The Pennsylvania State University, University Park, PA 16802, USA c Physical Anthropology Department, The Cleveland Museum of Natural History, Cleveland, OH 44106, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 20 November 2013 Accepted 5 May 2014 Available online xxx

A large series of fossil cercopithecids has been recovered from the hominid-bearing Woranso-Mille site, Afar State, northeastern Ethiopia. Here we report the taxonomy of those specimens from the Am-Ado, Aralee Issie, Korsi Dora, Makah Mera, and Mesgid Dora collection areas, which are all roughly contemporaneous and dated to between 3.6 and 3.8 million years ago. This series includes a minimum of two cercopithecine and three colobine species. Theropithecus oswaldi cf. darti is by far the most common species in the assemblage, making up over 90% of identifiable cercopithecid specimens. There is also at least one other species of papionin, which cannot be currently assigned to a genus. The colobines are here allocated to Cercopithecoides cf. meaveae and two other species, one small and one large, that cannot be currently assigned to genus. The T. oswaldi cf. darti series from Woranso-Mille is both the earliest and largest identified to date. It documents the earliest occurrence of the T. oswaldi lineage and strongly suggests that parallel evolution of molar morphology has occurred within the genus between T. oswaldi and Theropithecus brumpti. Given the dominance of monkeys at Woranso-Mille, and the preponderance of Theropithecus among cercopithecids, T. o. cf. darti is likely to be the most common mammal present at the 3.6e3.8 million-years-old localities of the Woranso-Mille study area. Some explanations for this unusual occurrence are explored, and implications for the paleoenvironment at Woranso-Mille are also discussed. Ó 2014 Elsevier Ltd. All rights reserved.

Keywords: Eastern Africa Fossil Old World monkey Parallel evolution

Introduction The Woranso-Mille project is well known for a series of important Pliocene hominin fossils, including Australopithecus afarensis (Haile-Selassie et al., 2007, 2010a, b, 2012). In addition, a large associated fauna has also been collected in which cercopithecid monkeys are highly abundant (Haile-Selassie et al., 2007, 2010a). This paper focuses on the cercopithecids from several paleontological collection areas along the northern bank of the Mille River within the Woranso-Mille project area: Am-Ado (AMA), Aralee Issie (ARI), Mesgid Dora (MSD), and Makah Mera (MKM), as well as Korsi Dora (KSD), which is located further to the south (Fig. 1). These sites have been securely dated to between 3.57 (
0.014) and 3.76 (
0.02) million years ago (Ma) (Deino et al., 2010). The Am-Ado collection area is approximately the same site

* Corresponding author. E-mail addresses: [email protected] (S.R. (N.G. Jablonski), [email protected] (Y. Haile-Selassie).

Frost),

[email protected]

as the International Afar Research Expedition (IARE) locality A.L. 100. The IARE collected approximately 100 fossil cercopithecids from A.L. 100 during 1971e1973, which included three cercopithecoid species (Frost and Delson, 2002; Haile-Selassie et al., 2007). Frost and Delson (2002) identified these as Theropithecus cf. oswaldi darti, ?Parapapio cf. jonesi, and a large colobine, with the first being the most common. A total of 1347 cercopithecid specimens was collected by the Woranso-Mille project from the AMA, ARI, KSD, MSD, and MKM collection areas during the field seasons between 2006 and 2011. Specimens collected by the Woranso-Mille Project are catalogued beginning with the three letter prefix for the locality, a VP (vertebrate paleontology) designation and specific locality number followed by the individual specimen number (e.g., ARI-VP-1/26 for the twenty-sixth specimen from the first Aralee Issie locality). The vast majority of specimens that can be identified below the family level represent the Theropithecus oswaldi lineage. Non-Theropithecus papionins and a minimum of three colobine species, including at least one of Cercopithecoides, are also present, but rare. This paper is an initial description of this material, focusing on taxonomic

http://dx.doi.org/10.1016/j.jhevol.2014.05.003 0047-2484/Ó 2014 Elsevier Ltd. All rights reserved.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

2

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

Figure 1. Satellite imageries showing the locations of the Am-Ado (AMA), Aralee Issie (ARI), Mesgid Dora (MSD), Makah Mera (MKM), and Korsi Dora (KSD) fossil vertebrate collecting areas within the Woranso-Mille Project area.

allocation. Functional analysis of the postcranial material that can be clearly associated with Theropithecus is the subject of another study (Jablonski et al., in preparation). Systematic paleontology Family Cercopithecidae Gray, 1821 Subfamily Cercopithecinae Gray, 1821 Tribe Papionini Burnett, 1828. Genus Theropithecus I. Geoffroy, 1843. T. oswaldi (Andrews, 1916) T. o. darti (Broom and Jensen, 1946) Subspecific diagnosis See Frost and Delson, 2002. T. o. cf. darti (Broom and Jensen, 1946)

maxilla with P3eM1), MKM-VP-1/147 (l. maxilla with P3eM2), MKM-VP-1/153 (male edentulous mandibular symphysis), MKMVP-1/155 (male r. mandibular symphysis with CeP3), MKM-VP-1/ 160 (female mandible with l. M1e3, r. I1eP3), MKM-VP-1/182 female r. maxilla with P3eM1), MKM-VP-1/229 (female mandibular symphysis with l. I1eC and r. I1eP4), MKM-VP-1/257 (r. mandible with M2e3), MKM-VP-1/313 (r. maxilla with P3eM1 roots), MKMVP-1/357 (female r. mandible with P4), MKM-VP-1/367 (r. mandible with M1e3), MKM-VP-1/387 (r. maxilla with M1), MSDVP-2/104 (l. mandible with M1e3), MSD-VP- 2/214 (r. maxilla with P4eM3), MSD-VP-2/307 (male rostrum with l. and r. CeM3), MSDVP-2/318 (r. maxilla with C, P4eM2), MSD-VP-3/1 (male mandible with l. M1e3 and r. P4eM3), MSD-VP-5/15 (calvaria, probably male), MSD-VP-7/1 (r. maxilla with M12 fragments), MSD-VP-9/34 (juvenile l. mandible with M2) MSD-VP-9/38 (subadult female mandible with l. CeM2 and r. M2), MSD-VP-9/48 (juvenile r. mandible with M1, M2 erupting), plus 331 isolated teeth.

Specimens included

Description

AMA-VP-1/1 (female r. mandible with M3), ARI-VP-1/16 (r. mandible with M1e2), ARI-VP-1/26 (partial skeleton), ARI-VP-1/130 (male l. mandible with P3eM3), ARI-VP-1/194 (r. mandible with M2), ARI-VP-1/288 (female l. maxilla with CeM3), ARI-VP-2/2 (female l. mandible with M1e3), ARI-VP-2/5 (l. frontal), ARI-VP-2/10 (r. mandible with P4eM1, isolated l. M2), ARI-VP-2/15 (l. maxilla with P4eM1 and r. maxilla with P4eM2), ARI-VP-2/22 (l. mandible with M3), ARI-VP-3/12 (l. mandible with M2e3), ARI-VP-3/13 (r. mandible with P4eM2), ARI-VP-3/277 (l. mandible with M2e3), ARI-VP-3/294 (female r. mandible with M2 fragment), KSD-VP-1/14 (l. mandible with M1e2), KSD-VP-1/29 (female l. mandible with P4eM3), MKMVP-1/1 (cranium with l. and r. dp34), MKM-VP-1/79 (male mandible with l. I1e2, P3e4, M2e3 and r. I1eM3), MKM-VP-1/108 (female mandible with l. I1eM2 and r. I1e2, P3eM3), MKM-VP-1/ 118 (l. mandible with M2e3 and r. mandible with M1e3), MKM-VP1/131 (juvenile r. mandible with dP3e4), MKM-VP-1/144 (male r.

The Woranso-Mille Theropithecus material is similar to that from Hadar in its overall morphology and typical of known T. o. darti (Eck, 1993). However, some important differences can be observed. The Woranso-Mille material is slightly smaller in overall body size, molar tooth size, has less complex molar crown morphology, and less well developed cranial superstructures related to the muscles of mastication. It has been observed previously (Leakey, 1993; Frost and Delson, 2002) that the three widely accepted chronological subspecies of T. oswaldi (from oldest to youngest: T. o. darti, T. o. oswaldi and T. o. leakeyi) are differentiated from one another based on a series of relatively continuous morphological trends, including body size and molar crown complexity, from most primitive to most derived. The Woranso-Mille material seems to extend this trend further back in time, being more primitive than the specimens from Hadar. Given that the Theropithecus material from Hadar is well described and that the Woranso-Mille material is largely

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

similar, the following description will focus on the ways in which the Woranso-Mille material is distinctive. Calvaria The calvaria is well preserved in MSD-VP-5/15, which is most likely an adult male, and in MKM-VP-1/1, a juvenile partial cranium, which is slightly crushed with considerable surface damage (Fig. 2). In general, MSD-VP-5/15 is similar to male crania from Hadar such as A.L. 187-10, A.L. 205-1 and A.L. 412-1, being generally ovoid in superior view with considerable postorbital constriction and well-developed sagittal and nuchal crests (Eck, 1993; Frost, 2001b, Table 1). In the likely males ARI-VP-2/5 and ARI-VP-2/62, the temporal lines are prominent and in MSD-VP-5/ 15 converge approximately 2 cm anterior to bregma and the sagittal crest reaches its maximum height of approximately 3 mm

3

near lambda. The nuchal crests are damaged, but it can be seen that they would have been quite prominent and similar to those of A.L. 205-1. The superior surface of the root of the zygomatic process of the temporal is broad and flattened to accommodate extensive m. temporalis. The basicranium is extensively damaged. The glenoid fossa is flat compared with those of later subspecies of T. oswaldi (Jolly, 1972; Frost, 2001a, 2007a), and is only moderately convex in the parasagittal plane and only mildly concave in the coronal plane so that its medial border does not curve to face laterally. The tympanics have ventral crests, though they are not prominent, and angle slightly posterolaterally. They are also separated from the broken bases of the postglenoid processes by narrow sulci.

