Systematics of early and middle Miocene Old World monkeys

Journal of Human Evolution 57 (2009) 195–211

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Systematics of early and middle Miocene Old World monkeys E.R. Miller a, *, B.R. Benefit b, M.L. McCrossin b, J.M. Plavcan c, M.G. Leakey d, A.N. El-Barkooky e, M.A. Hamdan e, M.K. Abdel Gawad e, S.M. Hassan e, E.L. Simons f a

Department of Anthropology, Wake Forest University, Winston-Salem, NC 27106-7807, USA Department of Anthropology and Sociology, New Mexico State University, Las Cruces, NM 88003, USA c Department of Anthropology, Old Main 330, University of Arkansas, Fayetteville, AR 72701, USA d National Museums of Kenya, P.O Box 40658, Nairobi, Kenya e Geology Department, Cairo University, Cairo, Egypt f Division of Fossil Primates, Duke University, Durham, NC 27705, USA b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 1 August 2007 Accepted 23 June 2009

New information about the early cercopithecoids Prohylobates tandyi (Wadi Moghra, Egypt) and Prohylobates sp. indet. (Buluk and Nabwal, Kenya) is presented. Comparisons are made among all major collections of Early and Middle Miocene catarrhine monkeys, and a systematic revision of the early Old World monkeys is provided. Previous work involving the systematics of early Old World monkeys (Victoriapithecidae; Cercopithecoidea) has been hampered by a number of factors, including the poor preservation of Prohylobates material from North Africa and lack of comparable anatomical parts across collections. However, it is now shown that basal cercopithecoid species from both northern and eastern Africa can be distinguished from one another on the basis of degree of lower molar bilophodonty, relative lower molar size, occlusal details, symphyseal construction, and mandibular shape. Results of particular interest include: 1) the first identification of features that unambiguously define Prohylobates relative to Victoriapithecus; 2) confirmation that P. tandyi is incompletely bilophodont; and 3) recognition of additional victoriapithecid species. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: Old World monkeys Cercopithecoidea Bilophodonty Miocene Egypt Kenya

Introduction Recent research on fossil cercopithecoid material from Wadi Moghra (¼Moghara), early Miocene, Egypt, combined with reanalysis of other penecontemporaneous cercopithecoid collections, provides new insight into the systematic relationships and degree of adaptive diversity present among the earliest known Old World monkeys. The earliest known Old World monkeys belong to the Victoriapithecidae, an extinct family of cercopithecoids commonly considered to represent the sister-group to extant Old World monkeys (e.g., Benefit and McCrossin, 2002; but see Leakey et al. [2003] and Cooke [2006] for an alternative view). Members of Victoriapithecidae span a time range of ca. 20–12.5 Ma, and a geographic range across northern and eastern Africa of ca.

* Corresponding author. E-mail addresses: [email protected] (E.R. Miller), bbenefi[email protected] (B.R. Benefit), [email protected] (M.L. McCrossin), [email protected] (J.M. Plavcan), [email protected] (M.G. Leakey), [email protected] (A.N. El-Barkooky), [email protected] (M.K. Hamdan), mkabdelgawad@ gmail.com (M.K. Abdel Gawad), safi[email protected] (S.M. Hassan), [email protected] (E.L. Simons). 0047-2484/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2009.06.006

4500 km between the most distant localities (Fig. 1). Currently, the family comprises four or five species in two genera. These taxa, along with their sample size and locality, are listed in Table 1. Some victoriapithecid species are represented by relatively large sample sizes (e.g., Victoriapithecus macinnesi, n ¼ ca. 2500; Prohylobates kipsaramanensis, n ¼ 89), and material of V. macinnesi has been particularly well-studied (e.g., Benefit, 1987, 1993, 1994; Harrison, 1989; Benefit and McCrossin, 1991, 1997). However, interpreting the systematic relationships among members of the Victoriapithecidae has always been problematic. One major reason is that Prohylobates tandyi from Wadi Moghra, Egypt – the first named genus and species (Fourtau, 1918) – is represented by only a few specimens with abraded teeth, so there has never been a clear understanding about which features actually diagnose Prohylobates. This problem is compounded by the fact that a second genus, Victoriapithecus, from eastern Africa, was erected without comparing the material to that of Prohylobates (von Koenigswald, 1969). In fact, as M. Leakey discussed more than twenty years ago, ‘‘there are no clearly defined characters separating the two genera Prohylobates and Victoriapithecus, and it is possible that the genera are synonymous’’ (Leakey, 1985: 9). Because Prohylobates is the name with priority, Leakey (1985) assigned fossil cercopithecoid

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P. tandyi from other early and middle Miocene taxa; 2) characteristics that differentiate Prohylobates from Victoriapithecus; and 3) identification of new taxa from both eastern and northern Africa. Abbreviations An upper case letter denotes a tooth in the maxillary series and a lower case letter a tooth in the mandibular series. For example, M2 is an upper second molar, m1 a first lower molar, and dp4 a deciduous lower fourth premolar. Institutional abbreviations are as follows: AMNH, Department of Vertebrate Paleontology, American Museum of Natural History, New York; CMK-BAR, Community Museum of Kenya; CGM, Cairo Geological Museum; DPC, Duke University Primate Center Division of Fossil Primates, Durham; KNM-MB, Kenya National Museums, Maboko Island; KNM-NL, Kenya National Museums, Nabwal; KNM-WS, Kenya National Museums, West Stephanie (Buluk); UMP-MOR, Uganda Museum of Paleontology, Moroto; CUWM, Cairo University, Wadi Moghra (WM numbers are field numbers, the material does not have accession numbers); YPM, Yale Peabody Museum, New Haven. Systematics Order Primates Linnaeus, 1758 Suborder Anthropoidea Mivart, 1864 Infraorder Catarrhini Geoffroy, 1812 Superfamily Cercopithecoidea Gray, 1821 Family Victoriapithecidae von Koenigswald, 1969 Included genera Prohylobates Fourtau, 1918; Victoriapithecus von Koenigswald, 1969; Noropithecus gen. nov.

Figure 1. Map of early and middle Miocene cercopithecoid localities.

material from Buluk, Kenya, to an indeterminate species of Prohylobates rather than to Victoriapithecus, although she acknowledged that this might become untenable with future discoveries. Placement of the Buluk material in Prohylobates sp. indet. (Leakey, 1985), coupled with only a vague diagnosis of the type material of Prohylobates, has contributed to a situation whereby early cercopithecoid specimens with obviously comparable dental morphology sometime reside not only in different species but in different genera. For example, material from Moroto, Uganda, has been allocated to Prohylobates macinnesi (Pickford and Kunimatsu, 2005) rather than Victoriapithecus macinnesi, and material from Kipsaraman, Kenya, was named Prohylobates kipsaramanensis, despite both collections being described as morphologically similar to Victoriapithecus macinnesi (Pickford et al., 2003; Pickford and Kunimatsu, 2005). In other cases the converse of this problem holds true. For example, recent work indicates that two morphologically distinct cercopithecoid taxa from Moghra are conflated under the name Prohylobates tandyi (see below). In addition, reassessment of the mandibular fragment originally named Prohylobates simonsi from Jabal Zaltan, Libya, indicates that the specimen is distinct from other victoriapithecids and warrants placement in a new genus, Zaltanpithecus (Benefit, 2008). In this contribution, analysis of new, as well as previously described Early and Middle Miocene fossil cercopithecoid material from northern and eastern Africa, is used to systematically revise species currently assigned to the Victoriapithecidae. This revision is based on the identification of: 1) features that clearly distinguish

Diagnosis An extinct family of Old World monkey distinguished from Cercopithecidae (Colobinae and Cercopithecinae) by having incomplete development of bilophodonty in either the upper or lower molar series, variable retention of crista obliqua and m1/m2 hypoconulids, p4 oriented strongly oblique to the cheek tooth row, and a high degree of molar flare due to the close approximation of cusp tips relative to crown width. Remarks Many of the features listed above as diagnostic of Victoriapithecidae (e.g., presence of a crista obliqua, presence of hypoconulids, incomplete bilophodonty) are also characteristic of basal non-cercopithecoid catarrhines, which means that the Victoriapithecidae is largely diagnosed on the basis of primitive features. Such a reliance on primitive traits may be considered suboptimal, but the situation may have a parallel in the Platyrrhini, a group whose members form a coherent clade, although no shared derived morphological features uniting all platyrrhines have ever been identified. Instead, the group is diagnosed by the retention of many primitive anthropoid features.

