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Early Primate Evolution in Afro-Arabia

ARTICLE in EVOLUTIONARY ANTHROPOLOGY ISSUES NEWS AND REVIEWS · NOVEMBER 2012

Impact Factor: 3.59 · DOI: 10.1002/evan.21335 · Source: PubMed

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Erik Seiffert

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Early Primate Evolution in Afro-ArabiaERIK R. SEIFFERT

The peculiar mammalian fauna that inhabited Afro-Arabia during the Paleo-

gene first came to the attention of the scientific community in the early part of

the twentieth century, when Andrews1 and Schlosser2 published their landmark

descriptions of fossil mammals from the Fayum Depression in northern Egypt.

Their studies revealed a highly endemic assemblage of land mammals that

included the first known Paleogene records of hyraxes, proboscideans, and

anthropoid primates, but which lacked ancestors of many iconic mammalian lin-

eages that are found in Africa today, such as rhinos, zebras, bovids, giraffes,

and cats. Over the course of the last century, the Afro-Arabian Paleogene hasyielded fossil remains of several other endemic mammalian lineages,3 as well as

a diversity of prosimian primates,4 but we are only just beginning to understand

how the continent’s faunal composition came to be, through ancient processes

such as the movement of tectonic plates, changes in climate and sea level, and

early phylogenetic splits among the major groups of placental mammals. These

processes, in turn, made possible chance dispersal events that were critical in

determining the competitive landscape—and, indeed, the survival—of our ear-

liest anthropoid ancestors. Newly discovered fossils indicate that the persistence

and later diversification of Anthropoidea was not an inevitable result of the

clade’s competitive isolation or adaptive superiority, as has often been assumed,

but rather was as much due to the combined influences of serendipitous geo-

graphic conditions, global cooling, and competition with a group of distantly

related extinct strepsirrhines with anthropoid-like adaptations known as adapi-

forms. Many of the important details of this story would not be known, andcould never have been predicted, without the fossil evidence that has recently

been unearthed by field paleontologists.

SETTING THE STAGE: ‘‘ISLAND

AFRICA’’ AND AFROTHERIA

Combined geophysical and paleo-biogeographic evidence indicatesthat the African and Arabian plates(Afro-Arabia) together formed a sin-gle landmass that had no permanent

connections to other continents from120 to 20 Ma; that is, through the

later part of the Early Cretaceous,the entire Late Cretaceous and Paleo-gene, and part of the early Miocene.5

Despite Madagascar’s proximity tothe southeast, Afro-Arabia has notbeen directly connected to thatisland since the Jurassic.6 During theLate Cretaceous, Madagascar had

close geographic and biogeographiclinks to the Indian subcontinent,7

but together the two bodies hadalready become isolated from otherGondwanan continents.6 India wouldlater move north to collide with Asia,with overland vertebrate dispersalcorridors likely first appearing in theearly Eocene.8 Afro-Arabia’s last con-nection before isolation was withSouth America, at 120 Ma, and itsslow northward drift finally termi-

nated when it collided with south-west Asia, permanently closing off the Tethys Sea, which previously hadseparated Afro-Arabia from Eurasia.9

The timing and nature of this colli-sion is complex and currently a mat-ter of debate. The process probablyinitiated in the later Paleogene, but

the first major pulse of terrestrial vertebrate faunal exchange, which isassumed to reflect an ephemeral landconnection between Arabia andsouthwest Asia, is not known to haveoccurred until 20 Ma.10 Faunalexchange continued to be stronglyfiltered well into the Miocene, forinstance by a major marine transgres-sion in the early middle Miocene.9

Very little is known about theterrestrial vertebrate fauna thatinhabited Afro-Arabia during the LateCretaceous and early Paleocene,

between 95 and 60 Ma. The fewfossils that have been discovered fromLate Cretaceous sites show that Afro-Arabia was home to an archosaurfauna that included various crocodyli-forms and both predatory theropodand herbivorous sauropod dinosaurs,7

but with the exception of a singlecaudal vertebra dating to about 95Ma,11 no mammals are known.Several mammals have been found inlater Cretaceous beds on other Gond-wanan land masses (Madagascar,South America, and India) but almost

all of these species are unequivocallyderived from archaic, non-therianclades.12 The only clear records of Cretaceous-aged placental mammalsin Gondwana are from India, andthese taxa, of which Deccanolestes isbest known, fall outside of the placen-tal crown clade based on availableevidence.13 Early crown therians andthe stem lineage of Placentaliaapparently diversified largely in theCretaceous of Laurasia (Fig. 1).14

Erik Seiffert is Associate Professor in theDepartment of Anatomical Sciences atStony Brook University. Email: [email protected]

VVC 2012 Wiley Periodicals, Inc.DOI 10.1002/evan.21335Published online in Wiley Online Library(wileyonlinelibrary.com).