Figure 2. Cranial material of Theropithecus oswaldi cf. darti. A. MSD-VP-2/307 (crushed male rostrum) left and right lateral views; B. MKM-VP-1/1 (juvenile cranium with left and right dp3e4) left lateral, frontal, dorsal and ventral views; C. ARI-VP-1/288 (female left maxilla with CeM3) lateral and ventral views; D. MSD-VP-5/15 (calvaria, probably male) left lateral, frontal, dorsal and ventral views.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

4

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

Table 1 Calvarial, maxillary and mandibular dimensions (mm). Cat. no.

Sex

OP-BA

BA-BR

GL-IN

GL-BA

BR-IN

IN-OP

BI-POR

Post. Orb.

MSD-VP-5/15

M?

14

54

96

70

50

34

74

45

Cat. no.

Sex

ARI-VP-1/288 MKM-VP-1/87 MSD-VP-2/307 MSD-VP-7/1

F F M ?

Cat. no.

Sex

AMA-VP-1/1 ARI-VP-1/130 ARI-VP-2/2 KSD-VP-1/14 KSD-VP-1/24 KSD-VP-1/29 MKM-VP-1/79 MKM-VP-1/108 MKM-VP-1/118 MKM-VP-1/153 MKM-VP-1/160 MKM-VP-1/221 MKM-VP-1/229 MKM-VP-1/257 MKM-VP-1/357 MKM-VP-1/367 MSD-VP-2/104 MSD-VP-3/1 MSD-VP-9/38

F M F ? F F M F ? M F M F ? F ? ? M F

BI-M1/2

DM3-PMI

(45)

(59) 47 72

W.C.ALV

PMI-PRO

ZMS-M1/2

ZMS-ZMI

ZMI-DM3

40

29

20

37

29

11

W.M2/3

D.SYM 35 47

17

24

26 19

54 (32)

38

(24)

D.P4/M1

D.M2/3

Br.M2/3

32 34 28

31 32 23

16 20 15 16

27

25

12

16

12 14

25

14

27 29 33 31

16 13 15 15 17

24

47

26 21

33

25 29

30 21

47 43

42 26

33 23

Cranial measures are between landmarks, OP ¼ opistion, BA ¼ basion, BR ¼ bregma, GL ¼ glabella, IN ¼ inion, BI-POR ¼ biporionic breadth, Post. Orb. ¼ postorbital breadth following Freedman (1957). Maxillary measures are between landmarks, BI-M1/2 ¼ alveolar breadth from left M1/2 contact to right; DM3 ¼ alveolar margin at distal M3, PMI ¼ inferior premaxillo-maxillary suture, PRO ¼ prosthion, ZMS ¼ superior zygomatico-maxillary suture, ZMI ¼ inferior zygomatico-maxillary suture. Mandibular measures: W.C.ALV ¼ width from left to right alveolar margin at the canines, W. M2/3 ¼ width at the M2 e 3 contact, D.SYM is depth from between the lower I1s to the inferior margin in the midline, D.P4/M1 ¼ depth from alveolar margin to inferior margin at the P4 e M1 contact, D.M2/3 ¼ depth from alveolar margin to inferior margin at the M2 e 3 contact, Br. M2/3 ¼ corpus breadth at the M2 e 3 contact. Values in parentheses ( ) are estimates.

Face The face is best preserved in the juvenile cranium MKM-VP-1/ 1 and in ARI-VP-1/288 a left maxillary fragment of an adult female individual (Fig. 2; Table 1). MSD-VP-2/307 is a nearly complete rostrum of a male with left and right CeM3, but it is mediolaterally crushed (Fig. 2). The female maxilla ARI-VP-1/288 is similar in its preserved morphology to the female crania A.L. 321-12 and A.L. 185-5 from Hadar (Eck, 1993). The rostrum is short compared with other similarly-sized papionins. As far as can be determined, the rostrum would have been steeply sloping and convex from nasion to rhinion. Its dorsal surface is parabolic in paracoronal cross-section and completely lacks any evidence for maxillary ridges or fossae. The male MSD-VP-2/307 has relatively low maxillary ridges and shallow maxillary fossae, rather similar to those of A.L. 205-1 and MAK-VP-1/1 (Eck, 1993; Frost, 2001a). The zygomata originate superior to the middle of the M2 in ARI-VP-1/288 and the M2/3 contact in MSD-VP-2/307. Mandible There are several well-preserved corpora (Fig. 3; Table 1), especially MKM-VP-1/79 a nearly complete mandibular corpus of a male lacking only the rami and inferior margin posterior to the P4, MSD-VP-3/1 also a complete corpus of a male missing the anterior dentition, but preserving damaged P4eM3 on both sides, and MKM-VP-1/108 a nearly complete corpus of a female. There are several other mandibular fragments representing both sexes. Overall, they are similar to mandibles of T. o. darti from Hadar (Eck, 1993), the Middle Awash (Frost, 2001b), and Makapansgat (Freedman, 1957), although the Woranso-Mille material is generally smaller. In superior view, the dental arcade of females is relatively parabolic given the fairly small incisive portion of the alveolar process, whereas that of males is more straight-sided due to the larger canine teeth. The inferior transverse torus extends posteriorly to the level of the P4

in most specimens. The symphysis bears a median mental foramen and is marked by mental ridges in both sexes, although these are only modest, and may be slightly more prominent in males. They are clearly less marked than those of Theropithecus brumpti (Eck and Jablonski, 1987). Overall the symphysis is strongly sloping in lateral view, making an angle of approximately 45 relative to the occlusal plane below the median mental foramen, but is generally more vertical above. The incisor portion of the alveolar process is small compared with that of Papio. In lateral view, the corpora are approximately even in depth anterioposteriorly. Corpora are robust, with a maximum thickness of approximately 12e20 mm at the level of the M3 (Table 1). On the lateral surface, corpus fossae are slight to absent. Dentition The Woranso-Mille material is essentially similar to that of other populations of Theropithecus o. darti (Freedman, 1957; Eck, 1993; Frost, 2001a; Frost and Delson, 2002), except that it is generally more primitive. Specifically, this means the molar morphology typical of Theropithecus is variably developed in different individuals, and is on average less well developed than in the material from Hadar, the Middle Awash and Makapansgat. For example, the upper molars of ARI-VP-1/288 are comparatively low-crowned and lack the flattening of the lingual margin (Fig. 2). Others, such as ARI-VP-3/13 (r. mandible with P4eM3), ARI-VP-1/219 (l. M3) and ARI-VP-3/307 (r. M3) are morphologically and diagnostically Theropithecus. The molar teeth also are on average smaller than those of other populations of T. o. darti although there is considerable overlap (Fig. 4; Table 2). Furthermore, the incisors and canines are relatively large as, correspondingly, is the mesiobuccal extension of the P3.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

5

Figure 3. Mandibles of Theropithecus oswaldi cf. darti showing occlusal and lateral views. Females are on the left, males on the right. A. AMA-VP-1/1, B. KSD-VP-1/29, C. MKM-VP-1/ 84, D. ARI-VP-1/130, E. MKM-VP-1/79, F. MSD-VP-3/1.

Remarks We favor the taxonomy of Leakey (1993) for T. oswaldi (recognizing three chrono-subspecies: T. o. darti, T. o. oswaldi, and T. o. leakeyi) because it emphasizes that the specimens so grouped are members of a single, phyletically evolving lineage that shows a clear increase in dental and body size through time as well as along several morphological trends related to terrestrial grazing (Jolly, 1972; Eck, 1987; Delson, 1993; Jablonski, 1993; Leakey, 1993; Frost and Delson, 2002; Frost, 2007a; Gilbert, 2013). In addition to Woranso-Mille, Theropithecus o. darti (including T. o. cf. darti) has

been described from Makapansgat, Hadar, the Middle Awash (Maka and its chronological equivalents), Kanam, Koobi Fora (Lokochot Member), and possibly the Shungura Formation (Member C) (Freedman, 1957; Eck, 1987, 1993; Delson, 1993; Frost, 2001b; Frost and Delson, 2002; Jablonski et al., 2008a). Morphologically, the Woranso-Mille Theropithecus material is similar to that from Hadar (Eck, 1993; Frost and Delson, 2002), except for features that have been previously noted to show progressive evolution over the course of the lineage, for which the Woranso-Mille specimens are even more primitive. In particular, general cranial and dental dimensions are slightly smaller than, but also greatly overlap those

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

6

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

Figure 4. Box and whiskers plot comparing molar size of Theropithecus samples from Woranso-Mille (white boxes) to Hadar (gray boxes). The central bar of each box represents the median, or 50th percentile. The bottom and top of each box represent the 25th and 75th percentiles, respectively. The whiskers extend to the furthest observation that is less than 1.5 the length of the box. Any individuals outside of the whisker range are marked separately. Molar size is represented as crown area, calculated as length x (anterior width þ posterior width/2). Hadar data are taken from Frost, 2001b and includes only specimens from the Hadar Formation.

from Hadar (Table 2; Fig. 4). Furthermore, the enamel complexity of the molar teeth is even less well developed as that from Hadar, such that some individuals appear similar to non-Theropithecus papionins in this regard. The cranial morphology, however, aligns the Woranso-Mille series with T. o. darti, for example the relatively short deep rostrum with reduced or absent maxillary ridges and Table 2 Summary of dental dimensions (mm) for Theropithecus oswaldi cf. darti.. Tooth

N

I1 C1(F) C1(M) P3 P4 M1 M2 M3 Mx dP3 dP4 I1 I2 C1(F) C1(M) P3(F) P3(M) P4 M1 M2 M3 Mx dp3 dp4

2 2 1 5 9 8 6 10 84 1 2 5 5 6 5 10 6 26 24 26 72 64 3 4

Widtha Mean 6.8 6.8 e 8.2 8.5 9.4 10.9 11.2 10.8 5.6 7.4 5.9 5.3 6.9 11.5 4.8 6.0 6.8 7.9 9.9 10.3 9.1 4.4 6.4

Min.

Other measuresb Max.

6.3 e 7.0 8.0 9.2 9.9 9.9 8.9

7.3 e 8.8 9.1 9.6 11.7 12.4 12.9

7.0 5.3 4.9 5.8 10.7 4.3 5.4 6.2 6.9 8.9 8.6 7.1 4.1 6.1

7.8 7.1 5.7 7.7 12.6 5.9 6.3 7.6 9.5 10.8 12.3 11.5 4.6 6.6

Mean 13.1 12.6 31.9 e e 8.8 10.8 9.1 9.4 6.1 7.1 6.0 6.2 10.8 21.2 9.9 16.0 e 8.2 9.4 9.2 8.8 5.3 6.4

Min.