Table 1 Victoriapithecid sample sizes and localities. Taxon

P. tandyia

P. sp. indet.b

P. simonsic

P. kipsaramanensisd

V. macinnesie

N Localities

5 Egypt (Wadi Moghra)

17 Kenya (Buluk, Nabwal)

1 Libya (Jabal Zaltan)

89 Kenya (Kipsaraman)

2500 Kenya (Maboko Island, Ombo, Loperot, Majiwa, Nyakach, Nachola, Ngorora); Uganda (Napak, Moroto)

a b c d e

Miller, 1996, 1999. Harris and Watkins, 1974; McDougall and Watkins, 1985. Delson, 1979. Pickford and Kunimatsu, 2005. Benefit, 1987.

E.R. Miller et al. / Journal of Human Evolution 57 (2009) 195–211

In addition, the diagnosis of Victoriapithecidae presented here is substantially more conservative than one published previously (Benefit, 1993). The reason for this is that the previous diagnosis was based on the assumption that features present in V. macinnesi – the best known species and the only one for which cranial and postcranial information is available – were likely representative of the family as a whole. However, most species in Victoriapithecidae are represented only by dental and gnathic remains, so it is unknown whether the cranial and postcranial traits observed for V. macinnesi are also characteristic of other members of the family. Prohylobates Fourtau, 1918 Prohylobates tandyi Fourtau, 1918 Diagnosis As for the genus.

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Holotype Specimen CGM 30936, a right mandible fragment with alveoli of i1-2, c, p3, and damaged crowns of p4-m3 (Fig. 2D, E) (also figured in Fourtau, 1918, 1920: Figure 63; Simons, 1969: Figs. 1B, 2, and 3B). Referred material Specimen DPC 6235, a right mandibular fragment with the root of the canine, p3-m3 (Fig. 2A–C) (also figured in Simons, 1994: Fig. 2). Age Early Miocene (Miller, 1996). Distribution Wadi Moghra, Egypt. Emended diagnosis Differs from other victoriapithecids in possessing the following combination of features: incomplete lower molar bilophodonty, with no lophids connecting the entoconid and hypoconid on m1; the metaconid and protoconid on m3; lower molar proportions m1 < m2  m3; m3 hypoconulid reduced.

Figure 2. Prohylobates tandyi. (A) DPC 6235, right ramus, lateral, anterior is right. (B) Occlusal and (C) occlusal with circles highlighting lack of lophids. (D) CGM 30936, right ramus, type specimen P. tandyi, lateral, anterior is left. (E) Occlusal. Scale ¼ 1 cm. Photos of DPC 6235 by Robert Usery. Photos of CGM 30936 by R. Ciochon.

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Figure 3. Differences in relative lower molar proportions in P. tandyi (m1 < m2  m3) versus V. macinnesi (m1 < m2 < m3). Note also the small size difference between m1 and m2 in P. tandyi.

Description Specimen DPC 6235 was first described by Simons (1994) and is similar in all its known parts to the type specimen of P. tandyi (CGM 30936). Although worn and abraded, the occlusal morphology visible on DPC 6235 clearly shows that P. tandyi was not completely bilophodont, lacking transverse lophids at least on the distal m1 and mesial m3 (Fig. 2C). Prohylobates tandyi has smaller molar teeth than most other victoriapithecids (Tables 2 and 3). Summed lower molar area (Table 3) ranges between about 87–98 mm2 in the Moghra specimens, but typically ranges between 87–191 mm2 in individuals of

Victoriapithecus, with only three out of 27 (9%) known Victoriapithecus specimens having molar sizes falling within the range for P. tandyi. Prohylobates tandyi also differs from other victoriapithecids in its relative lower molar proportions. In P. tandyi, m2 is the largest tooth in the lower molar series, both in length and in area, so that m1 < m2  m3. Also, m1 approaches m2 in size, being about 80–90% the size of m2. Individuals of Victoriapithecus show a different size gradient in their lower molar row. In V. macinnesi, m3 is the largest tooth in the lower molar series, such that m1 < m2 < m3. In addition, m1 is smaller relative to m2 than it is in P. tandyi, averaging about 66% the size of m2 (range ¼ 57%–79%) (Fig. 3). Material from Buluk shows a mix of features. Like V. macinnesi, the Buluk cercopithecoids have a molar size rank of m1 < m2 < m3, and although the size of m1 vs. m2 could only be assessed on one specimen, this molar ratio appears to be intermediate between that observed for P. tandyi and V. macinnesi, with m1 about 71% the size of m2. The portion of the mandibular symphysis preserved in DPC 6235 has a cross-sectional profile resembling that of KNM-MB 18893, a female mandible of V. macinnesi, in the angle and anteroposterior thickness of the planum alveolare. Because DPC 6235 is broken inferiorly, there is no indication of the height of the genial pit or shape of the inferior torus in P. tandyi. The corpus of DPC 6235 is shallower than in most other victoriapithecids (other specimens from Moghra, Buluk, Nabwal, Kipsaraman), with its height below m1

Table 2 Lower canine and molar dental metrics. Locality and Taxon

Specimen

c root

Wadi Moghra Prohylobates tandyi P. tandyi

CGM 30936 DCP 6235

Gen. indet. mogharensis Gen. indet. mogharensis Gen. indet. mogharensis

CGM 30937a DCP 3880 WM 06–31

Jabal Zaltan Z. simonsi

AMNH 17768

Maboko Island, Kenya Victoriapithecus macinnesi Mean Range N Buluk Noropithecus bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis Kipsaramanc cf. N. kipsaramanensis

Nabwal cf. N. fleaglei

KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS

m1

m2

m3

L

W

Area

L

MW

DW

L

MW

DW

L

MW

DW

6.3a

3.85a

24.25a

5.6 6.2

5.4 4.25a

4.1a

6 6.45

5.8 5.05a

4.7a

6.5 6.15

5 4.54

3.9

6.6

6

6.5

5a

6.8

5.2

3.8a

6.75a

5.9a

6.15a

7.3 7.5a 6.65a

6.65a

6.45a

8.4a

6.2a

4.25a

10.4

11

10.4

12.9

9.1

8.2

5.8 4.47 23.52 6.3 5.4 5.3 7.6 6.8 6.5 8.7 6.2 5.3 4.02–6.85 3.5–5.3 14.07–36.31 5.4–7.6 4.25–6.65 4.5–6.5 6.2–8.95 5.5–8.65 4.5–7.75 7.10–10.85 4.9–7.65 4.1–6.8 5b 5b 146 145 140 109 107 103 225 225 223 5b 122 123 6.8a 7659 12638 12639 12640 12641 12642 12646 12647 12650 12651

4.35a

7.8a

6.9a

7.5a

8

7.5

7.2

7.6

7.7

10

6

29.6a 7 6.9a

7.05

6.1

6.4

5.9 6.3a

10.3

7.2

6.3

10.2

8.3

7

11.3 9.3 8.6

7.6 6.4 6.3

6.9 5.6 5

6.12 5.7–6.6 7

5 4.4–5.3 7

7.15

5.25

6 7.7

Mean Range N

7.47

6.82

6.93

1

1

1

8.11 7.3–8.8 7

KNM-NL 30949

7.2

6.65

6.35

8.3

Measurements for CGM from Simons, 1969 (see also note in Leakey, 1985); measurements of AMNH by Delson in Leakey, 1985; measurements of KNM-WS from Leakey, 1985, except KNM-WS 123 which was measured by B.R.B. Measurements of BAR from Pickford and Kunimatsu, 2005; all other measurements by B.R.B. L ¼ length; W ¼ width; MW ¼ mesial width; DW ¼ distal width. a Indicates estimated. b Measured in mandibles with canine root preserved in situ. c Does not include material identified as m1 or m2.