ARTICLE

Evolutionary Anthropology 21:239–253 (2012)


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Given that so little paleontologicalwork has been undertaken in thelater Cretaceous of Afro-Arabia, thecurrent lack of mammalian fossilsfrom this time and place is more

likely to be an artifact of inadequatepaleontological sampling than a trueabsence. In fact, the now well-established molecular phylogeny of placental mammals,15,16 when inter-preted within the context of availablepaleontological evidence, predictsthat the morphologically diversesupraordinal clade Afrotheria (whichcontains elephants, sea cows,hyraxes, aardvarks, sengis or ele-phant-shrews, golden moles, andtenrecs) originated in Afro-Arabiaduring the later part of the Creta-

ceous (Fig. 1).17,18

This radical reor-ganization of mammalian phylogenyhas been well-established for justover a decade, and is only now gain-ing broad acceptance.3 The existenceof an ancient, endemic Afro-Arabianclade of placentals is a critically im-portant piece of this biogeographicpuzzle, which was not available toearlier students of mammalian evolu-tion, but now provides an elegant ex-planation of the odd Fayum faunas

that were first encountered byAndrews1 and Schlosser2: the diverseafrotherian fauna was the result of aLate Cretaceous origin in Afro-Arabiaand tens of millions of years of evo-

lution in isolation, while the pres-ence of all other non-afrotherian pla-centals had to be the result of morerecent overwater dispersals, mostlikely from Europe or Asia.

THE OLDEST AFRO-ARABIAN

PRIMATES AND OTHER EARLY

CENOZOIC IMMIGRANTS

Primates are not members of Afro-theria, but rather are most closelyrelated to colugos or ‘‘flying lemurs’’

(order Dermoptera)16,19,20

and, moredistantly, tree-shrews (order Scan-dentia), within a clade called Euarch-onta (Fig. 1).15,18 Euarchonta andthe larger clade Euarchontoglires,which includes the more distantlyrelated rodents (order Rodentia) andrabbits and pikas (order Lagomor-pha), is almost certainly of Laurasianorigin, based on each order’s firstappearance in the fossil record(Fig. 1).17 The oldest possible stem

primate is earliest Paleocene Purga-torius from North America,21 butdefinitive members of the primatecrown clade (that is, the clade con-taining all extant primates and their

last common ancestor) do not appearin the fossil record until near thePaleocene-Eocene boundary, 56Ma. By that time, cladistic stemstrepsirrhines (basal adapiforms)and stem or crown haplorhines (ba-sal omomyiforms) are already detect-able on the northern continents,22–27

indicating a more ancient origin forcrown primates in the Paleocene, if not earlier. Recent work refining mo-lecular divergence dates for primateclades suggests that the last commonancestor of crown primates probably

lived near the boundary between theCretaceous and the Paleogene, about66 Ma or slightly earlier.28,29 If thisis correct, the first 10 Ma of crownprimate evolution are currently miss-ing from the fossil record. Afro-Ara-bia would have been moving awayfrom the peak of its geographic isola-tion during this interval (Fig. 1), butstill would have been completely iso-lated, both by its geographic positionand a relatively high (but falling)

Figure 1. Phylogenetic relationships, biogeography, and divergence times of major therian mammal clades. Relationships and diver-

gence times based on dos Reis and colleagues29; inferred geographic origin for each order is based on the first appearances of either

stem or crown members in the fossil record. The geographic origin of stem Xenarthra and stem Afrotheria is here considered to be

uncertain, but the stem lineages of Placentalia, Boreoeutheria, Euarchontoglires, and Laurasiatheria are considered to be Laurasian.

Inset, global paleobiogeography at the Cretaceous-Cenozoic boundary (near the estimated time of origin of crown primates28), modi-

fied from a map provided by Ron Blakey (Colorado Plateau Geosystems, Inc.; cpgeosystems.com/paleomaps.html). [Color figure can

be viewed in the online issue, which is available at wileyonlinelibrary.com.]

240 Erik R. Seiffert ARTICLE


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global sea level.30 At the close of theCretaceous and through the earlypart of the Paleogene, Afro-Arabiawould have been closer to southwestEurope (the Iberian Peninsula andnearby islands) than to Asia (Fig. 1).5

Despite Primates’ probable Laura-sian origin, by the close of the Eocene(34 Ma) a remarkable array of primategroups had made appearances on the

isolated Afro-Arabian landmass4,31

:azibiids, djebelemurines, basal crownstrepsirrhines and definitive lorisi-forms, plesiopithecids, caenopithecineadapiforms, afrotarsiids, parapithe-coids, proteopithecids, catarrhines,and two particularly enigmatic prima-tes called Altiatlasius32 and Nosmips.33

The biogeographic origins of this diversity can only be understood byplacing these primate lineages in abroader phylogenetic context.