Max.

10.8

14.4

e e 8.6 10.0 8.1 7.2

e e 9.0 11.6 10.1 11.3

6.8 2.9 4.5 9.7 20.3 6.0 12.9 e 7.2 8.1 7.8 7.0 5.2 6.2

7.3 7.7 7.9 13.1 22.2 11.9 17.2 e 9.4 10.8 11.2 10.7 5.5 6.6

Lengthc Mean

Min.

Max.

7.1 8.0 14.5 6.8 7.1 9.9 12.3 12.8 12.1 7.8 8.7 5.2 5.2 4.3 6.6 7.3 10.4 7.8 9.5 11.8 15.8 11.9 8.4 9.5

6.1 7.7

8.1

5.3 6.2 8.3 11.6 11.4 10.1

7.9 8.0 10.7 12.8 14.5 14.2

8.6 5.1

8.8 5.2

3.9 6.2 6.8 8.9 6.4 7.6 8.8 14.0 9.4 8.2 9.2

4.7 6.8 8.0 11.3 8.7 11.1 13.7 18.2 15.1 8.9 9.8

For each dimension, mean, min. and max. are given (mm). a All widths are buccolingual and in the case of molars it is measured across the mesial moiety. b Other measures include: crown height for the incisors and canines; for lower third premolars flange height is taken from the protoconid to the inferior tip of the mesiobuccal honing flange; for the molars distal width across the distal moiety is presented. c All lengths are mesiodistal. Dental dimensions for individual specimens are given in the Supplementary Online Material (SOM) Table S1.

fossae, zygomata that are anteriorly positioned for a papionin of this size, superior-inferiorly tall and anteriorly sloping, strongly developed temporal lines that form a sagittal crest at or anterior to bregma, large degree of postorbital constriction, thick mandibular corpus generally with shallow or absent corpus fossae, and a steep sloping symphysis with constricted area for the incisor alveoli (Freedman, 1957; Eck, 1993; Frost, 2001b; Frost and Delson, 2002). Among T. o. darti populations, the Woranso-Mille material is most similar to that from Hadar (Eck, 1993; Frost, 2001b) and the Middle Awash (Frost, 2001b), especially when compared with that from Makapansgat (Freedman, 1957). Frost and Delson (2002) described several features that distinguish the population from Hadar from the population at Makapansgat, including a less projecting glabellar region, less concave rostral profile, less welldeveloped maxillary ridges and shallower mandibular corpus fossae. In all of these features, the Woranso-Mille series is more similar to that from Hadar and therefore similarly allocated to T. o. cf. darti. The Woranso-Mille T. o. cf. darti population is significant on several grounds. At 3.6e3.7 Ma, it is among the oldest known populations of the genus, and by allocating it to T. o. cf. darti it is the oldest population that can be definitively assigned to either of the well-known lineages T. brumpti or T. oswaldi. The Theropithecus specimens that exceed the Woranso-Mille sample in geological age are a mandible (WEE-VP-1/1) from 3.9 Ma deposits in the nearby Middle Awash (Frost, 2001b), some isolated dental specimens from the Lonyumun Member of the Koobi Fora Formation, East Turkana, Kenya (Jablonski et al., 2008a), and one molar (KNM-KP 32879) tentatively assigned to the genus from Kanapoi, Kenya (Harris et al., 2003). None of these can be clearly allocated to either the T. brumpti or T. oswaldi lineage. It is also one of the largest known series of T. oswaldi darti from a restricted time-horizon, with over 350 identified specimens. This number probably underestimates the preponderance of T. o. darti at Woranso-Mille because there are at least 88 additional specimens that likely belong to the same subspecies, but given their very primitive morphology cannot be identified beyond all doubt as either T. o. darti or as a Papionini gen. et. sp. indet. However, with the observed overall variation, the Woranso-Mille Theropithecus lies approximately where expected given the wellestablished trends observable in the lineage (Leakey, 1993; Frost and Delson, 2002). An additional concern, given the primitive morphology, is that some of the material identified here is in fact from a second, larger papionin. While this possibility cannot be excluded completely, there is currently no evidence for material similar in size with T. o. darti, that is incompatible with it in morphology, such that the best interpretation is that all of this material is Theropithecus until any evidence to the contrary can be found. All of these points mean that the Woranso-Mille Theropithecus population provides the unique opportunity to understand the origins and evolution of this important lineage. First, it suggests that the highly derived condition of the molar teeth present in both T. brumpti and geologically younger populations of T. oswaldi evolved at least partly in parallel. This is because the Woranso-Mille material is only very slightly derived towards Theropithecus in its molar morphology, but is already part of the T. oswaldi lineage based on its cranial and mandibular morphology. Given that there is evidence of the T. brumpti lineage that already shows highly derived molars by at least 3.4 Ma, and possibly as early as 3.6 Ma in the Turkana Basin, parallel evolution of the molar morphology is the simplest explanation (Jablonski et al., 2008a). Whether this is true of Theropithecus gelada as well is difficult to determine given its lack of a fossil record (Jablonski and Frost, 2010). Alternatively, it is conceivable that the facial morphology of the T. oswaldi lineage is

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

primitive for the genus and that the Woranso-Mille population is actually a stem form ancestral to both T. brumpti and T. oswaldi. This alternative would require the Woranso-Mille population to be a relict that has survived to be nearly contemporary with the more dentally advanced T. brumpti, but that there were also populations of T. oswaldi that are more dentally derived than the Woranso-Mille series. This alternative would also necessitate the very rapid evolution of the extremely autapomorphic T. brumpti cranial morphology. This latter alternative, at present, appears less likely. The sample of T. o. cf. darti from Woranso-Mille is the most primitive known because it lacks morphological specializations that differentiate early from later populations of T. oswaldi. Papionini gen. et sp. indet. Specimens included ARI-VP-1/241 (r. dP4), ARI-VP-1/324 (l. Mx), ARI-VP-1/530 (r. M1or2), ARI-VP-1/613 (l. M3), ARI-VP-3/17 (r. M1or2), ARI-VP-3/97 (l. M1or2), ARI-VP-3/138 (l. M3), ARI-VP-3/210 (l. Mx), ARI-VP-3/244 (l. M3), ARI-VP-3/256 (l. M1or2), ARI-VP-3/338 (l. M3), ARI-VP-3/379 (l. M3), ARI-VP-3/395 (r. dP4), KSD-VP-1/10 (r. M3), MKM-VP-1/75 (r. Mx), MKM-VP-1/286 (r. M1or2), MKM-VP-1/321 (l. Mx), MKM-VP-1/ 322 (r. Mx), MSD-VP-1/93 (female mandible with r. M2-3, l. M1; R. premaxilla with I2), MSD-VP-2/154 (r. M1or2), MSD-VP-2/175 (r. M1or2), MSD-VP-9/11 (r. Mx).

7

Description Papionins other than Theropithecus are represented by a fragmentary mandible and a collection of 23 isolated teeth (Fig. 5). This sample could potentially be incorporated into a single, highly sexually dimorphic taxon, or it may include multiple species. The teeth range in size from specimens consistent with Pliopapio alemui (e.g., ARI-VP-1/530, ARI-VP-1/324, MKMVP-1/321, MKM-VP-1/322) to others more similar to Parapapio cf. jonesi from Hadar (e.g., KSD-VP-1/10, ARI-VP-3/17) (Frost, 2001a; Frost and Delson, 2002). Measurements are given in Table 3. The hypothesis that multiple species are present in this series is also favored by the morphological variability in the sample. Some individual molar teeth are relatively long and narrow, with a low level of crown flare (e.g., ARI-VP-3/17, ARI-VP3/256, MSD-VP-2/154, MSD-VP-2/175, ARI-VP-1/530) and others are more low crowned, broad, and flaring (e.g., MKM-VP-1/321, 322, ARI-VP-3/210). Remarks Given the primitive nature and range of molar morphology observed in the T. oswaldi cf. darti series from Woranso-Mille, some discussion is warranted of how Papionini gen. et sp. indet. is distinguished from T. o. cf. darti at Woranso-Mille. This is based on a combination of morphology and size. Firstly, none of this material

Figure 5. Papionini gen et sp. indet. Right side, A. MSD-VP-1/93 (right mandibular corpus with M2e3) buccal (top), superior (middle), lingual (bottom). B. Upper molars, from left to right, MKM-VP-1/321; MKM-VP-1/322; MSD-VP-9/11 buccal (above) and occlusal (below) views. C. Lower molars, from left to right ARI-VP-1/530, MSD-VP-2/154, ARI-VP-3/256, ARI-VP-3/17 occlusal (above) and lingual (below) views. D. M3s from left to right ARI-VP-1/613; ARI-VP-3/244; ARI-VP-3/138 occlusal (above) and lingual (below) views.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

8

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

Table 3 Dental dimensions for Papionini gen. et sp. indet (mm). Cat. No.