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Table 3 Lower molar dental indices. Area calculated as MW  L. Locality and taxon

Specimen

m1 area

m2 area

m3 area

Summed area

m1/m2

Wadi Moghra Prohylobates tandyi P. tandyi

CGM 30936 DCP 6235

30.24 26.35a

34.8 32.57a

32.5 27.92a

97.54 86.84a

0.87 .81a

Gen. indet. mogharensis Gen. indet. mogharensis Gen. indet. mogharensis

CGM 30937a DCP 3880 WM 06–31

39.6

47.45

35.36

122.41

0.83

39.82a

44.22a

52.08a

84.05a

.90a

Jabal Zaltan Z. simonsi

AMNH 17768

114.4

117.39

52.23 38.42–67.65 48

57.47 39.2–69.12 37

132.81 86.5–191.37 27

0.66 0.57–0.79 32

b

Maboko Island, Kenya Victoriapithecus macinnesi

Buluk Noropithecus bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis N. bulukensis

Kipsaramanc cf. N. kipsaramanensis

Nabwal cf. N. fleaglei a b c

Mean Range N KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS KNM-WS Mean Range N

35.25 26.16–49.28 42 122 123 7659 12638 12639 12640 12641 12642 12646 12647 12650 12651

53.82a 74.16 42.7

60

0.71 84.66

58.52 85.88 59.52 54.18 45.12 43.91 42.7–45.91 2

59.36 58.52–60 2

71.6 54.18–85.88 5

50.96

Mean Range N

1

49.84 41.61–58.08 7

KNM-NL 30949

47.88

59.35

Indicates estimated. Includes only teeth preserved in mandibles, measured by B.R.B. Does not include material identified as m1 or m2.

approximating that observed for female specimens of V. macinnesi. A single mental foramen is positioned below p4 on both specimens. Specimen DPC 6235 preserves the root but not the crown of what would have been a large canine. Because of its shallow mandibular corpus, overall small size, and lack of an exaggerated p3 honing facet, DPC 6235 has been viewed as a female (Simons, 1994). However, the size and orientation of the canine root suggest that DPC 6235 may represent a male (see Fig. 4). In addition, despite the fact that no canine crowns are preserved on either of the P. tandyi specimens, length and width dimensions of the canine root are taken here to represent what the minimum size of the canine would be if measured at the cervix; these dimensions fall on the high end of the range for Victoriapithecus, and so are more consistent with the size of male rather than female specimens from Maboko (Table 2). Plus, given the small size of the cheek tooth row in P. tandyi relative to other victoriapithecids, canine size in P. tandyi appears to be especially large, and DPC 6235 is distinct from members of Victoriapithecus in pairing a large canine with a relatively small cheek tooth row (Fig. 5). In short, if DPC 6235 represents a female, then it has a large canine relative to molar size. If DPC 6235 represents a male, as perhaps indicated by the large canine size, then it has an unusually small p3 honing facet relative to other male Old World monkeys. Either way, P. tandyi is distinct from all other cercopithecoids. Remarks The observation that P. tandyi lacks transverse lophids, at least on distal m1 and mesial m3, supports the work of Simons and Delson (1978; Delson, 1979), who described the lower molars of

P. tandyi as being ‘‘not as completely bilophodont as those of Victoriapithecus’’ (Simons and Delson, 1978: 112). This conclusion was questioned by Leakey (1985) and Miller (1996), who thought that specimens of Prohylobates known at the time were too worn to assess their degree of bilophodonty with any degree of confidence. However, recovery of DPC 6235 supports Delson’s proposal (1979) that North African Prohylobates is best understood as a more primitive genus of cercopithecoid than Victoriapithecus, because Prohylobates is not as completely bilophodont. The presence of incomplete bilophodonty along with a shallower mandibular corpus, the presence of small cheek teeth including a very small m3, and a molar size sequence of m1 < m2  m3, enhance the distinctiveness of North African P. tandyi relative to other victoriapithecids. Gen. indet. mogharensis Fourtau, 1918 Synonymy ?Dryopithecus mogharensis Fourtau, 1918 Prohylobates tandyi (part) Simons and Pilbeam, 1965 Referred material A right mandibular fragment, CGM 30937a, with alveoli of c, p3–4, and damaged crowns of m1–3 (Fig. 6A, B) (also figured in Fourtau, 1920: Figures 64a, a0 ; Simons, 1969: Fig. 1C). CGM 30937b, a left mandible fragment with p4-m2 (Fig. 6 G, H) (also figured in Fourtau, 1920: Figures 64b, b0 ; Simons, 1969: Figs. 1A and 3A).

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Age Early Miocene (Miller, 1996). Distribution Wadi Moghra, Egypt. Discussion

Figure 4. Comparison of lower canine size in (A) cast of KNM-MB 38182, male Victoriapithecus, (B) P. tandyi DPC 6235, and (C) cast of KNM-MB 31279, female Victoriapithecus. All lateral views. P. tandyi has been reversed to facilitate comparison. Scale ¼ 1 cm. Photo (B) by Robert Usery.

The original of CGM 30937b is presumed lost, but a cast is available. DPC 3880, a right mandibular fragment with damaged partial crowns of m1-m3 (Fig. 6C, D) (see also Simons, 1994: Fig. 1). CUWM 06-31, a right mandibular fragment with canine alveolus, roots of p3-m3 (Fig. 6E, F).

Figure 5. Graph of canine area compared with total molar area for V. macinnesi and DPC 6235, P. tandyi. Only those specimens preserving the canine root as well as all three molars intact in the jaw were used, resulting in a small number of specimens for this comparison.

Recognition of a second primate taxon at Moghra has a precedent. Fourtau (1918) originally identified two of the gen. indet. mogharensis specimens (CGM 30397a and b) as belonging to ?Dryopithecus mogharensis rather than P. tandyi. Other researchers emended this by recognizing that all Moghra primates were cercopithecoids rather than hominoids (Le Gros Clark and Leakey, 1951; see also Remane, 1965), and in 1965 – with no other early Miocene monkey material available for comparison – Simons and Pilbeam followed the conservative procedure of attributing size and morphological differences between the smaller and larger Moghra specimens to sexual dimorphism. Simons and Pilbeam (1965) then synonymized ?D. mogharensis with Prohylobates tandyi and placed Prohylobates in the Cercopithecoidea. However, work presented here indicates that material originally assigned to ?D. mogharensis, while not belonging to Dryopithecus, is distinct from Prohylobates and therefore the ‘‘mogharensis’’ material represents a species without a genus. Although it is possible to demonstrate that the ‘‘mogharensis’’ material is distinct from that of other victoriapithecids, all known ‘‘mogharensis’’ specimens are partial mandibles with tooth crowns either missing or so abraded that no occlusal details are visible. Despite the fragmentary nature of this material, a lectotype (CGM 30937a) has been designated (Simons, 1969), but we refrain here from applying a formal generic nomen pending the recovery of specimens with sufficient morphology to permit a differential diagnosis. Despite the fact that no occlusal details are available on any of the gen. indet. mogharensis specimens, members of this taxon are clearly larger than P. tandyi, and from what can be seen of their mandibular morphology, the gen. indet. mogharensis specimens have proportionally deeper and narrower mandibular corpora than do individuals of P. tandyi, as well as most other victoriapithecids (Fig. 7, Table 4). A general trend is present among male and female members of Victoriapithecus, in that as corpus height increases corpus width increases. Deeper-jawed specimens also tend to have proportionally thicker corpora. However, for the two gen. indet. mogharensis specimens, the mandibular corpus is unlike that seen among specimens of Victoriapithecus, in being deep without being correspondingly broad. Although a match for the mandibular proportions seen among the gen. indet. mogharensis specimens may sometimes be found among the Victoriapithecus sample (for m1, n ¼ 1 or 2 out of 12, for m2, n ¼ 1 out of 19), the overall trend within Victoriapithecus is clearly different. Because of the small sample size available for the Moghra specimens (n ¼ only 2 measurable specimens), and the fragmentary nature of the material, it is not possible to assess more fully how morphologically distinctive the larger Moghra specimens are relative to other victoriapithecids. Nonetheless, it may be taxonomically important that it is not one but both of the measurable mogharensis corpora that show the pattern of having a very deep corpus – as deep or deeper than for other victoriapithecids, without being correspondingly broader. In the past, differences in size and mandibular construction between the larger and smaller Moghra specimens have been attributed to a high degree of sexual dimorphism in P. tandyi. Given the deep mandibular corpora of the gen. indet. mogharensis specimens, these individuals may well represent males, but if they do they