The oldest euarchontan from Afro-Arabia is latest Paleocene Altiatlasiusfrom Morocco.32 Given our currentunderstanding of early primate evo-

lution, Altiatlasius is enigmatic, dueto its antiquity, geographic place-ment, and fragmentary nature (beingknown from only ten isolated teethand a mandibular fragment holdinga second lower molar). Phylogenetic

analyses have placed Altiatlasiusas either a basal stem anthro-poid,22,24,25,28,34–36 a tarsiiform,36 abasal haplorhine of uncertain place-ment relative to anthropoids andtarsiiforms,24,34 or even as a plesia-dapiform.37 It has been argued that Altiatlasius suite of upper and lowermolar characters is more similar tothat of later primitive anthropoidsthan what is seen in the basal omo-myiforms and adapiforms that are

known from the early Eocene onnorthern continents,38–40 but its fewanthropoid-like dental features, suchas relatively well-developed lingual

cingula on the anterior uppermolars, have evolved convergently innon-anthropoids several times overthe course of primate evolution.Unfortunately, in light of this, muchmore information is needed to estab-

lish Altiatlasius’ affinities with anyconfidence.

On northern continents, the ear-liest Eocene was marked by the firstappearances of crown primates andtheir rapid intercontinental dispersalat high latitudes, evidently facilitatedby an intense episode of globalwarming that has been called thePaleocene-Eocene Thermal Maxi-mum (PETM).41 Terrestrial mamma-lian response to the PETM has now

Figure 2. Temporal distribution of primates from the Paleogene of Afro-Arabia. Abbreviations: Azib., Azibiidae; Galag., Galagidae; indet.,

indeterminate; Proteo., Proteopithecidae. Possible members of the strepsirrhine crown group are placed under the category ‘‘crown?’’.

Question mark (?) for Moeripithecus reflects its uncertain placement in the Fayum succession; that for Propliopithecus from Taqah, Omanreflects the unresolved generic placement of that species. See Fig. 3 for a map showing the geographic placement of localaties.

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been documented in Asia, Europe,and particularly North America, butpractically nothing is known aboutthis time period in Afro-Arabiabecause few mammal sites of earliestEocene age are known. Primates

have not been recovered at any of the early Eocene sites in Africa (forexample, El Kohol in Algeria andOuled Abdoun in Morocco). Theselocalities also provide no unambigu-ous evidence of immigration of non-

primate mammals from northernland masses (marsupials andadapisoriculids being possible excep-tions5), seemingly attesting to Afro-Arabia’s continued isolation fromEurope and Asia by the Tethys Sea.

Definitive fossil evidence for filteredfaunal exchange does not occur inthe Afro-Arabian record for anotherfive million years, near the boundarybetween the early and middle Eocenestages (49 Ma) (Figs. 2, 3, and 4).Important sites of this approximateage include Chambi in Tunisia andGlib Zegdou in Algeria, both of which have yielded remains of pri-mates,35,42–44 as well as Afro-Arabia’soldest rodents, the Zegdoumyidae.45

The latter are undoubted immigrantsfrom Eurasia that ultimately gave

rise to the Anomaluroidea, Africa’sextant scaly-tailed flying squirrels(Anomaluridae) and springhares

(Pedetidae).45,46

The early-to-middle Eocene prima-tes from northwest Africa haveperplexed students of early primateevolution for decades, but newdiscoveries have finally helped toclarify their identities. The first pri-mate recovered from Glib Zegdouwas Azibius trerki, which Sudredescribed in 1975 on the basis of apartial lower jaw with three teeth.47

Before the discovery of more com-plete remains of Azibius reported in2009, this odd species had beeninterpreted as a plesiadapiform, anadapiform, or even a non-primatemammal.35 Two isolated teeth, anM2 and an M3, of a smaller primatefrom Glib Zegdou, Algeripithecusminutus, were reported in 1992 byGodinot and Mahboubi.43 Morpho-

Figure 3. Geographic distribution of major primate-bearing fossil localities from the Paleo-

gene of Afro-Arabia.

Figure 4. Mammalian dispersals into and out of Afro-Arabia during the Eocene, imposed on a middle Eocene (Lutetian) paleogeo-

graphic map modified from that in Gheerbrant and Rage5 (which followed that of Dercourt and coworkers99). [Color figure can be

viewed in the online issue, which is available at wileyonlinelibrary.com.]



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logically similar but larger upper andlower molars were later reported bythe same authors48 and formed thehypodigm for another new genusand species, Tabelia hammadae,which, like Algeripithecus, was inter-

preted as a primitive anthropoid.The anthropoid identity of Algeripi-thecus and/or Tabelia would come tobe widely accepted by a number of other authorities24,39,40,49–53 and, inthe case of Algeripithecus, supportedby phylogenetic analysis.26 The sup-posed presence of primitive anthro-poids at such an ancient horizon inAfro-Arabia had a major influence onthe anthropoid origins debate forabout 15 years.