Tooth

WS

Width

ARI-VP-1/241 ARI-VP-1/324 ARI-VP-1/530 ARI-VP-1/613 ARI-VP-3/17 ARI-VP-3/97 ARI-VP-3/138 ARI-VP-3/210 ARI-VP-3/244 ARI-VP-3/256 ARI-VP-3/338 ARI-VP-3/379 ARI-VP-3/395 KSD-VP-1/10 MKM-VP-1/75 MKM-VP-1/286 MKM-VP-1/321 MKM-VP-1/322 MSD-VP-1/93b MSD-VP-1/93a MSD-VP-1/93a MSD-VP-2/154 MSD-VP-2/175 MSD-VP-9/11

dP4 Mx Mx M3 Mx Mx M3 Mx M3 Mx M3 M3 dP4 M3 Mx Mx Mx Mx M1 M2 M3 Mx Mx Mx

12 4 3 5 5 2 1 7 9 2

5.3 7.8 6.2 8.3 8.2 5.6 7.6 8.5 8.1 7.0 (8.8) 8.0 6.1 9.4 8.0 7.1 8.0 8.4

5.5 7.2 6.3 7.6 7.9 6.3 7.8 7.9 7.9 7.1 6.8 6.8 5.6 8.3

6.6 7.3 8.0

6.7 6.9 7.8

2 10 9 8 7 6 6

3 1 4

Other

7.2 7.1 7.0

Length 7.5 9.0 8.7 14.0 10.8 8.7 13.1 9.7 13.3 10.0 8.8 8.4 14.2 8.7 10.2 8.6 9.1 (8.5þ) 10.6 (14.5þ) 9.6 10.0 9.7

Dimensions same as for Table 2. WS, dental wear stage (after Delson, 1973). Values in parentheses are estimates.

has any hint of the derived Theropithecus morphology observable in some of the T. o. cf. darti sample. These specimens are also all either outside or at the lowest extreme of the T. o. cf. darti size range, which is represented by sizeable samples at all tooth positions (Tables 2 and 3). Furthermore, those Papionini gen. et sp. indet. specimens that do overlap the bottom of the T. o. cf. darti range all have particularly low and flaring crowns, whereas even the most primitive T. o. cf. darti specimens have taller cusps and less crown flare. Even so, it was not always possible to distinguish these two morphs, and 88 specimens had to be left unassigned to either taxon. Subfamily Colobinae Jerdon, 1867. Genus Cercopithecoides Mollett, 1945. Cercopithecoides meaveae Frost and Delson, 2002. Cercopithecoides sp. cf. C. meaveae Specimens included ARI-VP-1/261 (l. M1or2), ARI-VP-1/404 (l. M1or2), ARI-VP-1/507 (l. Mx), ARI-VP-1/659 (r. M3), ARI-VP-3/85 (r. M3), ARI-VP-3/437 (r. Mx), ARI-VP-3/438 (r. Mx), ARI-VP-3/472 (r. M1or2), MKM-VP-1/87 (female skull fragments), MKM-VP-1/308 (r. maxilla with dP3-M1, M2 erupting), MKM-VP-1/396 (l. Mx), MKM-VP-1/433 (r. mandible with M1-3), MSD-VP-1/115 (r. Mx), MSD-VP-5/31 (l. M3). Description MKM-VP-1/87 preserves the supraorbital region including the interorbital pillar and most of the superior orbital rims except for the central 1.5 cm on the right and 0.5 cm around the supraorbital notch on the left; it also includes some of the squamous portion around the temporal lines. A separate fragment makes up most of the palate except for the area around the posterior part of the incisive foramen, along with approximately 1.5 cm of maxillary bone superior to the alveolar process (Fig. 6; Table 4). On the right side, only M2 is present as are the roots of I12, P3eM1 and on the left M23 are present along with the roots of I1, CeM1. Five mandibular fragments are present including the alveolar process of

the right corpus with M1e3 and just the anterior portion of the ramus, a fragment of the left corpus with M1e2, another fragment of the left corpus with the posterior rim of the canine alveolus plus roots for P3e4, a symphysis fragment with the roots of the incisors, right canine and anterior root of the right P3. Finally there is the posterior margin of the right ramus extending from the condylar process inferiorly to close to the gonial area. MKM-VP-1/308 is a right maxillary fragment with dP3eM1 and the crown of M2 just beginning to erupt. It preserves the base of the palatal process, approximately 1 cm of the lower part of the rostrum and the root of the zygomatic process. MKM-VP-1/433 is a right mandibular corpus fragment with broken crowns of M1e3, which in their preserved parts show heavy wear indicating an older individual. The crown of M3 is also cracked along its lingual and mesial margins distorting its size and shape moderately. The corpus is preserved from directly under the teeth to the inferior margin, although there is some cracking and distortion to its original shape. ARI-VP-3/182 is a left maxillary fragment preserving M12 and the maxillary bone immediately superior to it for about 1.5 cm. In overall craniodental size, Cercopithecoides cf. meaveae from Woranso-Mille is close to, but slightly larger than, the type series of Cercopithecoides meaveae from Leadu and Hadar, smaller than Cercopithecoides williamsi and Cercopithecoides kimeui, and larger than Cercopithecoides kerioensis and Cercopithecoides alemayehui (Freedman, 1957, 1961; Leakey, 1982; Frost and Delson, 2002; Frost et al., 2003; Leakey et al., 2003; Gilbert and Frost, 2008; Jablonski et al., 2008b, Table 4). Frontal The only frontal preserved is that of MKM-VP-1/87. The supraorbital rim is separated from the neurocranium by a wide and shallow ophryonic groove. The glabellar region is less projecting than that of Rhinocolobus, but more than that of Paracolobus chemeroni, and generally similar to that of Cercopitheocides. In superoinferior thickness the supraorbital rim is thinner than that of the male C. meaveae holotype A.L. 2-34, but that may be because MKM-VP-1/87 is from a female individual. The difference is certainly consistent with a single species, given that brow thickness has been seen to have a large range within C. williamsi (Anderson et al., 2013). The interorbital region is relatively broad, similar to most known colobines, but different from Dolichopithecus, Rhinocolobus, Libypithecus, and Nasalis (Szalay and Delson, 1979; Frost, 2001b). The interorbital breadth of the female specimen MKM-VP-1/87 (ca. 14.5 mm) is slightly larger than that of male C. meaveae holotype A.L. 2-34 (13.8 mm). In superior view, the temporal lines of MKM-VP-1/87 are pronounced, but are relatively widely spaced and oriented posteriorly such that it is unlikely they would have formed a sagittal crest. Rostrum As preserved by MKM-VP-1/87, the rostrum is moderately short and generally similar in outline to that of Cercopithecoides and Kuseracolobus. The exact position of the zygomatic process of the maxilla is difficult to determine given damage to the specimen, but is either above the M2 or at the M1/M2 contact. The inferior margin of the zygomatic process is only slightly elevated above the alveolar process, which is similar to its position in C. meaveae, but lower than in most C. williamsi (Freedman, 1957, 1961, 1965; Leakey, 1982; Jablonski et al., 2008b). In inferior view, the palate is relatively broad, shallow and parabolic in outline. As is typical for female colobines, the canines and incisors form a continuous anterior arc. Anteriorly, the inferiormost portion of the piriform aperture is preserved on MKM-VP-1/87. As far as can be determined, it was relatively narrow and had a ‘V’-shaped inferior border. The roots of the upper incisors would have diverged around it. In profile it would have been relatively vertically oriented, with its inferior-most limit making an angle of approximately 45 with the occlusal plane.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

9

Figure 6. Specimens of Cercopithecoides cf. meaveae. Above, MKM-VP-1/87 male skull fragments including: A. Maxilla, B. Frontal, C. Left corpus with M1e2, and D. Right corpus with M1e3. E. MKM-VP-1/308b (juvenile right maxilla with dp34, M12), and F. MKM-VP-1/433 (left mandible M1e3).

Table 4 Dental dimensions for Cercopithecoides cf. meaveae (mm). Cat. No.

Tooth

ARI-VP-1/261 ARI-VP-1/404 ARI-VP-1/507 ARI-VP-1/659 ARI-VP-3/85 ARI-VP-3/437 ARI-VP-3/438 ARI-VP-3/472 MKM-VP-1/87 MKM-VP-1/87 MKM-VP-1/87 MKM-VP-1/87 MKM-VP-1/87 MKM-VP-1/87 MKM-VP-1/308b MKM-VP-1/308b MKM-VP-1/308b MKM-VP-1/396 MKM-VP-1/433 MKM-VP-1/433 MKM-VP-1/433 MSD-VP-1/115 MSD-VP-5/31

Mx Mx Mx M3 M3 Mx Mx Mx C1 M2 M3 M1 M2 M3 dP3 dP4 M1 Mx M1 M2 M3 Mx M3

Dimensions same as for Table 3.

WS

Width

Other

Length

7

6.8

6.9

0 5 12 0 0 2

8.6 7.4

8.0 7.3 7.3 7.7 7.6 7.3

8.8 8.9 9.4 11.9 12.3 8.6 9.0 9.5 6.7 8.9 9.4 8.2 9.1 12.9 (5.4) 6.6 7.8 9.0 (6.4) 8.3 (10.3) 8.1 8.9

9 7 10 10 7 12 4 8 16 16 16 16 1

8.1 8.2 6.8 6.3 8.8 8.4 6.5 7.7 7.6

8.1 7.9 6.6 7.9 7.5

5.8 6.7 7.9

5.6 6.5 7.3

7.6

7.4

8.7 8.2

7.7 6.6

Mandible In overall morphology, the mandible is typical of Cercopithecoides in general, and to that of C. meaveae in particular. MKM-VP-1/87 preserves portions of the alveolar part of both sides of the corpus, but lacks the inferior margin, and MKM-VP-1/433 preserves much of the right side, complete to the inferior margin, posterior to M1. Overall, the corpus is shallow, broad, and relatively robust. The corpus of MKM-VP-1/433 measures approximately 25 mm in depth, but this may be mildly exaggerated due to cracking and infilling by matrix. Regardless, this is somewhat deeper than either A.L. 2e34 or A.L. 231-1. It also appears to have been deepest underneath the M2 and slightly shallower under the M3. The corpus is relatively wide overall and widest at mid-height as is typical of Cercopithecoides. The corpus of MKM-VP-1/433 has a breadth of 13 mm at the level of the M3, and while that of MKM-VP-1/87 cannot be measured, it would have been similar. In superior view, there is a broad buccinator groove lateral to M2e3. A fragment of the posterior portion of the right ramus with most of the posterior margin, condylar process, posterior portion of the triangular fossa, and superior part of the gonial region is associated with MKM-VP-1/87. While fragmentary, it appears that the ramus was relatively low, which would be similar to other specimens of Cercopithecoides, but distinct from Paracolobus, Rhinocolobus, and Kuseracolobus (Freedman, 1957; Leakey, 1969, 1982; Frost, 2001a; Jablonski et al., 2008b).