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201

Figure 6. Gen. indet mogharensis. (A) CGM 30937a, right ramus, lateral and (B) occlusal. (C) DPC 3880, right ramus, lateral and (D) occlusal. (E) WM06–31, lateral and (F) occlusal. (G) YPM cast of CGM 30937b, left ramus, lateral. (H) Cast of CGM 30937b, occlusal. Scale ¼ 1 cm. Photos C, D by Robert Usery, A, B, E, F, H by R. Ciochon.

are not the males of P. tandyi. Metric comparison between the gen. indet. mogharensis material and a large sample of extant cercopithecoids indicates that the size difference observed among the smaller and larger Moghra monkeys, if due to sexual dimorphism, would be highly unusual. Depth of the mandibular corpus at m1 or m2 was measured for the smaller (CGM 30396 [type of P. tandyi], DPC 6235) and larger (GCM 30937a, DPC 3880) Moghra specimens (Table 4), and compared with a large sample of extant anthropoid taxa (n ¼ 190) ranked by degree of sexual dimorphism (Plavcan, 2003) (Table 5, Fig. 8). The Moghra specimens fall into two clusters, which is initially suggestive of males and females of a single species.

However, assuming that these clusters represent males and females, the ratio of dimorphism in this taxon would be 1.46 (ratio of ‘‘males’’ to ‘‘females’’), which among extant anthropoids is exceeded only by Mandrillus sphinx (ratio of males to females ¼ 1.55) (Plavcan, 2003). Because the Moghra sample is small, a bootstrapping program was written in Matlab to examine estimates of dimorphism in the Moghra sample compared with that observed among extant primate species. From each extant species, two males and females were drawn, corresponding to the putative sex ratio of the Moghra specimens if they comprise a single species. Analyses were carried out on a subset of 102 extant anthropoid samples for which

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m1 corpus width

m1 corpus height versus width 14 13 12 11 10 9 8 7 6

V. macinnesi Nabwal specimen P. tandyi Gen. indet. Moghra 10

15

20

25

m1 corpus height m2 corpus height versus width m2 corpus width

16 V. macinnesi

14

Nabwal specimen

12

BAR 219'02 10

Buluk specimens Gen. indet. Moghra

8 6 10

15

20

25

m2 corpus height Figure 7. Corpus height versus width at (A) m1 and (B) m2. Note that gen. indet. mogharensis specimens have deep but relatively thin mandibular corpora compared with other victoriapithecids, and the Nabwal specimen has a more robust mandibular construction than either P. tandyi or the Kipsaraman monkey.

The potentially high level of dimorphism in the Moghra sample coupled with the large range of variation in the ‘‘female’’ specimens raises the question of how likely it would be to randomly sample such a distribution from a single species. To evaluate how easily the Moghra distribution of jaw depths could be drawn for a single species, the number of samples for which both dimorphism and female range simultaneously equaled or exceeded the Moghra sample was also tabulated. None of the 102 anthropoid species in the reference sample simultaneously yielded both a level of dimorphism and a range of female values that equaled or exceeded that of the Moghra sample (Table 5). Both conditions were met in only 9 out of 120 species, with the greatest frequency (0.83%) occurring in Cercopithecus mitis kolbi. Results from bootstrapping analyses suggest that, while the Moghra specimens could possibly be drawn from a single, highly sexually dimorphic species, the likelihood is low. Both the level of dimorphism and the range of putative female values are unusual among anthropoid primates. Combined, it was not possible to generate the Moghra distribution from any of the available extant samples (Table 5). Although it is impossible to falsify a singlespecies hypothesis on the basis of metric and bootstrapping analysis alone (Plavcan and Cope, 2001), the unusual metric distributions evaluated here, combined with observed morphological differences in mandibular morphology between the larger and smaller Moghra

Table 4 Mandibular corpus dimensions. H ¼ corpus height, W ¼ corpus width.

a minimum of 10 males and 10 females were available. All data were log-transformed to standardize variances across the large size range (from Cebuella to Gorilla). Dimorphism was calculated as the natural log of the male to the female mean values (¼ ln[male mean] – ln[female mean]). For each reference species, 10,000 samples were drawn with replacement, dimorphism tabulated, and the number of samples noted for which dimorphism exceeded that of the Moghra specimens. Of the 102 reference samples, only 7 produced a level of dimorphism equal to or exceeding that of the Moghra specimens at the 5% level (i.e., 5% or more of the randomly drawn samples exceeded the dimorphism of the Moghra sample) (Table 5). On the basis of these results, the level of mandibular depth dimorphism between the putative ‘‘male’’ versus ‘‘female’’ Moghra specimens is highly unusual, but would not be unique among extant primates. However, another salient feature of the Moghra jaw depth distribution is the wide dispersion among putative ‘‘females.’’ The ratio of jaw depth in the larger to smaller Moghra ‘‘females’’ is 1.26. This figure is within the range of values observed for only the most variable single sex samples among all anthropoid primates, and would indicate a fairly high level of dimorphism even between a male and a female of a single anthropoid species (Fig. 8). Among all extant anthropoids, only 20 of 160 species exhibit a jaw depth dimorphism ratio greater than 1.26 (see Plavcan, 2003). These results raise the question of whether or not the range of values seen for the putative ‘‘females’’ is unusual. To test this hypothesis, a second Matlab program was written to bootstrap the range of variation from female samples of extant anthropoids, and compare them to the range of the two ‘‘female’’ Moghara specimens. For this exercise, all data were natural log-transformed, 10,000 samples of n ¼ 2 were drawn from each taxon with replacement, the difference was calculated between the two specimens, and the number of differences exceeding that observed for the ‘‘female’’ Mohgra specimens was tabulated. Of the 102 samples, 13 produced a size range for females equal to or exceeding that of the Moghra ‘‘females’’ at the 5% level (Table 5).

Specimen

p4 H

m1 W

H

m2 W

H

m3 W

H

P. tandyi CGM 30936 DCP 6235

18.45 13.48

8.89 6.75

Gen. indet mogharensis CGM 28971 DCP 3880

23.84 22.7

9.58 23.95 10.54 24.63 8.47 22.4 9.84

8.32

V. macinnesi KNM-MB 1 KNM-MB 34 KNM-MB 11674 KNM-MB 11676 KNM-MB 11931 KNM-MB 12005 KNM-MB 18735 KNM-MB 18736 KNM-MB 18738 KNM-MB 18739 KNM-MB 18993 13.9 7.35 KNM-MB 21027 9.05 KNM-MB 21033 KNM-MB 29158 KNM-MB 31279 KNM-MB 31280 KNM-MB 31282 KNM-MB 31283 KNM-MB 31284 KNM-MB 31288 KNM-MB 31291 KNM-MB 97Mb40297

21.8 14.1 14.35 15.35 15.55 16.25 13.85 14.2 8.1 13.9 17.5 10.1 16.05 13.5 8.05 12.09 17.5 11.1 15.6 23.4 13.1 22.1 17.27 19.3 10.75 19.9 20.6 21 9.7 18.9 18.3 9 18.2 16.2 8.5 22.17 11.07 22.34

N. bulukensis KNM-WS 12638 KNM-WS 12639

21.6

24.2 22.5

23.25 14.15 23.25 11.9 20.9

cf. N. fleaglei KNM-NL 20949

20.53 9.77

20.72 10.5

18.44 12.2

cf. N. Kipsaramanensis BAR 219’02 17.97

15.5 14.85 21.3 13.75

W

15.1 15.1 8 8.5 7.2

18

8.9 9.4

15 17.8

10.55

9.65 8 9.75 9.9 9.95 9.9 10.05 14.8 11 9.2 11.8 14.55 10.45 11.6 14.02 10.7 11.01

10.05

12.2

8.3

All measurements by B.R.B. except for BAR 219’02, which are from Pickford and Kunimatsu (2005).