New material of Algeripithecus and Azibius described by Tabuce and co-

workers35

has surprisingly revealedthat Algeripithecus is, however, notan anthropoid at all, but rather is

closely related to Azibius, and thattogether these ‘‘azibiids’’ are likelyallied with crown (‘‘toothcombed’’)strepsirrhines (lemurs, lorises, andgalagos). With upper teeth of Azibiusnow available for comparison, it isalso clear that ‘‘Tabelia’’ is in fact Azibius, and that the hypodigm of another genus from Glib Zegdou,‘‘ Dralestes,’’ is composed of speci-mens that are attributable to both

Algeripithecus and Azibius.35

In onefell swoop, these discoveries removedthe only compelling records of Anthropoidea and Plesiadapiformesfrom this period in Afro-Arabia, andrevealed that primate taxonomicdiversity at Glib Zegdou was actuallymuch lower than previously thought,with all taxa being members of one

very strange primate family. Withthe benefit of hindsight, it is nowonder that isolated teeth of Algeripi-thecus, Azibius, ‘‘ Dralestes,’’ and‘‘Tabelia’’ engendered so much confu-

sion – despite their great antiquity,aziibids are highly specialized, andindeed are some of the more bizarreprimates known from the Eocene of any continent. They combine multi-cusped and superficially anthropoid-like upper molars with elongate,strepsirrhine-like lower molars, and

have long, serrated upper and lowerpremolar teeth that have large acces-sory cusps of uncertain homology.Tabuce and colleagues’35 identifica-

tion of azibiids as stem strepsir-rhines has since gained additionalsupport from the recovery of azibiidastragali that exhibit probable strep-sirrhine synapomorphies.42

DJEBELEMURINES AND THE ORIGIN

OF CROWN STREPSIRRHINES

The primate fauna from theroughly contemporaneous Chambilocality in Tunisia includes threeprimates: the tiny species Djebelemur martinezi, known from a mandiblewith P3-M3 and an isolated lowercanine54; a small unnamed azibiid,known from isolated upper molars,that is similar to and possibly conge-neric with Algeripithecus55; and a

much larger adapiform representedby two lower molars.56 Djebelemur was described as a member of theadapiform subfamily Cercamonii-nae,54 a potentially paraphyleticgroup know n largely from theEocene of Europe, but soon there-after was interpreted as a possiblebasal anthropoid38 or as a cercamo-niine that ‘‘may lie very near the pro-simian-anthropoidean transition.’’53

The phylogenetic analysis of Seiffert,Simons, and Attia57 later placed

Djebelemur not as an anthropoid or

cercamoniine, but as an advancedstem strepsirrhine, more closelyrelated to ‘‘toothcombed’’ strepsir-rhines than any adapiforms fromnorthern continents. This relation-ship is supported by a series of derived features of the lower postca-nine teeth that Djebelemur shareswith other advanced strepsirrhinesknown from younger sites in Afro-Arabia, but Djebelemur presumablyfalls outside of the strepsirrhinecrown group because it lacked atoothcomb. Godinot4,55 has since

accepted and discussed this scenarioin greater detail, and formally pro-posed that Djebelemur and itsyounger Afro-Arabian relatives bereferred to as ‘‘djebelemurines.’’

Key to the recognition of Djebele-mur as an advanced stem strepsir-rhine was the recovery of the firstdefinitive Paleogene toothcombedstrepsirrhines, Karanisia clarki andSaharagalago misrensis, at a younger(37 Ma, earliest late Eocene) locality

in the Fayum Depression of Egypt in2001.57 These discoveries marked amajor breakthrough for the study of strepsirrhine evolution because fossillorisids and galagids had long beenknown from early Miocene (< 20

Ma) sites in East Africa,

58

suggestinga much more ancient diversificationof lorisiforms in Afro-Arabia. Myste-riously, however, older and moreprimitive forms had never beenfound. The absence of crown strep-sirrhines in the Paleogene defied ex-planation, particularly given that thelate Eocene/early Oligocene Fayumsites had been worked intensively fordecades and had otherwise produceda diverse primate fauna thatincluded both large and small spe-cies. In the absence of a better expla-

nation, this odd pattern led some tosuggest that crown strepsirrhinesmight have originated in Asia andonly later dispersed to Afro-Arabia.59

Karanisia and Saharagalago wereinterpreted, respectively, as a crownlorisid and a stem galagid—identifi-cations that required lorises and gal-agos to have already diverged by themiddle Eocene; the lemuriform-lori-siform split must have been mucholder.57 More recent phylogeneticanalyses incorporating a larger num-ber of taxa and characters have

called into question the initial identi-fication of Karanisia as a crown lori-sid and generally place the genus ina more basal position as either astem lorisiform or a stem lemuri-form.

Saharagalago is still known onlyfrom one upper molar and one lowermolar, but the suite of upper molarfeatures that it shares with Miocene-to-Recent galagos (notably a deepnotch in the distal margin of thetooth and a large, distolingually pro-truding lobe for the hypocone) is

unique among primates. The galagidrelationship that was proposed forSaharagalago has since gained sup-port from the discovery of morecomplete remains of a younger ge-nus, Wadilemur , which is knownfrom a 34 Ma Fayum site called Lo-cality 41 (L-41) (Fig. 5E). Like Djebe-lemur , Wadilemur was originallyidentified as a cercamoniine adapi-form based on the morphology of itsP3-M3,

60 but was later found to have



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a large and anteriorly protruding P2crown as in many toothcombed pri-mates. In addition, Wadilemur isnow known to have had galagid-likemorphology of the upper molars and

proximal femur.27

Like Saharagalago,Wadilemur appears to be a stem gal-agid,4,27 but is situated closer to thegalagid crown group than that taxonin phylogenetic analyses, which isconsistent with its younger age.