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

10

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

Dentition The dentition is essentially morphologically similar to that of C. meaveae from Leadu and Hadar except that it is slightly larger. Incisors are not represented, and the canines are typical of Old World monkeys. The molars are typical of colobines with widely spaced cusps, a low amount of crown flare, and well developed cross-loph(id)s. The upper molars are relatively quadrate in occlusal outline, and relatively broad. As is typical of colobines, the M2s have a distal lophid that is either broader than or subequal to the mesial lophid in width. The M3s have distal lophids that are either equal or slightly narrower than the mesial lophid. Remarks Previously, Cercopithecoides meaveae was only known from Leadu and Hadar, younger sites from the Afar Depression (Frost and Delson, 2002). The morphology of the Woranso-Mille material described here is very similar to that of the type sample, but is slightly larger. For example, the partial female cranium MKM-VP-1/ 87 is slightly larger in nearly all dental dimensions than the male C. meaveae holotype A.L. 2-34, but is still significantly smaller than known samples of C. williamsi (Freedman, 1957, 1961, 1965; Maier, 1970; Jablonski et al., 2008b). At this stage, taxonomic distinction is not warranted for the Woranso-Mille material, but given its larger size than the type series, though still smaller than C. williamsi, it is designated C. cf. meaveae. While C. meaveae is currently only known from Hadar, Leadu, and tentatively Woranso-Mille, there are other localities where colobines similar in size, but of unclear affinity, have been found. These include Cercopithecoides sp. from Laetoli (Harrison, 2011), several isolated teeth from the Usno and Shungura Formations (Leakey, 1987), a mandible assigned to cf. Cercopithecoides sp. from Kanapoi (Harris et al., 2003), a few jaw fragments from Koobi Fora (Delson, 1984; Frost, 2001b; Jablonski et al., 2008b) and some isolated molars from the Middle Awash (Frost, 2001b). The Cercopithecoides from Laetoli differs from C. meaveae in some morphological features including a less robust mandibular corpus and various dental proportions (Harrison, 2011). The mandible from Kanapoi is considerably deeper than that of known specimens of C. meaveae, suggesting that it represents a different species and possibly different genus (Harris et al., 2003). The other material is too fragmentary to determine whether it represents C. meaveae or not. Colobinae gen. et sp. indet. A.

Table 5 Dental dimensions for Colobinae gen. et sp. indet. A (mm). Cat. No.

Tooth

ARI-VP-3/194 ARI-VP-1/416

P3 P4

WS

Width

2 1

5.6 3.9

Other

Length 5.2 5.8

Dimensions same as for Table 3.

depth to extant Colobus, but smaller than known extinct colobines. In profile, the symphysis is close to vertical anteriorly for approximately 1 cm, then curves posteriorly. It appears to have lacked a median mental foramen, but this cannot be determined with certainty due to damage in the midline region. There are very faint mental ridges (not really mental ridges, just swellings) that appear to grade into a fairly broad and robust corpus that would have had its thickest point inferiorly, unlike C. meaveae where its thickest point is at mid-height. This leads to the presence of very shallow corpus fossae under the premolars, as is common among colobines with robust corpora. The mental foramen is only observable on the right side, where it is positioned near to the inferior rim underneath the posterior part of P3. In superior view, the incisors are arranged in a small arc just anterior to the canines, as opposed to being directly between them, and the tooth rows diverge slightly posterior to this. The superior transverse torus has a steeply sloping superior surface, and extends posteriorly to the level of the distal P3. There is a deep genial fossa separating the superior transverse torus from the inferior transverse torus, which extends posteriorly to the level of the distal P4. Dentition In occlusal view, the P3 is essentially round except for a narrow mesial extension anterior to the paracone. The paracone is tall and sharp, but the protocone is completely lacking. Instead, there is a well-developed lingual cingulum, similar to extant African colobines (Strasser and Delson, 1987). There is a distinct and sharp crest that extends lingually from the paracone in the direction of where the protocone would have been. Mesiobuccally it can be seen that there was a well-developed extension on the root, but this is broken immediately below the cervix. The P4 has a prominent protoconid, but a fairly strongly reduced metaconid. The protoconid is tall and rises sharply above the talonid, which is relatively low. The talonid consists of a low cingulum that rises slightly posteriorly, but includes no distinct cusps.

Specimens included

Remarks

ARI-VP-1/416 (l. P4), ARI-VP-3/194 (r. P3), KSD-VP-1/24 (mandible fragment with roots of l. I1eM1, and r. I1eP4)

In size this material is consistent with extant Colobus and Procolobus. In morphology it is also consistent with those genera along

Description KSD-VP-1/24 consists of the left and right corpora back to the M1 on the left and P4 on the right, preserving the inferior margin for the left side, but not the right. It is also broken in the midline. ARIVP-3/194 is a right P3 preserving the entire crown and lingual root, but missing the distal portions of the buccal roots. ARI-VP-1/416 is a left P4 preserving most of the crown but lacking the roots. The three specimens included here are considerably smaller than all of the other colobine material from Woranso-Mille. In overall size they are consistent with extant Colobus and are smaller than material assigned to Cercopithecoides cf. meaveae or Colobinae gen. et sp. indet. B. (Table 5). Mandible The symphysis of KSD-VP-1/24 is relatively shallow and vertical, with an approximate depth of 24 mm. This is similar in

Table 6 Dental dimensions for Colobinae gen. et sp. indet. B (mm). Cat. No.

Tooth

WS

Width

Other

Length

ARI-VP-1/436 ARI-VP-3/167 ARI-VP-3/390 ARI-VP-3/434 ARI-VP-3/434 MKM-VP-1/99 MKM-VP-1/99 MKM-VP-1/99 MKM-VP-1/221 MKM-VP-1/221 MKM-VP-1/221 MKM-VP-1/221

Mx Mx M3 P3 P4 P4 M1 M2 I1 I2 C1 P3

9 10 9 3 4 4 10 7

7.2 8.5 10.1 7.8 8.1 8.5 8.5 9.6 5.3 5.8 10.7 6.2

7.6 8.3 8.9

9.5 9.8 11.0 7.1 6.9 7.2 9.1 10.0 4.1 4.3 6.5 9.1

9.0 6.5 8.0 14.0

Dimensions same as for Table 3.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

with known extinct genera with robust mandibles, such as Cercopithecoides. Given its fragmentary nature, it is not allocated to genus here, but if it were to represent one of the extant genera it would be the earliest occurrence, but well within the time range predicted for these genera by molecular analysis (Ting, 2008). Colobinae gen. et sp. indet. B. Specimens included ARI-VP-1/436 (r. M1or2, ARI-VP-3/167 (r. maxilla with M), ARIVP-3/390 (l. M3), ARI-VP-3/434 (r. maxilla with P34), MKM-VP-1/ 99 (female l. maxilla with P4eM2 and roots of P3, M3), MKM-VP1/221 (male mandible with l. I1e2, r. I1, P3), MKM-VP-1/297 (male r. maxilla edentulous). Description In overall size this taxon is larger than the material assigned to Cercopithecoides cf. meaveae (Table 6). It is similar in size to Cercopithecoides williamsi (Freedman, 1957, 1965; Maier, 1970; Leakey, 1982; Jablonski et al., 2008b) and the larger colobine material from Laetoli assigned to cf. Paracolobus sp. by Leakey and Delson (1987) and to cf. Rhinocolobus sp. by Harrison (2011). It is generally smaller than Paracolobus chemeroni, P. mutiwa or Cercopithecoides kimeui (Leakey, 1969, 1982; Frost et al., 2003).

11

Maxilla The rostrum is more projecting than that of C. cf. meaveae. The lateral surface of the rostrum is also more rounded in crosssection. The lateral surface of the rostrum lacks any evidence for facial fossae. The rim of the piriform aperture is inclined at approximately 30 relative to the alveolar margin, so that its opening would have faced superiorly. The inferior margin of the base of the zygomatic process is positioned above the M1/M2 contact. The root of the zygomatic process is positioned relatively low on the maxilla, which is similar to Kuseracolobus and Cercopithecoides meaveae, but unlike Cercopithecoides williamsi, C. kimeui, Rhinocolobus, and Paracolobus (Freedman, 1957; Leakey, 1982; Frost, 2001a; Hlusko, 2006; Jablonski et al., 2008b). The palate of both MKM-VP-1/297 and MKM-VP-1/99 is shallow and broad (Fig. 7). Based on the broken superior surface of MKM-VP1/297 and ARI-VP-3/167 a maxillary sinus appears to be present, a feature documented in Cercopithecoides, Libypithecus, Kuseracolobus, and the larger colobine from Laetoli, but generally lacking in other colobines (Rae, 2008; Harrison, 2011; Personal observation). Inferiorly, the palatal process is very shallow on both MKM-VP-1/99 and MKM-VP-1/297, especially given the overall size of the specimens. Mandible The mandible is only preserved in the male symphysis MKM-VP-1/221, which is similar in size and morphology to the symphysis of A.L. 256-1 and A.L. 248-5 from Hadar, both assigned to cf. Rhinocolobus turkanaensis (Frost and Delson, 2002). It is

Figure 7. Colobinae gen. et sp. indet. B. A. MKM-VP-1/297 (male right edentulous maxilla), lateral (above) and inferior (below) views. B. MKM-VP-1/99 (left female maxilla P4-M2), lateral (above) and inferior (below) views. C. MKM-VP-1/221 (male symphysis with left I1eC, right I1, P3), lateral (left), dorsal (center), and anterior (right) views.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