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Figure 8. Mandibular depth at m1 or m2 in gen. indet mogharensis and P. tandyi compared with males and females of four extant cercopithecoid taxa of medium size: Cercopithecus hamlyni, C. nictitans, Cercocebus atys, and Macaca mulatta. Mo ¼ gen. indet mogharensis, P ¼ Prohylobates, F ¼ females, M ¼ males.

specimens, lends support to the hypothesis that two species are present in the sample.

Zaltanpithecus Benefit, 2008 Diagnosis

Remarks Some of the gen. indet. mogharensis specimens have had conflicting reported accession numbers. Fourtau (1918) was the first to describe the Moghra primates but no specimen numbers were given in his monograph. The first publication of specimen numbers associated with the Moghra material was in Simons (1969), and at that time the type of P. tandyi was identified as CGM 30936, the specimen originally described as the type of ?D. mogharensis (here CGM 30937a) was identified as CGM 28971, and a second ?D. mogharensis specimen (here CGM 30937b), was identified as CGM 29872. At the Cairo Geological Museum, the type of P. tandyi carries the number CGM 30936, and the two other specimens are accessioned together under the number CGM 30937. It makes sense that the sequential numbering of the Moghra primate material is probably the original numbering system, because it is logical that Fourtau’s specimens would have been accessioned at the same time, and so would carry consecutive numbers. It is unknown how the number CGM 28971 came to be associated with the original type of ?D. mogharensis, or how the number CGM 28972 sometimes came to be associated with Fourtau’s referred specimen. Nonetheless, gen. indet. mogharensis specimens housed together as CGM 30937 (Fig. 6G, H; see also Fourtau, 1918: Figures 64b, b0 ; Simons, 1969: Figs. 1A and 3A), are identified here by the number they carry at the museum where the originals were accessioned, with the modification CGM 30937a, b.

Differs from other victoriapithecids in having a mandible and teeth of much larger size; m2 broader than long; m2 with two independent distal roots; m3 with a bifurcated mesial root. Zaltanpithecus simonsi (Delson, 1979) Holotype A partial mandible, AMNH 17768, with m2–3 (Fig. 11G, H). Also figured in Delson (1979). Age Middle Miocene (Pickford, 1991). Distribution Jabal Zaltan (Gebel Zelten), Libya. Diagnosis As for genus. Remarks The Zaltan specimen shares with other victoriapithecids a quadrate arrangement of cusps on m2, m2 molar waisting, and a high degree of buccal flare. Because Z. simonsi is known only from a single mandibular fragment preserving worn m2–3, additional derived characteristics that would define the taxon better are not preserved. However, the large size and bifurcated lower molar roots distinguish Z. simonsi from other victoriapithecids (Benefit, 2008). Victoriapithecus macinnesi von Koenigswald, 1969 Synonymy Victoriapithecus leakeyi von Koenigswald, 1969; Prohylobates macinnesi Pickford et al., 2003

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Table 5 Results from bootstrap experiments comparing the Moghara specimens to extant species. Listed are the percentage of samples out of 10,000 replications (each species) that showed greater dimorphism, greater female range, and both greater dimorphism and female range than the Moghara jaw depth sample. Species

Dimorphism

Female range

Both

Platyrrhini Alouatta seniculus seniculus Alouatta seniculus insulanus Alouatta pigra Alouatta fusca Alouatta palliata aequatorialis Aotus azarae Aotus lemurinus Aotus trivirgatus lemurinus Aotus vociferans Ateles fusciceps Ateles geoffroyi vellerosus Cacajao melanocephalus Callicebus moloch discolor Callicebus torquatus lugens Callithrix argentata argentata Callithrix humeralifer humeralifer Callithrix jacchus penicillata Cebuella pygmaea pygmaea Cebus albifrons cesarea Cebus apella libidinosus Cebus apella paraguyanus Cebus capucinus capucinus Cebus olivaceus castenea Cebus olivaceus apiculatus Chiropotes satanas chiropotes Lagotherix lagothricha cana Lagothrix lagothricha poeppigii Pithecia irrorata irrorata Pithecia monachus Pithecia pithecia Saimiri oerstedii oerstedii Saimiri sciureus macrodon Saimiri ustus Saguinus fuscicollis nigrifrons Saguinus midas niger Saguinus mystax mystax Saguinus nigricollis graellsi Saguinus oedipus geoffroyi

2.15 1.68 1.64 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0.04 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 5.34 0 0.02 0 0 0 1.62 2.43 1.50 0 0 1.20 1.85 0 0 1.25 0 0 0 0 0 0 0 0 0 0 0 0 0 5.54 0 0 0.47 0 0 0

0 0

Catarrhini Cercopithecoidea Cercocebus agilis agilis Cercocebus torquatus atys Cercopithecus aethiops hilgerti Cercopitheecus aethiops ngamiensis Cercopithecus aethiops sabaeus Cercopithecus ascanius whitesidei Cercopithecus cephus cephus Cercopithecus denti Cercopithecus diana diana Cercopithecus hamlyni Cercopithecus lhoesti lhoesti Cercopithecus mitis kolbi Cercopithecus mona Cercopithecus neglectus Cercopithecus nictitans nictitans Cercopithecus petaurista petaurista Cercopithecus pogonius grayi Cercopithecus wolfi wolfi Colobus angolensis cottoni Colobus guereza caudatus Colobus guereza kikiyuensis Colobus polykomos polykomos Colobus satanas Erythrocebus patas Kasi vetulus Lophocebus albigena aterrimus Lophocebus albigena johnstoni Macaca fascicularis fascicularis Macaca hecki Macaca mulatta mulatta

0 0 0.80 0.84 7 0 0 0 0 3.75 6.16 7.53 0.82 0 0 0 0 0 0 0.75 0 0 0 7.41 0 0 0 0 0.14 0.21

0 0 9.52 2.57 0 0 0 0 0.64 16.87 4.24 13.68 6.62 0 0.28 1.27 0.87 0 0 0 0 0.99 0 0 0 0 0 0 2.69 6.82

0 0

.01 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

Table 5 (continued ) Species

Dimorphism

Female range

Both

Macaca nemestrina nemestrina Macaca nigra Macaca sinica Mandrillus leucophaeus leucophaeus Miopithecus talapoin talapoin Nasalis larvatus Papio anubis Papio ursinus Presbytis comata Presbytis melalophos chrysomelas Presbytis potenziani Procolobus badius badius Procolobus badius oustaletti Procolobus verus Pygathrix nemaeus nigripes Semnopithecus entellus thersites Theropithecus gelada Trachypithecus cristata pyrrhus Trachypithecus cristata ultima Trachypithecus obscura obscura Trachypithecus pileata shortridgei

0.35 2.19 0.69 36.43 0 14.60 1.58 9.98 0 0 0 0.01 0.75 0 0.23 0.34 1.39 0 0 0 0

3.45 5.81 6.64 4.40 14.35 3.90 0.36 8.17 0 0.74 0 2.65 4.21 0.90 4.13 5.29 0 0 0 0.43 0