Three other tiny primate species,one from the latest Eocene of Egypt(‘‘ Anchomomys’’ milleri) and twofrom the early Oligocene of Oman(Omanodon minor and Shizarodon dhofarensis) were, like Djebelemur

and Wadilemur , initially identified asprobable cercamoniine adapiforms,specifically aligned with a Europeangroup called anchomomyins, basedon very limited material.60,61 In light

of what has recently been learnedabout early strepsirrhine evolution inAfro-Arabia, it now seems that thesespecies are more likely to be djebele-murines than anchomomyin cerca-moniines. The lower molars of djebe-lemurines differ from those of anchomomyins in very subtle ways,but there are obvious differences inthe antemolar teeth. As in tooth-combed strepsirrhines, ‘‘ A.’’ millerihas three rather than four premolars,

the second premolar is single-rooted,and the anterior premolar crownsproject anteriorly. The lower canineof ‘‘ A.’’ milleri is particularly interest-ing in also being relatively procum-bent, mesiodistally elongate, and

blade-like. It appears to represent anintermediate morphological condi-tion between the more upright lowercanine of typical adapiforms and thegreatly procumbent and elongatecanines of crown strepsirrhines. Aclade containing ‘‘ A.’’ milleri and Dje-belemur (that is, a monophyletic Dje-belemurinae) was first recovered bySeiffert, Simons, and Attia’s phyloge-netic analysis in 200357 and hassince been found in some,27 but notall,25,36 subsequent analyses of anexpanded dataset.

It remains to be determinedwhether a clade including djebele-murines and crown strepsirrhines is

in fact nested within a Europeanradiation of anchomomyin adapi-forms. Several recent phylogeneticanalyses have recovered such aresult.25,28,35,36 This possibility isinteresting in light of the recent dis-covery of Namaia bogenfelsi, a pri-mate from the middle Eocene of Namibia.62 This species is remark-able both for its antiquity and itslocation, being the first Eocene pri-

mate from sub-Saharan Africa.Unfortunately, it is represented solelyby a maxilla with the crowns of M2–3

(the P4 referred to N. bogenfelsi isfrom another locality that is prob-ably considerably younger, and fur-thermore is too small to belong tothe same species as the holotypemaxilla). Namaia was described asan anthropoid, but, in my opinion, islikely a stem or crown strepsirrhine(again, for lack of a better term, apossible ‘‘djebelemurine’’). Unlikeanthropoids known from the later

Eocene of North Africa, Namaia hasan M2 that is transversely narrowand completely lacks a lingual cingu-lum around the protocone, but has adistinct hypocone. Among Eoceneprimates, this upper molar pattern ismost similar to that of some Euro-pean anchomomyins.

The only other Paleogene Afro-Ara-bian species of relevance to the prob-lem of crown strepsirrhine origins isthe bizarre plesiopithecid Plesiopithe-

Figure 5. Lower postcanine dentitions of Paleogene Afro-Arabian primates. Top, scaled to

the same M1 length; bottom, to scale (scale bar ¼ 5 mm). A) Nosmips aenigmaticus , (Pri-

mates incertae sedis , earliest late Eocene, Egypt; B) Algeripithecus minutus (Strepsirrhini,

Azibiidae, early-middle Eocene, Algeria); C) Afradapis longicristatus (Strepsirrhini, Caeno-

pithecinae, earliest late Eocene, Egypt); D) Aframonius dieides (Strepsirrhini, Caenopithe-

cinae, latest Eocene, Egypt); E) Wadilemur elegans (Strepsirrhini, Galagidae, latestEocene, Egypt, M3 not preserved); F) Plesiopithecus teras (Strepsirrhini, Plesiopithecidae,

latest Eocene, Egypt); G) Catopithecus browni (Anthropoidea, Oligopithecidae, latest

Eocene, Egypt); H) Propliopithecus haeckeli (Anthropoidea, Propliopithecidae, likely early

Oligocene (stratigraphic placement unknown), Egypt); I) Qatrania wingi (Anthropoidea,

Parapithecidae, early Oligocene, Egypt, P2-3 not known); J) Apidium moustafai (Anthro-

poidea, Parapithecidae, early Oligocene, Egypt, P2-3 not known); K) Proteopithecus syl-

viae (Anthropoidea, Proteopithecidae, latest Eocene, Egypt).



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cus teras, known solely from the ter-minal Eocene Fayum Locality 41.While the dentition of djebelemur-ines apparently remained fairly con-servative through the Eocene, the an-terior dentition of Plesiopithecus is

very specialized, bearing a singleenlarged and procumbent tooth ante-rior to the premolars on each side of the lower jaw. This enlarged toothresembles the canine teeth of crownstrepsirrhines and is presumably ho-mologous,63 though it does differ insome key details – for instance inhaving a root that is in line with thelong axis of the crown, rather thanbeing mesially inflected. The onlyenlarged tooth of the upper dentitionis the canine,64 which would haveoccluded distal to the enlarged lower

tooth (that is, there is no evidencefor enlarged upper incisors thatwould have occluded tip-to-tip with