12

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

slightly smaller than, but similar in morphology to the male ASI-VP2/200 from Asa Issie assigned to Kuseracolobus hafu (Hlusko, 2006). The anterior surface of the symphysis is steeply inclined, sloping at an angle of approximately 65 to the alveolar margin. The exact depth of the symphysis cannot be gauged as the inferior margin is broken. There is no median mental foramen present, but it is not certain whether one may have existed in the area below the break. Even though the exact depth of the corpus cannot be determined, it is clear that the corpus would have been significantly deeper than that of ARI-VP-1/433 assigned here to Cercopithecoides cf. meaveae. The incisors are fairly large compared with other colobines and vertically implanted. The planum alveolare is steeply sloping and the superior transverse torus extends posterior to the level of the P3. Dentition The dentition is generally similar to that of other colobines. The lower incisors and premolars are only represented by MKM-VP-1/221. The lower incisors are typical in their morphology, but are relatively large compared with the posterior dentition. The male P3 has a well-developed paraconid and the mesiobuccal extension is only moderate in length. The talonid is only moderately broad. The upper premolars are large. The protocone of the P3 is strongly reduced, on ARI-VP-3/434 the only specimen where it is preserved. This morphology is typical of extant colobines, Cercopithecoides and Rhinocolobus, but also occurs variably in others (Szalay and Delson, 1979; Frost and Delson, 2002). The molars have tall, widely spaced cusps, well-developed cross lophs(id)s and low lingual/buccal notches, which is similar to most colobines, but distinct from Cercopithecoides kimeui. Remarks While this material is too fragmentary to make a positive assignment to a genus, it is possible to rule out some taxonomic designations. The rostrum is too short and the zygomatic process is positioned too far anteriorly and inferiorly for this material to be assigned to Libypithecus, Paracolobus, or Rhinocolobus (Szalay and Delson, 1979; Leakey, 1982). The presence of a clear maxillary sinus in the Woranso-Mille material is also inconsistent with the latter two genera (Rae, 2008), but would be consistent with the larger colobine at Laetoli (Harrison, 2011). The Woranso-Mille large colobine would be most consistent overall with either Kuseracolobus or Cercopithecoides, though it is not a perfect match for any of the known species of either genus. It is most similar in size to Cercopithecoides williamsi (Freedman, 1957), but the zygomatic is positioned somewhat lower on the rostrum in MKM-VP-1/99 and MKM-VP-1/297 and it is smaller than Kuseracolobus hafu from Asa Issie (Hlusko, 2006) and larger than K. aramisi from the Middle Awash and Gona (Frost, 2001a; Semaw et al., 2005; Frost et al., 2009). Discussion In the Afar Depression, there is significant difference in cercopithecid faunas between Early Pliocene localities such as Aramis and Assa Issie in the Middle Awash and As Duma at Gona, and Middle Pliocene ones such as Hadar, Maka and its contemporaries in the Middle Awash (Frost, 2001a, b; Frost and Delson, 2002; Semaw et al., 2005; Hlusko, 2006; White et al., 2006; Levin et al., 2008). The former are similar to earlier Late Miocene sites where cercopithecids are generally common with both cercopithecines and colobines being abundant (Frost et al., 2009), whereas in the latter sites Theropithecus predominates and colobines are generally rare. The Woranso-Mille sample is thus rather more like these later sites in this regard.

Among the cercopithecids from Woranso-Mille, Theropithecus greatly predominates, making up approximately 90% of all identifiable specimens with other papionins and colobines making up the rest. While it is typical for Theropithecus to predominate among cercopithecids at most eastern African sites between approximately 3.5 and 1.5 Ma (e.g., Benefit, 1999; Frost, 2007b), WoransoMille is among the more extreme in this regard. For example, Theropithecus accounts for approximately 75e85% of the cercopithecid sample in the Shungura Formation (Bobe, 1997; Frost, 2001b), 85% at Hadar (Eck, 1993; Frost, 2001b), as well as Maka, Matabaietu (and contemporary sites), and the Hata Member of the Bouri Formation in the Middle Awash (Frost, 2001b). The genus ranges from 75 to 85% of the cercopithecid specimens at Koobi Fora (Frost, 2001b; Jablonski et al., 2008a) and West Turkana (Harris et al., 1988; Frost, 2001b), and represents about 80% at Olduvai (Jolly, 1972; Leakey and Leakey, 1973; Frost, Personal observation). In fact, among sites with large samples the relative abundance of Theropithecus at Woranso-Mille is only exceeded by that at Olorgesailie DE 89/Horizon B (which is the majority of the assemblage from the Middle Pleistocene Member 6/7) where all but one of 1951 cercopithecid specimens is T. oswaldi leakeyi (Leakey, 1977; Shipman et al., 1981; Potts, 2007; Potts, Personal communication; Frost, Personal observation). Interestingly, Laetoli, the eastern African site closest in age to Woranso-Mille, either lacks Theropithecus entirely (Leakey and Delson, 1987; Harrison, 2011) or it is uncommon (Frost, Personal observation, e.g. Laetoli specimen MB Ma 42442 þ 42447 may be Theropithecus), in spite of preserving a large monkey sample (Leakey and Delson, 1987; Harrison, 2011). The very high abundance of Theropithecus at Woranso-Mille is made all the more striking by the remarkably high frequency of cercopithecids overall. Approximately 44% of identifiable mammal specimens are cercopithecids (Haile-Selassie et al., 2007), implying that T. oswaldi represents approximately 40% of all mammals from the collection areas considered in this study. This high abundance of monkeys is unique among African sites with samples consisting of more than just a few specimens. While other eastern African sites are known with similarly high abundances of monkeys, such as Aramis and Lemudong’o (Hlusko, 2007; White et al., 2009), none is dominated by a single species to this extreme degree (Frost, 2001a; Hlusko, 2007; White et al., 2009). The only site with similar abundance is Olorgesailie DE 89/B, where cercopithecids, and Theropithecus in particular, predominate among mammals (Leakey, 1977; Shipman et al., 1981; Potts, 2007; Potts, Personal communication). There is no definitive explanation for this phenomenon, but some possibilities can be considered. The specific habitat sampled by ARI in particular, but also AMA, MKM, and MSD may include particularly rich feeding patches for early T. oswaldi. Based on dental morphology, microwear and enamel carbon isotopic ratios, T. oswaldi in general, and T. o. darti in particular, have been reconstructed as having a diet dominated by grasses (Lee-Thorp et al., 1989; Teaford, 1993; van der Merwe et al., 2003; Codron et al., 2005; El Zaatari et al., 2005; Fourie et al., 2008; Teaford et al., 2008; Cerling et al., 2013). So perhaps these areas represented patches of grass that were exploitable by T. oswaldi in particular compared with other contemporary grazers. Alternatively they may represent some other important resource such as sleeping sites. Both extant gelada and hamadryas baboons are known to consolidate in large numbers around cliffs and rocky areas that serve as sleeping sites where trees are rare (e.g., Kummer, 1968; Iwamoto, 1993). This may have been the case for T. oswaldi as well, or perhaps it preferred to use trees as sleeping sites in otherwise open areas as many baboons do today (Hamilton, 1982; Wahungu, 2001). Another possibility could be that these sites represent areas used by a predator that preferred T. oswaldi as a prey item. There are no

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

obvious signs that the Woranso-Mille series shows evidence of carnivore ravaging beyond what is seen at other contemporary sites (Haile-Selassie et al., 2007), though the fragmentary nature of much of the material makes this possibility difficult to assess pending a detailed taphonomic analysis. The significance of the overall abundance of cercopithecids in the sample, as well as the predominance of Theropithecus among the cercopithecids for interpretations of the habitat at WoransoMille is difficult to assess in isolation. In general, such a high predominance of cercopithecids would imply the presence of a significant amount of tree-cover on the landscape. However, given that T. o. darti has been shown to be a terrestrial grazer (Jolly, 1972; Lee-Thorp et al., 1989; Krentz, 1993; Frost and Delson, 2002; ElZaatari et al., 2005; Cerling et al., 2013) this may not be the case for Woranso-Mille. More definitive interpretations must await an analysis of the overall fauna. As stated above, the primitive molar morphology of the Woranso-Mille T. o. cf. darti assemblage suggests that the derived molar morphology of T. oswaldi and T. brumpti lineages evolved at least partially in parallel. In its molar morphology, the WoransoMille series ranges from specimens that are clearly Theropithecuslike to more primitive individuals that would be difficult to identify to the genus in isolation. We suggest that the last common ancestor of T. brumpti and T. oswaldi was likely similar in this regard, a variable but primitive population. Thus, later T. oswaldi and T. brumpti further developed their derived molar morphology in parallel, but from an already nascent state and not entirely de novo. Recent cladistic analysis (Gilbert, 2013) consistently placed ?Theropithecus baringensis as the sister taxon to a clade including T. gelada, T. oswaldi, and T. brumpti. The weak, but variable development of Theropithecus molar morphology seen between the two known specimens of ?T. baringensis, KNM-BC 2 and KNM-BC 1647, would be consistent with this scenario. If ?T. baringensis were indeed ancestral to, or the sister taxon of, T. oswaldi and T. brumpti then it would require that this species persisted at least 500 ka (thousands of years) after their divergence as the current hypodigm of ?T. baringensis dates to 3.2 Ma (Deino and Hill, 2002). Even though the most striking feature shared by T. oswaldi and T. brumpti may have evolved partially in parallel, there are strong morphological reasons why they could be close relatives. Most importantly, both T. oswaldi and T. brumpti share with T. gelada the distinctive manual morphology where the metacarpals and phalanges are extremely short and stout but the first metacarpal is elongate relative to the other digits (Etter, 1973; Jablonski, 1986; Jablonski et al., 2002; In preparation; Personal observation). In addition, despite the highly derived and distinctive cranial morphology of T. brumpti, all species of Theropithecus share a wellmarked sagittal crest, strong post-orbital constriction, and develop a reverse curve of Spee (Eck and Jablonski, 1987; Jablonski, 1993). Furthermore, a recent analysis of associated postcrania in T. oswaldi and T. brumpti found few differences, and several uniquely shared features including the reversed valgus angle of the femur and broad medial malleolus (Guthrie, 2011). The Woranso-Mille series implies that T. oswaldi and T. brumpti diverged by at least 3.7 Ma, and the ca. 3.6 Ma material that likely represents T. brumpti from the Turkana Basin reinforces this (Jablonski et al., 2008a). It is currently unclear whether any of the ca. 3.9 Ma specimens from Koobi Fora (Jablonski et al., 2008a) and the Middle Awash (Frost, 2001b), or the 4.1 Ma molar from Kanapoi (Harris et al., 2003) currently assigned to Theropithecus sp. or cf. Theropithecus sp. can be allocated to either lineage due to their fragmentary nature. On current evidence, this older material could, therefore, either represent a more primitive species ancestral to both T. brumpti and T. oswaldi (such as ?T. baringensis or an as yet unnamed species) or could even be earlier representatives of each