0

0.72 0.16 0 0 0 0 0 0 0 0 0 0.49 1.07

2.50 3.05 2.96 1.89 2.11 3.38 4.46 4.87 2.35 4.17 3.86 0 7.16

0 0 0 0 0 0 0 0 0 0 0 0

Hominoidea Gorilla gorilla beringei Gorilla gorilla gorilla Hylobates concolor Hylobates hoolock Hylobates klossi Hylobates lar carpenteri Hylobates pileatus Hylobates syndactylus syndactylus Pan paniscus Pan troglodytes schweinfurthii Pan troglodytes troglodytes Pongo pygmaeus abelii Pongo pygmaeus pygmaeus

.03 0 .05 0 .43 0 .44 0 0 0 0 0 0 0 .05 0 0 0 0 0

.03

Holotype Specimen KNM-MB 1, a partial mandible (Fig. 9D). Age

.02 0 0 0 0 0 0 0 0 .83 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 .02

Middle Miocene (19–12.5 Ma; Bishop, 1964; Feibel and Brown, 1991; Hill et al., 2002). Distribution Napak, Moroto, Uganda; Loperot, Maboko Island, Majiwa, Nachola, Nyakach, Ngorora, Ombo, Kenya. Diagnosis Dentition differs from that of other victoriapithecids by the following: smaller P4 relative to molar size; molar size gradients M1 < M2 > M3 and m1 < m2 < m3; upper molars and deciduous premolars wider than long; dP3 with very small hypocone, metacrista obliquely oriented and terminating in trigon basin, dP3 trigon continuous with distal shelf; variable development of bilophodonty on dp4; m1 square in occlusal outline and smaller relative to m2 and m3 than in other cercopithecoids; invariably complete distal lophids on molars, m3 hypoconulid positioned slightly buccally, shorter mesial shelf length relative to crown height (Fig. 9A–D). Cranially, Victoriapithecus differs from that of other cercopithecoids in having: a lower neurocranium relative to length and width; more airorhynchous hafting of the neurocranium and face, with less flexed basicranium and longer midcranial region as measured

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Maboko Island and a new species from Kipsaraman, Kenya and smaller than those of Prohylobates sp. from Buluk, Wadi Moghara and Gebel Zelten’’ (Pickford et al., 2003: 657). Despite the close agreement in size between the Moroto specimens and material of Victoriapithecus from Maboko, the Moroto specimens were attributed to Prohylobates because, at the time the Moroto material was described, no clear features were known to distinguish Prohylobates from Victoriapithecus, it was possible that the two genera were synonymous, and the name Prohylobates had priority. Prohylobates has now been shown to be distinct from Victoriapithecus, but the small sample sizes and fragmentary nature of both the Moghra and Moroto material means there is little comparable morphology available between the two collections. However, because the Moroto specimens are within the size and morphological range of Victoriapithecus, the Moroto material is attributed to that taxon. Noropithecus gen. nov. Etymology ‘‘Noro’’ means ‘‘monkeys’’ in Dassanatch, the local language in the area where the type species is from, and ‘‘pithecus’’ from the Greek pithekos (ape), a common suffix for primates. Diagnosis

Figure 9. (A) Victoriapithecus macinnesi, KNM-MB 29158, lateral, (B) medial, and (C) occlusal. (D) KNM-MB 1, V. macinnesi, type, lateral. Scale ¼ 1 cm. Photo by B.R.B.

from postglenoid process to M3; steep and linear facial profile; frontal trigon formed in part by the anterior convergence of temporal lines and presence of supraorbital costae; orbits taller than wide; orbits and zygomatics that are angled dorsally rather than perpendicularly relative to the Frankfurt plane, so that the superior rim of the orbit is posterior to its inferior rim; deep malar region of the zygomatic; shallow palate; inferior transverse torus is cercopithecine-like; mandibular coronoid process extends well above the apex of condylar process; with pronounced sagittal and nuchal crests. Postcranially, victoriapithecids are cercopithecine-like in having a humeral greater tubercle that extends above the head, retroflected entepicondyle and ulnar olecranon process; short and stout phalanges; restricted range of hallux abduction; small acetabulum and long ischial body (adapted from Benefit and McCrossin, 2002).

Differs from Prohylobates in having lower molars that are completely bilophodont; lower molar size gradient m1 < m2 < m3; m3 hypoconulid well developed. Differs from Victoriapithecus and all extant cercopithecoids in having a symphyseal region that is taller, and with a more vertically oriented inferior transverse torus, which results in a steeper symphyseal angle and less elongated symphysis. Further differs from other cercopithecoids in having more bunodont lower molar cusps; and greater degree of molar flare due to mesial and distal cusp tips being more closely approximated. Type species Noropithecus bulukensis sp. nov. Synonymy Prohylobates sp. indet. Leakey, 1985 Etymology For the site of ‘‘Buluk’’ in northern Kenya, where the type specimen was recovered.

Referred specimens

Holotype

Specimen UMP-MOR II 17’01, a right lower canine, UMP-MOR II 18’01, a right p3, and UMP-MOR II 25’01, a right p4. All likely belonging to a single individual, described, discussed, and figured in Pickford et al. (2003: Fig. 3), as Prohylobates macinnesi.

Specimen KNM-WS 12639, a right mandibular fragment preserving the inferior portion of the symphysis, canine alveolus, damaged crowns of p4-m1, and roots of p4 and m2 (Fig. 10A–C; Leakey, 1985: Fig. 2B).

Remarks

Referred material

Victoriapithecus is the best known member of the Victoriapithecidae, being represented by ca. 2500 specimens, including cranial and postcranial material (Benefit, 1987, 1993; Benefit and McCrossin, 2002). The three cercopithecoid teeth recovered from Moroto, dated to ca. 17.5 Ma (Pickford et al., 2003), have been described as ‘‘similar in size to those of Prohylobates macinnesi from

Fifteen specimens described in Leakey (1985) as Prohylobates sp. indet. These are: KNM-WS 122, a left mandibular fragment with m2–3; KNM-WS 123, a mandibular symphysis with roots, left i1-p4, right i1-c; KNM-WS 7659, a left m3; KNM-WS 12637, a right maxillary fragment with P4, half of M2, M3, roots of P3-M1; KNMWS 12638, a right mandibular fragment with m2–3, roots of c, p4,

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Figure 10. Noropithecus bulukensis. (A) KNM-WS 12369, type specimen, lateral. (B) KNM-WS 12369, medial. (C) KNM-WS 12638, occlusal. (D) KNM-WS 123, lateral. (E) KNM-WS 123, medial. Note the steeply vertical symphysis. Scale ¼ 1 cm. Photos A, B by J. Fleagle.

m3; KNM-WS 12640, a right mandibular fragment with m3; KNMWS 12641, a left mandibular fragment with broken m2; KNM-WS 12642, a right m3; KNM-WS 12646, a right m3, KNM-WS 12647, a right m3; KNM-WS 12648, a right M2; KNM-WS 12649, a right M1; KNM-WS 12650, a right mandibular fragment with m2; KNMWS 12651, a buccal half of left m2; KNM-WS 12652, a distal portion of left m3 crown.

to M2, such that the buccal aspect of M3 is positioned more lingually than that of M1; and right and left M3s converge more strongly on the sagittal plane than do M1–2. Age Early Miocene (>17.2 Ma; McDougall and Watkins, 1985). Distribution

Diagnosis Buluk, Kenya. Differs from other species of Noropithecus in having a higher planum alveolare and higher genial pit above the inferior border of the symphysis (Table 6, Fig. 10); multiple mental foramina are common; larger tooth sizes than cercopithecoid species from Kipsaraman (cf. N. kipsaramanensis, see below) and Nabwal (cf. N. fleaglei) (Tables 2, 3; see also Pickford and Kunimatsu, 2005). Also differs from Victoriapithecus and other cercopithecoids in having a more abrupt change in the long axis of the upper molar row distal

Description Specimen KNM-WS 12639 is designated as the holotype because it is the specimen that best preserves the symphyseal region of the mandible, the morphology of which distinguishes Noropithecus from Victoriapithecus. Symphyses of the Buluk monkeys (e.g., KNMWS 12639 [Fig. 10A, B], KNM-WS 123 [Fig. 10D, E]) differ from those