the enlarged lower tooth).Simons and coworkers63:194 sug-

gested that Plesiopithecus used theseenlarged anterior teeth to gnaw onresistant food items, and that thespecies ‘‘filled the niche in the foodchain of the African Paleogene occu-pied elsewhere by plesiadapiformsand arboreal squirrels.’’ One possibil-ity is that Plesiopithecus is derivedfrom a lineage that initially had a

toothcomb like those of generalizedcrown strepsirrhines, but subse-quently lost the intervening incisorsand enlarged and reoriented the ca-nine roots as part of the transforma-tion of these teeth into a gnawing orgouging apparatus. Plesiopithecuswas initially identified as an anthro-poid65 before the recovery of its cra-nium,64 which revealed that it hadenlarged orbits and no postorbitalclosure. Its lower molars are superfi-cially similar to those of later Paleo-gene anthropoids in being quite

bunodont, buccolingually broad, andlow-crowned; the lower premolarsare also superficially anthropoid-likein being obliquely implanted (Fig.5F). The upper molars of Plesiopithe- cus are very generalized and have acomplete lingual cingulum, as inearly anthropoids, but also earlystrepsirrhines such as Karanisia.These anthropoid-like dental featuresoccasionally pull Plesiopithecus overto the anthropoid side of the primate

tree in phylogenetic analyses,25,33,36

though that position is here consid-ered to be unlikely.

AN UNEXPECTED RADIATION OF

ANTHROPOID-LIKE ADAPIDS

As noted earlier, the early-middleEocene Chambi locality has alsoyielded two lower molars of a rela-tively large primate species. At thetime of its description as ‘‘an enig-matic mammal’’ by Court,56 the onlycandidate adapiform from Afro-Ara-bia was Djebelemur , explaining hisreluctance to attribute these speci-mens to Primates. He noted similar-ities to both sivaladapid adapiformsand non-primate hyopsodontid con-dylarths. Late Eocene beds of the

Fayum have since confirmed thatthere was a radiation of true adapidsthat diversified alongside djebelemur-ines and basal crown strepsirrhines

after an independent trans-Tethyancrossing (possibly from Europe, Fig.4). The Chambi teeth indicate thatthis dispersal had occurred by thebeginning of the middle Eocene.

The existence of this adapid cladewas definitively confirmed in 1995with the description of Aframonius dieides, a 1.5 kg species from theterminal Eocene Fayum Locality

41.66

Aframonius has elongate lowermolars with well-developed shearingcrests (Fig. 5D), greatly reducedupper and lower second premolars,large and sexually dimorphic can-ines, and fairly generalized uppermolars that bear large hypocones.67

As in some other adapiforms, themandibular symphysis fused in olderindividuals. Aframonius was initiallyinterpreted as another Afro-Arabiancercamoniine that was relevant tothe problem of anthropoid origins,but subsequent discoveries have

shown that Aframonius lacks postor-bital closure and has fairly enlargedorbits (work in preparation). Godi-not68 argued that Aframonius shouldbe removed from Cercamoniinae andplaced in a new subfamily of Adapi-dae, the Caenopithecinae, along withthe middle Eocene genera Caenopi-thecus (from Europe), Mahgarita(from North America), and Adapoides(from Asia). The hypothesis of amonophyletic Caenopithecinae has

since been supported by large-scalephylogenetic analyses.25,27,33

The later discovery of a highly spe-cialized caenopithecine, Afradapislongicristatus (Fig. 5C), at the 37Ma Locality BQ-2, revealed that the

group must have undergone a majordiversification during the middleEocene in Afro-Arabia. At 3 kg, Afradapis was the largest primateknow n from the Afro-ArabianEocene, and indeed one of the larg-est primates known from the Eoceneof any continent. Afro-Arabiananthropoids did not come to occupythis body mass range until well intothe early Oligocene, about 6 Malater. Afradapis had dorsoventrallydeep and robust mandibular corpora,a fused mandibular symphysis, and

numerous elongate shearing crestson its upper and lower molars thatare arranged in a pattern like that of folivorous howler monkeys( Alouatta). The premolar dentition of Afradapis is particularly remarkable;uniquely among ‘‘prosimians,’’ thegenus lost its upper and lower sec-ond premolar and enlarged the lowerthird premolar into a massive blade-like tooth that sheared against theupper canine. This arrangement isotherwise seen only in catarrhineanthropoids that appear much later

in the Fayum succession, but it wasnever taken to such an extremeamong Paleogene catarrhines. Afradapis’ molar morphology leaveslittle doubt that the species washighly folivorous,33 while its loris-like astragalus suggests a highlymobile ankle joint and a probablepreference for cautious climbingrather than leaping.36 Perhaps Afra- dapis occupied a niche similar tothose of extant Alouatta species,while living alongside advanced stemand basal crown anthropoids whose

feeding and locomotor ecology moreclosely resembled that of various liv-ing cebid species. It is fascinatingthat Afradapis might provide a phylo-genetically independent example of this adaptive strategy because asimilar niche has been inferred69 forpropliopithecid catarrhines such as Aegyptopithecus, which occur indeposits that are several millionyears younger, in the same restrictedpart of northeast Africa.