13

of these lineages. The former would place the origin of the genus Theropithecus between 4.1 and 3.9 Ma. If the latter scenario were correct, based on geography it seems more likely the Middle Awash specimen would be from the T. oswaldi lineage and the Koobi Fora and Kanapoi material could potentially be from either or both. This latter scenario would push the divergence between T. brumpti and T. oswaldi even earlier to ca. 3.9 or even 4.1 Ma and would imply that the origin of the genus was even earlier. Even though colobines are rare, they are fairly diverse; a pattern typical of most Middle Pliocene sites in eastern Africa in general and the Afar region in particular, reinforcing the impression that Woranso-Mille is more like these sites than those of the earlier Pliocene in its cercopithecid community (e.g., Frost, 2001b, 2007b). Woranso-Mille colobine species B is relatively large, being close in size to the larger species at Laetoli (Harrison, 2011), but is not in the range of the very large bodied colobines from the Lake Turkana region that appear at later Pliocene horizons (Leakey, 1982, 1987; Jablonski et al., 2008b). Their diversity also may indicate the presence of at least some tree-cover in the vicinity. The preponderance of Cercopithecoides among colobines at Woranso-Mille, however, may be consistent with the preponderance of Theropithecus, suggesting a relatively open environment. Conclusions The cercopithecid sample from the 3.6e3.8 Ma localities of AmAdo, Aralee Issie, Korsi Dora, Mesgid Dora, and Makah Mera in the Woranso-Mille Project area includes a minimum of five species from both subfamilies. These are T. oswaldi cf. darti and at least one other papionin, as well as Cercopithecoides cf. meaveae and at least two additional colobine species, including one similar in size to extant Colobus and one significantly larger. Within this sample, the T. o. cf. darti material is predominant, making up approximately 90% of the cercopithecid sample. In this sense, the Woranso-Mille series is similar to younger sites in the Afar Depression such as Hadar and Maka (Eck, 1993; Frost, 2001b; Frost and Delson, 2002). It is distinct from these other sites, however, in that cercopithecids are highly abundant compared with the overall mammalian sample (HaileSelassie et al., 2007), illustrating that while there are basin-wide patterns to cercopithecid evolution and abundance, there is also considerable variation among broadly contemporaneous sites within the Afar Depression. The Woranso-Mille T. oswaldi cf. darti series is the oldest and most primitive known and is likely near to the origin of the lineage. In this regard, it illustrates how the trends observable in the later evolution of T. oswaldi can be extrapolated back in time to at least 3.7 Ma. This is significant because it shows that T. oswaldi had begun to adapt to a terrestrial grazing niche since at least this time: one it would occupy for the next 3.50 million years to become the predominant primate in Africa until around 0.25 Ma. Furthermore, it suggests that there has been at least some parallel evolution in dental morphology between T. oswaldi and T. brumpti. Acknowledgments We thank the Authority for Research and Conservation of Cultural Heritage (ARCCH) of the Ministry of Culture and Tourism and the government of the Afar Regional State of Ethiopia for facilitating fieldwork permits. We also thank Getachew Senishaw, Alemu Ademasu, Thomas Getachew and Yared Assefa of the Paleoanthropology Laboratory of the National Museum of Ethiopia for laboratory space and access to the original fossil specimens, field participants of the Woranso-Mille Project for the fossil discoveries, and Liz Russell for photography. Sarah Elton, Eric Delson, two anonymous reviewers and the associate editor all made helpful

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

14

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15

comments that improved this manuscript; we thank them for their efforts. The National Science Foundation (BCS-0234320, BCS0542037, and BCS-1124705), the Leakey Foundation, the National Geographic Society, and the Wenner-Gren Foundation grants to YHS supported the field and laboratory work. SF thanks the University of Oregon for support of this research. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.jhevol.2014.05.003. References Anderson, M., Frost, S.R., Gilbert, C.C., Delson, E., 2013. Morphological diversity and species recognition in South African Cercopithecoides williamsi. Am. J. Phys. Anthropol. S56, 68. Benefit, B.R., 1999. Biogeography, dietary specialization, and the diversification of African Plio-Pleistocene monkeys. In: Bromage, T.G., Schrenk, F. (Eds.), African Biogeography, Climate Change, and Early Hominid Evolution. Oxford University Press, Oxford, pp. 172e188. Bobé, R., 1997. Hominid Environments in the Pliocene: an Analysis of Fossil Mammals from the Omo Valley, Ethiopia. Ph.D. Dissertation, University of Washington. Cerling, T.E., Chritz, K.L., Jablonski, N.G., Leakey, M.G., Manthi, F.K., 2013. Diet of Theropithecus from 4 to 1 Ma in Kenya. Proc. Natl. Acad. Sci. 110, 10507e10512. Codron, D., Luyt, J., Lee-Thorp, J.A., Sponheimer, M., de Ruiter, D.J., Codron, J., 2005. Utilizations of savanna-based resources by Plio-Pleistocene baboons. S. Afr. J. Sci. 101, 245e248. Deino, A.L., Hill, A., 2002. 40Ar/39Ar dating of Chemeron Formation strata encompassing the site of hominid KNM-BC 1, Tugen Hills, Kenya. J. Hum. Evol. 42, 141e 151. Deino, A.L., Scott, G.R., Saylor, B., Alene, M., Angelini, J.D., Haile-Selassie, Y., 2010. 40 Ar/39Ar dating, paleomagnetism, and tephrochemistry of Pliocene strata of the hominid-bearing Woranso-Mille area, west-central Afar Rift, Ethiopia. J. Hum. Evol. 58, 111e126. Delson, E., 1973. Fossil colobine monkeys of the circum-Mediterranean region and the evolutionary history of the Cercopithecidae (Primates, Mammalia). Ph.D. Dissertation, Columbia University. Delson, E., 1984. Cercopithecid biochronology of the African Plio-Pleistocene: correlation among eastern and southern hominid-bearing localities. Cour. Forsch. -Inst. Senckenberg 69, 199e218. Delson, E., 1993. Theropithecus fossils from Africa and India and the taxonomy of the genus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 157e189. Eck, G.G., 1987. Theropithecus oswaldi from the Shungura Formation, Lower Omo Basin, Southwestern Ethiopia. In: Coppens, Y., Howell, F.C. (Eds.), Les faunes Plio-Pléistocènes de la Basse Vallée de l’Omo (Éthiopie). Tome 3, Cercopithecidae de la Formation de Shungura. CNRS, Paris, pp. 123e139. Cahiers de Paléontologie, Travaux de Paléontologie Est-Africaine. Eck, G.G., 1993. Theropithecus darti from the Hadar Formation, Ethiopia. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 15e83. Eck, G.G., Jablonski, N.G., 1987. The skull of Theropithecus brumpti compared with those of other species of the genus Theropithecus. In: Coppens, Y., Howell, F.C. (Eds.), Les faunes Plio-Pléistocènes de la Basse Vallée de l’Omo (Éthiopie). Tome 3, Cercopithecidae de la Formation de Shungura. CNRS, Paris, pp. 11e122. Cahiers de Paléontologie, Travaux de Paléontologie Est-Africaine. El-Zaatari, S., Grine, F.E., Teaford, M.F., Smith, H.F., 2005. Molar microwear and dietary reconstructions of fossil Cercopithecoidea from the Plio-Pleistocene deposits of South Africa. J. Hum. Evol. 49, 180e205. Etter, H.F., 1973. Terrestrial adaptations in the hands of the Cercopithecinae. Folia Primatol. 20, 331e350. Fourie, N.H., Lee-Thorp, J.A., Ackermann, R.R., 2008. Biogeochemical and craniometric investigation of dietary ecology, niche separation, and taxonomy of PlioPleistocene cercopithecoids from the Makapansgat Limeworks. Am. J. Phys. Anthropol. 135, 121e135. Freedman, L., 1957. The fossil Cercopithecoidea of South Africa. Ann. Transvaal Mus. 23, 121e257. Freedman, L., 1961. Some new fossil cercopithecoid specimens from Makapansgat, South Africa. Palaeont. Afr. 7, 7e45. Freedman, L., 1965. Fossil and subfossil primates from the limestone deposits at Taung, Bolt’s Farm, and Witkrans South Africa. Palaeont. Afr. 9, 19e48. Frost, S.R., 2001a. New Early Pliocene Cercopithecidae from Aramis, Middle Awash Valley, Ethiopia. Am. Mus. Novit. 3350, 1e36. Frost, S.R., 2001b. Fossil Cercopithecidae from the Afar Depression, Ethiopia: Species Systematics and Comparison to the Turkana Basin. Ph.D. Dissertation, City University of New York. Frost, S.R., 2007a. Fossil Cercopithecidae from the Dawaitoli Formation, Middle Awash, Ethiopia. Am. J. Phys. Anthropol. 134, 460e471.