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Table 6 Symphyseal measurements of victoriapithecid mandibles. Specimen V. macinnesi KNM-MB 11676 KNM-MB18928 KNM-MB 18993 KNM-MB 21027 KNM-MB 21035 KNM-MB 31279 KNM-MB 31282 KNM-MB 31283 KNM-MB 11951

Sex

Sym height

M

21.5

F M M M M

15

20.2 17.5 22.1

Sym A-P thickness

14.5 15.5 15.6 17.5 13.2þ

Sup Tor H below alveolus

6.2 6.85 7.9 12.35 10.04

Sup Tor thickness

11.34

17.8 17.3

11.55

N. bulukensis KNM-WS 123 KNM-WS 12639

24.6 26.9

20.5

cf. N. kipsaramanensis BAR 219’02

19.42

13.88

9 10.7

13.9

Gen pit H below alveolus

Gen pit H above inf border

Sym angle

12.4 9.25 9.1

3.8 4.6

47 36

11.6 16.4 13.1 10.8 14.05

6.6 7.3 8.55

45

10.55 15.5

10.74 11.76

12.35a

40 48.5 52

7.67a

Measurements by B.R.B. Sym height ¼ symphyseal height; Sym A-P thickness ¼ symphyseal thickness measured anterior-posterior; Sup Tor H below alveolus ¼ height of the superior torus below the alveolus; Sup Tor thickness ¼ thickness of the superior torus; Gen pit H below alveolus ¼ distance from the genial pit to incisor alveoli; Gen pit H above inf border ¼ distance from the genial pit to the inferior border of the symphysis; Sym angle ¼ degree of anterior inclination of the mandibular symphysis from the perpendicular. a Indicates estimated due to large size of genial pit.

of V. macinnesi (Fig. 10), but are similar to that of the Kipsaraman monkeys (Fig. 11A–C; see also Pickford and Kunimatsu, 2005), in having an inferior transverse torus that is steeply inclined below the genial pit. The configuration of the symphyseal region in the Buluk mandibles differs from that seen in many colobine monkeys, where the inferior torus bends anteriorly toward the inferior border, and differs from that seen in many cercopithecines and Victoriapithecus, where a simian shelf is present due to a more continuously posterior extension of the torus inferiorly (Fig. 12). Mandibles KNM-WS 123 and KNM-WS 12639 differ from the Kipsaraman mandible, CMK-BAR 219’02, and from Victoriapithecus, in having a higher position of the genial pit (Table 5).

longer tenable, primarily because the Kipsaraman lower molars are fully bilophodont. The Kipsaraman cercopithecoid is here provisionally attributed to the genus Noropithecus because the type mandible (CMK-BAR 219’02) shares with N. bulukensis the presence of a steep vertical symphysis. The steep vertical symphysis in N. bulukensis and cf. N. kipsaramanensis is distinct from the sloping, inferior transverse torus observed among cercopithecines and Victoriapithecus. However, the mandible of cf. N. kipsaramanensis differs from that of N. bulukensis in being shallower and more robust, and in having a lower position of the genial pit relative to symphyseal height. cf. Noropithecus fleaglei sp. nov.

cf. Noropithecus Included species: cf. Noropithecus kipsaramanensis (Pickford and Kunimatsu, 2005); cf. Noropithecus fleaglei sp. nov. cf. Noropithecis kipsaramanensis Synonymy Prohylobates kipsaramanensis (Pickford and Kunimatsu, 2005). Diagnosis Differs from P. tandyi in having complete lower molar bilophodonty; differs from V. macinnesi but resembles N. bulukensis in having a more vertical mandibular symphysis; differs from N. bulukensis in having a shallower and broader mandible; lower position of the genial pit relative to symphyseal height; and smaller cheek teeth. Holotype Mandible CMK-BAR 219 ’02, partial right mandibular corpus, symphyseal region, left mandibular corpus, and left m2 (Fig. 11A–C; Pickford and Kunimatsu, 2005: Fig. 19). Referred material Eighty-eight specimens described in Pickford and Kunimatsu (2005). Age Middle Miocene (14.5 Ma; Pickford, 1981). Distribution Kipsaraman, Kenya. Remarks Material of N. kipsaramanensis was originally described as Prohylobates kipsaramanensis, when the manner in which Prohylobates was distinct from other victoriapithecids had not yet been elucidated (Leakey, 1985; Pickford and Kunimatsu, 2005). However, the assignment of the Kipsaraman material to Prohylobates is no

Holotype Specimen KNM-NL 30949, a right partial mandible with unworn crowns of m2 and m3, roots of p3-m1, the lateral portion of the symphyseal region is preserved, and the mandible has an intact corpus below p4-m3, but is broken behind m3 so that only the anterior part of the ramus is present (Fig. 11D–F). Etymology For Dr. John Fleagle, whose team recovered the type specimen, and for his contributions to primatology. Diagnosis Differs from P. tandyi in having more complete lower molar bilophodonty, and a larger m3 with a well developed hypoconulid. Differs from Z. simonsi in having a mandible and teeth of much smaller size, and m2 longer than broad. Differs from V. macinnesi but resembles Noropithecus in having closer proximity of molar cusp tips, stronger molar flare, and more bunodont cusps. Differs from Prohylobates, Noropithecus, the gen. indet mogharensis material, and most specimens of V. macinnesi in having a mandibular corpus that is broad over its superior threefourths, but which thins dramatically above the inferior border creating a small indentation for passage of the geniohyoid (Fig. 11F). Age Early Miocene (<17.2 Ma; Fleagle et al., 1997). Distribution Nabwal, northern Kenya. Description Metrically, the proportions of the Nabwal mandible fall within the range observed for Victoriapithecus (Tables 2–4), but the Nabwal specimen has a broader mandibular corpus relative to height than do specimens of Prohylobates, the gen. indet. mogharensis material, or the Kipsaraman cercopithecoids (Table 4, Fig. 6). Overall, the Nabwal specimen exhibits a combination of features

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Figure 11. (A) BAR 219’02, cf. N. kipsaramanensis, lateral, (B) occlusal, and (C) medial. (D) Cast of KNM-NL 30949, cf. N. fleaglei, lateral, (E) occlusal, and (F) medial. (G) Z. simonsi, AMNH 11768, right ramus, lateral, and (H) occlusal. Scale ¼ 1 cm. Photos of BAR 219’02 by M. Pickford, photos of AMNH 11768 by E. Delson.

not seen together in any other species of victoriapithecid. However, an individual match for any one of the features observed in the Nabwal specimen, including the broad mandibular corpus with a well-defined passage for the geniohyoid, may occasionally be found among the larger V. macinnesi sample (e.g., KNM-MB 21027). Although metrically the Nabwal cercopithecoid falls within the range for Victoriapithecus, the Nabwal species is provisionally

attributed to Noropithecus based on occlusal resemblances to N. bulukensis. Remarks Recovery of a single partial mandible from Nabwal, northern Kenya, was announced by Fleagle et al. (1997). Nabwal is geographically close to Buluk, but is stratigraphically below the basalt that forms the base of the Buluk sequence. The significance of the age and stratigraphic differences between Nabwal and Buluk is

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Figure 12. Comparative cross-sections of the mandibular symphysis in (A) cercopithecines (e.g., Chlorocebus tantalus), (B) colobines (e.g., Procolobus verus), (C) V. macinnesi, photo and drawing, and (D) N. bulukensis, photo and drawing. Note the steep inferior torus in N. bulukensis. G ¼ genioglossal pit, ST ¼ superior torus, IT ¼ inferior torus. Figure based on Fleagle (1999); laser scans of C. tantalus and P. verus courtesy of Jennifer St. Germain and Eric Delson.