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THE ORIGIN AND

DIVERSIFICATION OF

AFRO-ARABIAN ANTHROPOIDS

Anthropoid diversity in the Fayumsuccession was long assumed to be

the result of an ancient anthropoidpresence in Afro-Arabia.40,51,53 Formany years, this hypothesis appearedto be bolstered by the early occur-rence of forms such as Algeripithecus, Altiatlasius, and ‘‘Tabelia.’’38 With theaffinities of late Paleocene Altiatla- sius very much open to debate, thecombined removal of early-middleEocene Algeripithecus and ‘‘Tabelia’’from the anthropoid clade35 and thediscovery of several candidate basalanthropoids in the middle and lateEocene of Asia70,71 has forced a

reconsideration of this long-held view.72 There are no longer any com-pelling records of Anthropoidea inthe early and middle Eocene recordsof Afro-Arabia; only a tiny lowermolar trigonid and talonid from the

44-46 Ma (middle Eocene) Aznagsite in Morocco, described as a possi-ble tarsiiform,73 remains as a possi-

ble middle Eocene anthropoid. A P4from Namibia referred to middleEocene Namaia62 displays someanthropoid-like features, but wasfound at a site that is of contested

age, as it also contains rodents thatare similar to those from the earlyMiocene of East Africa.45,74

In light of this, the oldestundoubted Afro-Arabian anthropoidsare those that are known from the37 Ma BQ-2 Locality in Egypt26

and the roughly contemporaneousBir el-Ater (Nementcha) site inAlgeria.75 Recently, it has been incor-rectly claimed that an anthropoid-bearing primate fauna from Dur at-Talah in Libya is 38-39 Ma in age,76

but it is probably several million

years younger, perhaps

35-36 Ma,and certainly younger than BQ-2based on mammalian biochronol-ogy.77 The Bir el-Ater site was thefirst to yield remains of Biretia, a ge-nus that was long known from onlya single lower molar.75 Work at BQ-2has since considerably expanded ourunderstanding of the genus, withmultiple specimens representingmost of the upper and lower postca-nine dentition, as well as fragmen-

tary mandibles and a partial maxillathat has revealed some interestingdetails of Biretia’s orbital floor.26

Biretia is now known from three spe-cies, all of which are tiny (< 300 g)bunodont anthropoids with molar

cusp patterns that are similar to, butmore primitive than, those of laterparapithecids known from the latestEocene/early Oligocene Jebel QatraniFormation. The upper molars of Biretia have well-developed hypo-cones and variably developed conulesintervening between the three pri-mary cusps, while the lower molarshave distinct hypoconulid cusps andreduced or absent paraconids on themore posterior teeth. Phylogeneticanalyses that have included this newmaterial of Biretia have placed the

genus as a basal member of a parapi-thecoid clade,25,26,28,33,34,36,72 a resultthat is consistent with the diversifica-

tion of parapithecoids that has beendocumented in younger beds in thesame area. Biretia is unique amongliving and extinct anthropoids inhaving a very compressed orbitalfloor; the orbital lamina is fused tothe palate and the lingual root of M2

is not only exposed in the orbitalfloor, but is itself apically com-pressed. This pattern was interpretedas a spatial correlate of orbital hy-

pertrophy, potentially implying that Biretia was nocturnal,26 but a morerecently recovered maxillary speci-men that preserves a portion of theorbital rim indicates that Biretiaprobably did not have particularlyenlarged orbits.78

One other as yet undescribedanthropoid species occurs at BQ-2. Itis much more common than Biretia,and now is represented by the entireupper and lower dentition, some cra-nial parts, and numerous postcranialbones. As reported in an earlier

abstract,79

this species shares dentalfeatures with slightly older Bahinia[from Burma (¼Myanmar)], andyounger oligopithecids such as Cato- pithecus and Oligopithecus but,unlike oligopithecids, retains threeupper and lower premolars and hasrelatively simple premolars. It is nowclear that this new species is alsosimilar to the poorly known youngergenus Talahpithecus from Libya.76

Unlike Biretia, the undescribed BQ-2

form and Talahpithecus lack conuleson the upper molars, have tinyhypocones, and entoconid and hypo-conulid cusps are closely appressedon the lower molars.

Work at BQ-2 has also uncovered

isolated teeth of a very odd primate, Nosmips aenigmaticus, whose higher-level affinities are currently unclear(Fig. 5A).33 The molars of Nosmipsare similar to those of later anthro-poids in being relatively short(mesiodistally) and having reducedparaconids and broad talonid basins;however, they differ in having poorlydeveloped hypoconulid and entoco-nid cusps. The P4 is also somewhatlike those of derived anthropoids inhaving an enlarged metaconid cuspthat is connected to the protoconid

by a tall crest, but the tooth is rela-tively elongate, with a long, curvedparacristid. This pattern is furtherexaggerated on P3, which bears aparticularly long, arcuate paracristid.The upper molars appear to be quiteconservative, with no conules and nohypocone, while the P3 has elongatebuccal crests that would shearagainst the elongate P4 paracristid.Seiffert and coworkers33 ran severalphylogenetic analyses, alteringassumptions about ordering andscaling of multistate characters, and

found that Nosmips was not consis-tently placed in Anthropoidea. Intri-guingly, it would occasionallyemerge as the sister taxon of Plesio- pithecus. Nosmips’ phylogenetic posi-tion simply cannot be determinedwithout more informative remains.