Frost, S.R., 2007b. African Pliocene and Pleistocene cercopithecid evolution and global climatic change. In: Bobe, R., Alemseged, Z., Behrensmeyer, A.K. (Eds.), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht, pp. 51e76. Frost, S.R., Delson, E., 2002. Fossil Cercopithecidae from the Hadar Formation and surrounding areas of the Afar Depression, Ethiopia. J. Hum. Evol. 43, 687e748. Frost, S.R., Plummer, T., Bishop, L.C., Ditchfield, P., Ferraro, J., Hicks, J., 2003. Partial cranium of Cercopithecoides kimeui from Rawi, Kenya. Am. J. Phys. Anthropol. 122, 191e199. Frost, S.R., Haile-Selassie, Y., Hlusko, L., 2009. Cercopithecidae. In: Haile-Selassie, Y., WoldeGabriel, G. (Eds.), Ardipithecus kadabba: Late Miocene Evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley, pp. 135e158. Gilbert, C.C., 2013. Cladistic analysis of extant and fossil African papionins using craniodental data. J. Hum. Evol. 64, 399e433. Gilbert, W. H., Frost, S. R., 2008. Cercopithecidae. In: Gilbert W. H., Asfaw, B. (Eds.), Homo erectus: Pleistocene Evidence from the Middle Awash, Ethiopia. University of California Press, Berkeley, pp. 115e132. Guthrie, E.H., 2011. Functional morphology of the postcranium of Theropithecus brumpti (Primates: Cercopithecidae). Ph.D. Dissertation, University of Oregon. Haile-Selassie, Y., Deino, A., Saylor, B., Umer, M., Latimer, B., 2007. Preliminary geology and paleontology of new hominid-bearing Pliocene localities in the central Afar region of Ethiopia. Anthropol. Sci. 115, 215e222. Haile-Selassie, Y., Saylor, B.Z., Deino, A., Alene, M., Latimer, B., 2010a. New hominid fossils from Woranso-Mille (Central Afar, Ethiopia) the taxonomy of early Australopithecus. Am. J. Phys. Anthropol. 141, 406e417. Haile-Selassie, Y., Latimer, B., Alene, M., Deino, A., Gibert, L., Melillo, S.M., Saylor, B.Z., Scott, G.R., Lovejoy, C.O., 2010b. An early Australopithecus afarensis postcranium from Woranso-Mille, Ethiopia. Proc. Natl Acad. Sci. 107, 12121e 12126. Haile-Selassie, Y., Saylor, B.Z., Deino, A., Levin, N.E., Alene, M., Latimer, B., 2012. A new hominin foot from Ethiopia shows multiple Pliocene bipedal adaptations. Nature 483, 565e569. Hamilton III, W.J., 1982. Baboon sleeping site preferences and relationships to primate grouping patterns. Am. J. Primatol. 3, 41e53. Harris, J.M., Brown, F.H., Leakey, M.G., 1988. Stratigraphy and paleontology of Pliocene and Pleistocene localities West of Lake Turkana, Kenya. In: Contributions in Science, Natural History Museum of Los Angeles County, vol. 399, pp. 1e128. Harris, J.M., Leakey, M.G., Cerling, T.E., 2003. Early Pliocene tetrapod remains from Kanapoi, Lake Turkana Basin, Kenya. In: Harris, J.M., Leakey, M.G. (Eds.), Geology and Vertebrate Paleontology of the Early Pliocene Site of Kanapoi, Northern Kenya, Contributions in Science, Natural History Museum of Los Angeles County, vol. 468, pp. 1e132. Harrison, T., 2011. Cercopithecids (Cercopithecidae, Primates). In: Harrison, T. (Ed.), Paleontology and Geology of Laetoli: Human Evolution in Context, Fossil Hominins and the Associated Fauna, vol. 2. Springer, Dordrecht, pp. 83e139. Hlusko, L.J., 2006. A new large Pliocene colobine species (Mammalia: Primates) from Asa Issie, Ethiopia. Geobios 39, 57e69. Hlusko, L.J., 2007. A new late Miocene species of Paracolobus and other cercopithecoidea (Mammalia: Primates) fossils from Lemudong’o, Kenya. Kirtlandia 56, 72e85. Iwamoto, M., 1993. The ecology of Theropithecus gelada. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 441e452. Jablonski, N.G., 1986. The hand of Theropithecus brumpti. In: Else, J.G., Lee, P.C. (Eds.), Primate Evolution, Selected Proceedings of the Tenth Congress of the International Primatological Society, vol. 1. Cambridge University Press, Cambridge, pp. 173e182. Jablonski, N.G., 1993. The phylogeny of Theropithecus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 209e224. Jablonski, N.J., Frost, S.R., 2010. Chapter 31. Cercopithecoidea. In: Werdelin, L., Sanders, W.J. (Eds.), The Cenozoic Mammals of Africa. University of California Press, Oakland, pp. 393e428. Jablonski, N.G., Leakey, M.G., Kiarie, C.K., Antón, M., 2002. A new skeleton of Theropithecus brumpti (Primates: Cercopithecidae) from Lomekwi, West Turkana, Kenya. J. Hum. Evol. 43, 887e923. Jablonski, N.G., Leakey, M.G., Antón, M., 2008a. Systematic paleontology of the cercopithecines. In: Jablonski, N.G., Leakey, M.G. (Eds.), Koobi Fora Research Project, The Fossil Monkeys, vol. 6. California Academy of Sciences, San Francisco, pp. 103e300. Jablonski, N.G., Leakey, M.G., Ward, C.V., Antón, M., 2008b. Systematic paleontology of the large colobines. In: Jablonski, N.G., Leakey, M.G. (Eds.), Koobi Fora Research Project, The Fossil Monkeys, vol. 6. California Academy of Sciences, San Francisco, pp. 31e102. Jablonski, N.G., Frost, S.R., Haile-Selassie, Y., in preparation; n.d. The earliest skeleton of Theropithecus. J. Hum. Evol. Jolly, C.J., 1972. The classification and natural history of Theropithecus (Simopithecus) (Andrews, 1916), baboons of the African Plio-Pleistocene. Bull. Brit. Mus. Geol. 22, 1e122. Krentz, H.B., 1993. Postcranial anatomy of extant and extinct species of Theropithecus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 383e422. Kummer, H., 1968. Social Organization of Hamadryas Baboons. Chicago University Press, Chicago.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003

S.R. Frost et al. / Journal of Human Evolution xxx (2014) 1e15 Leakey, M.G., 1977. Appendix B7: skeletal remains of Theropithecus (Simopithecus) oswaldi from the site DE/89, Horizon B. In: Isaac, G. (Ed.), Olorgesailie: Archaeological Studies of a Middle Pleistocene Lake Basin in Kenya. University of Chicago Press, Chicago, pp. 231e299. Leakey, M.G., 1982. Extinct large colobines from the Plio-Pleistocene of Africa. Am. J. Phys. Anthropol. 58, 153e172. Leakey, M.G., 1987. Colobinae (Mammalia, primates) from the Omo Valley, Ethiopia. In: Coppens, Y., Howell, F.C. (Eds.), Les faunes Plio-Pléistocènes de la Basse Vallée de l’Omo (Éthiopie), Cercopithecidae de la Formation de Shungura. Cahiers de Paléontologie, Travaux de Paléontologie Est-Africaine, Tome 3. CNRS, Paris, pp. 148e169. Leakey, M.G., 1993. Evolution of Theropithecus in the Turkana Basin. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 85e123. Leakey, M.G., Delson, E., 1987. Fossil Cercopithecidae from the Laetolil Beds, Tanzania. In: Leakey, M.D., Harris, J.M. (Eds.), The Pliocene Site of Laetoli, Northern Tanzania. Oxford University Press, Oxford, pp. 91e107. Leakey, M.G., Leakey, R.E.F., 1973. Further evidence of Simopithecus (Mammalia, Primates) from Olduvai and Olorgesailie. Fossil Vert. Afr. 3, 101e120. Leakey, R.E.F., 1969. New cercopithecidae from the Chemeron Beds of Lake Baringo, Kenya. Fossil Vert. Afr. 1, 53e69. Lee-Thorp, J.A., van der Merwe, N.J., Brain, C.K., 1989. Isotopic evidence for dietary differences between two extinct baboon species from Swartkrans. J. Hum. Evol. 18, 183e190. Levin, N.E., Simpson, S.W., Quade, J., Cerling, T.E., Frost, S.R., 2008. Herbivore enamel carbon isotopic composition and the environmental context of Ardipithecus at Gona, Ethiopia. In: Quade, J., Wynne, J.G. (Eds.), The Geology of Early Humans in the Horn of Africa, Geological Society of America, Special Paper, vol. 446, pp. 215e234. Maier, W., 1970. New fossil Cercopithecoidea from the Lower Pleistocene cave deposits of the Makapansgat Limeworks, South Africa. Palaeont. Afr. 3, 69e 107. Potts, R., 2007. Environmental hypotheses of Pliocene human evolution. In: Bobe, R., Alemseged, Z., Behrensmeyer, A.K. (Eds.), Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Springer, Dordrecht, pp. 25e49.

15

Rae, T.C., 2008. Paranasal pneumatization in extant and fossil Cercopithecoidea. J. Hum. Evol. 54, 279e286. Semaw, S., Simpson, S.W., Quade, J., Renne, P.R., Butler, R.F., McIntosh, W.C., Levin, N., Dominiguez-Rodrigo, M., Rogers, M.J., 2005. Early Pliocene hominids from Gona, Ethiopia. Nature 433, 301e305. Shipman, P., Bosler, W., Davis, K.L., 1981. Butchering of giant geladas at an Acheulian site. Curr. Anthropol. 22, 257e268. Strasser, E., Delson, E., 1987. Cladistic analysis of cercopithecid relationships. J. Hum. Evol. 16, 81e99. Szalay, F.S., Delson, E., 1979. Evolutionary History of the Primates. Academic Press, San Diego. Teaford, M.F., 1993. Dental microwear and diet in extant and extinct Theropithecus. In: Jablonski, N.G. (Ed.), Theropithecus: The Rise and Fall of a Primate Genus. Cambridge University Press, Cambridge, pp. 331e349. Teaford, M.F., Ungar, P.S., Kay, R.F., 2008. Molar shape and molar microwear in the Koobi Fora monkeys: ecomorphological implications. In: Jablonski, N.G., Leakey, M.G. (Eds.), Koobi Fora Research Project, The Fossil Monkeys, vol. 6. California Academy of Sciences, San Francisco, pp. 337e358. Ting, N., 2008. Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys. J. Hum. Evol. 55, 312e325. van der Merwe, N.J., Thackeray, F.J., Lee-Thorp, J.A., Luyt, J., 2003. The carbon isotope ecology and diet of Australopithecus africanus at Sterkfontein, South Africa. J. Hum. Evol., 581e597. Wahungu, G.M., 2001. Common use of sleeping sites by two primate species in Tana River, Kenya. Afr. J. Ecol. 39, 18e23. White, T.D., WoldeGabriel, G., Asfaw, B., Ambrose, S., Beyene, Y., Bernor, R.L., Boisserie, J.C., Currie, B., Gilbert, H., Haile-Selassie, Y., Hart, W.K., Hlusko, L.J., Howell, F.C., Kono, R., Lehmann, T., Louchart, A., Lovejoy, C.O., Renne, P., Saegusa, H., Vrba, E.S., Wesselman, H., Suwa, G., 2006. Asa Issie, Aramis and the origin of Australopithecus. Nature 440, 883e889. White, T.D., Ambrose, S.H., Suwa, G., Su, D.F., DeGusta, D., Bernor, R.L., Boisserie, J.-R., Brunet, M., Delson, E., Frost, S.R., Garcia, N., Giaourtsakis, I.X., Haile-Selassie, Y., Howell, F.C., Lehmann, T., Likius, A., Pehlevan, C., Saegusa, H., Semprebon, G., Teaford, M.F., Vrba, E., 2009. Macrovertebrate paleontology and the Pliocene habitat of Ardipithecus ramidus. Science 326, 87e93.

Please cite this article in press as: Frost, S.R., et al., Early Pliocene Cercopithecidae from Woranso-Mille (Central Afar, Ethiopia) and the origins of the Theropithecus oswaldi lineage, Journal of Human Evolution (2014), http://dx.doi.org/10.1016/j.jhevol.2014.05.003