difficult to know, but the two sites share an otherwise similar faunal array. Discussion The monophyly of Cercopithecidae (Colobinae þ Cercopithecinae) is supported by both molecular (e.g., Xing et al., 2005) and morphological (e.g., Strasser and Delson, 1987) evidence, and a number of important anatomical features have been identified among colobines and cercopithecines that are absent among victoriapithecids. These include: a taller, wider, and more rounded neurocranium; increased klinorhinchy; orbits wider than tall; a less obliquely oriented p4; absence of a crista obliqua; consistent mesial and distal lophids on dp4M2; presence of distal transverse lophs on dP3-M3; absence of

hypoconulids; and presence of a well developed hypoconid and entoconid on dp3 (Benefit, 1993, 1999; Benefit and McCrossin, 1993, 1997). The systematic relationships among early and middle Miocene fossil cercopithecoids, and between stem cercopithecoid and crown forms are not as clear. Early and middle Miocene catarrhine monkeys can be distinguished from one another on the basis of degree of bilophodonty, relative molar size, symphyseal construction, and mandibular shape. The distribution of these characteristics indicate that, at present, as many as seven species can be recognized, in a minimum of four but perhaps as many as seven genera: Prohylobates tandyi, Zaltanpithecus simonsi, Victoriapithecus macinnesi, Noropithecus bulukensis, cf. N. kipsarmanensis, cf. N. fleaglei, and gen. indet. mogharensis (Table 7). In addition,

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Table 7 Victoriapithecid taxa. Taxon

N

Localities

Prohylobates tandyi Gen. indet. mogharensis Zaltanpithecus simonsi Victoriapithecus macinnesi

2 4 1 2500

Noropithecus bulukensis cf. N. kipsaramanensis cf. N. fleaglei

16 89 1

Wadi Moghra, Egypt Wadi Moghra, Egypt Jabal Zaltan, Libya Maboko Island, Ombo, Loperot, Nachola, Ngorora (Kenya), Napak, Moroto (Uganda) Buluk, Kenya Kipsaraman, Kenya Nabwal, Kenya

each of these genera is highly distinct relative to the others. Prohylobates tandyi shows incomplete bilophodonty in its lower molar series, and, because of this, P. tandyi likely represents the most morphologically primitive cercopithecoid known. Although incomplete bilophodonty has been documented previously among victoriapithecids in the upper molar series and on dp4 (e.g., Benefit, 1987; Benefit and McCrossin, 2002), P. tandyi is currently the only known species that is not fully bilophodont in its lower molar series. Little information is available about Z. simonsi because the taxon is represented by only a single mandibular fragment, but the much larger size and divergent morphology of Z. simonsi (e.g., bifurcated molar roots) makes Z. simonsi a clear outlier relative to other victoriapithecids. Noropithecus bulukensis shares a number of molar features with other victoriapithecids, including strong molar buccal flare and variable occurrence of a crista obliqua, but N. bulukensis also exhibits some features that appear to be unique among victoriapithecids, including a steeply inclined symphyseal region. Members of V. macinnesi exhibit a unique mosaic of cercopithecoid traits, some colobine-like and others more cercopithecine-like (reviewed in Benefit and McCrossin, 2002). Many problems interpreting the systematic relationships of stem cercopithecoids result from the fragmentary representation of all species except V. macinnesi. However, an additional confounding factor is that Victoriapithecidae may be paraphyletic, with complex relationships among fossil stem forms, and between stem and crown forms. The concept of paraphyly in Victoriapithecidae has been discussed previously, particularly with regard to a possible relationship between Victoriapithecus and cercopithecines (Leakey et al., 2003; Cooke, 2006). However, the fact that Prohylobates lacks full development of the key adaptive innovation uniting all other cercopithecoids strongly suggests that Victoriapithecidae is paraphyletic, and that Prohylobates may represent the sister taxon to other victoriapithecids þ cercopithecids. In fact, given the distinctiveness of Prohylobates, Zaltanpithecus, Noropithecus, and Victoriapithecus, one conclusion may be that the Victoriapithecidae encompasses a number of different stem cercopithecoids occupying varying degrees of relationship to one another, and perhaps to crown cercopithecids. Such a scenario of rampant paraphyly among the Victoriapithecidae would be in contrast to the more traditional view of the family, namely, that Victoriapithecidae represents a more cohesive archaic family of cercopithecoids whose members are united by the retention of features present in more basal catarrhines but absent in derived cercopithecoids, and that the Victoriapithecidae occupies a sister-group relationship to Cercopithecidae. Proposed taxonomy Although a case can be made that the Victoriapithecidae is paraphyletic, at present we prefer to maintain Victoriapithecidae as a distinct family of archaic cercopithecoids for the following five

reasons. First, colobines and cercopithecines are united by a number of morphological features that are absent among victoriapithecids. Members of the two extant subfamilies presumably inherited these features from a common ancestor, which has not been identified among known fossil cercopithecoids. Second, many of the features cited as shared between Victoriapithecus and cercopithecines are primitive for cercopithecoids, and so would not be indicative of a special relationship between the two taxa. Instead, it may be that cercopithecines more closely approximate the primitive condition for modern Old World monkeys than do colobines. Third, if Victoriapithecus and other early cercopithecoids with full lower molar bilophodonty (i.e., all except Prohylobates) were placed in the Cercopithecidae, a new family would have to be erected for Prohylobates (‘‘Prohylobatidae’’), and this new taxon would be based on a primitive feature: lack of lower molar bilophodonty. Such an arrangement does not resolve the problem of having to recognize an archaic family of cercopithecoids defined on the basis of one or more primitive features. Fourth, specimens of Noropithecus share a number of molar features with other victoriapithecids, but Noropithecus also exhibits some features that appear to be unique among early cercopithecoids. One possible solution would be to erect a new family for Noropithecus, so that it occupies a sister group relationship to Victoriapithecus þ cercopithecids, and to have Prohylobates as the sister group to that, but such a successive series of monotypic sister taxa, from Prohylobates to Noropithecus to Victoriapithecus þ cercopithecines, is considered undesirable because it contributes to instability in Cercopithecoidea. Fifth, although it is distinctly possible that Victoriapithecidae constitutes a paraphyletic group, the family may in fact be monophyletic, much as modern platyrrhines form a monophyletic group (based on molecular evidence, e.g., Singer et al., 2002; Ray et al., 2005), although no morphological synapomorphies supporting their monophyly have been identified. Such a possibility may not be cladistically satisfying, but it may represent biological reality. Better resolution of the systematics of the Victoriapithecidae awaits future discovery of more fossil evidence of Prohylobates, Zaltanpithecus, and Noropithecus, which will demonstrate whether or not these catarrhine monkeys are similar to Victoriapithecus cranially and postcranially. Acknowledgements We thank the Government of Egypt for permission to work at Wadi Moghra, and the Director General, Dr. Mohamed Ezzet ElHakim, and staff in Vertebrate Paleontology at the Cairo Geological Museum: G. Medhat, S. Abdel Ghany, Magdy Zakaria, Magdi Gamil, and Afifi Abdel Ghafar, for help in the Cairo collections. We also thank the Office of the President of Kenya, and the Director General of Kenya National Museums, Dr. Idle Farah, for permission to work at Buluk, and Dr. Emma Mbua, Mary Muungu, and the staff in Paleontology at Kenya National Museums for access to material in their care. Dr. Gregg Gunnell recovered specimen CUWM 06–31, and we thank Drs. Gregg Gunnell, John Fleagle, and William Hylander for discussion as well as for help with casts and figures. Dr. Eric Delson provided photographs of P. simonsi, and scan-based cross sections of modern cercopithecoids. R. Usery (Duke Photography) and Dr. Russell Ciochon took the photographs of the Moghra specimens, and Dr. Martin Pickford provided photographs of the Kipsaraman mandible. Walter Joyce at the Yale Peabody Museum located the cast of CGM 30937 (YPM 57165). A special debt of gratitude is owed to Dr. Eric Delson, Dr. Terry Harrison, an anonymous reviewer, and the Editor, Dr. Bill Kimbel, whose comments greatly improved the manuscript. Research support was provided by the National Science Foundation; the Leakey Foundation; Social, Behavioral & Economic Research Fund, Wake Forest University; and the Archie Fund, Wake Forest University. Duke Lemur Center Publication 1131.

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