The younger Talahpithecus-bearingprimate fauna from the Dur at-Talahbeds in Libya, at present made upentirely of isolated teeth, alsoincludes species of Karanisia, Biretia,and, surprisingly, Afrotarsius,76 aform that is otherwise known from

early Oligocene beds in the Fayumarea. Afrotarsius has been the topicof ongoing debate since its initialdescription as a tarsier relative in1985.80 Some authors have arguedthat it might be a basal anthropoid.52

Previously known only from a partialmandible with M1-3 and the P4talonid, the new discoveries fromLibya include the first upper molarsof the genus, which reveal a remark-ably primitive occlusal morphology.



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Though Jaeger and colleagues76

interpreted Afrotarsius as a stemanthropoid ‘‘eosimiiform,’’ it shares

features with the primitive Miocenetarsier Tarsius sirindhornae81 (fromThailand) that are not seen even inthe most primitive eosimiids.71 Thenew evidence suggests to me that Afrotarsius is indeed a tarsier relative.

THE ASIAN CONNECTION

The anthropoids from BQ-2 andBir el-Ater are the oldest from theEocene of Afro-Arabia, but they

occur at the end of a long (10 Ma)gap in the Afro-Arabian fossil recordthat has been filled only by the

poorly documented Namaia-bearingBlack Crow site in Namibia and theMoroccan Aznag locality (Figs. 2 and3). Anthropoids could have arrived inAfro-Arabia at any point during thatinterval. So where did they comefrom? This is not a question that canbe answered by considering Afro-Arabia alone, because many special-ists now consider Asian eosimiids tobe basal stem anthropoids, while themuch more derived amphipithecids,

known primarily from Burma andThailand, are generally situated in amore advanced position within

Anthropoidea, potentially within thecrown clade (Fig. 6).33,72,82 Amphipi-thecids pose major problems becausethey are not represented by completecranial remains. Also, there is con-siderable uncertainty surroundingattribution of isolated primate post-cranial bones from the primaryamphipithecid-bearing sites inBurma; some of these bones resem-ble those of adapiforms while othersmore convincingly resemble those of

Figure 6. Time-calibrated MRP supertree based on nine trees from six sources, 22,24,34,35,72,82 with a parsimony reconstruction of a biogeo-

graphic character on the MRP tree; the reconstruction is the same whether the character is treated as unordered or ordered as North

America ¼> Asia ¼> Afro-Arabia ¼> South America. The analysis was rooted with the early Eocene North American adapiform Cantius .

The taxa Kamoyapithecus , Saadanius , and Lokonepithecus were not included in any of the source trees and are placed close to

their inferred phylogenetic positions (advanced stem catarrhines in the case of Kamoyapithecus and Saadanius ; Lokonepithecus is

placed near Parapithecidae). Body mass is shown by a heat map. To the right, representation of different anatomical parts known for

each taxon. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]



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undoubted anthropoids.83,84 By thelate middle Eocene, the teeth of large-bodied amphipithecids are cer-tainly anthropoid-like, but are al-ready very highly specialized, leadingsome to argue that amphipithecids

are adapiforms that evolved theiranthropoid-like dental features convergently.83 Furthermore, the cali-bration-free molecular dating analy-ses of Steiper and Seiffert28 suggestthat the anthropoid crown clade ori-ginated close to, or even after, someof the most highly specializedamphipithecids had left theirremains in the 37 Ma PondaungFormation of Burma – again argu-ing against their placement ascrown anthropoids.

Several recent phylogenetic analy-

ses have included Paleogene anthro-poids, but these studies differ intheir sampling of characters andtaxa, and, not surprisingly, in theirresults. One way of summarizing allof these different results is to use a‘‘supertree’’ method (matrix represen-tation with parsimony or MRP),which converts the source trees fromeach study into their own matrices,in which members of each clade areassigned a derived state; all of theresulting matrices from each sourcetree can then be analyzed together to

find the most parsimonious resultfrom all of the studies combined. AnMRP analysis of early anthropoids ispresented in Figure 6. The resultingsupertree places eosimiids and Altiat-lasius as the most basal stem anthro-poids, while amphipithecids inter-

vene between crown Anthropoideaand a proteopithecid-parapithecoidclade. When biogeography is mappedonto this supertree, four trans-Te-thyan dispersals from Asia to Africaare reconstructed, one that explainsthe early presence of Altiatlasius, one

that explains the later presence of Afrotarsius (placed as a tarsiid in thesupertree), and two independent dis-persals to explain the presence of 1)a proteopithecid-parapithecoid cladeand 2) a crown anthropoid clade inAfro-Arabia. This reconstructionhinges on the position of the early

Oligocene primate Bugtipithecus,from Pakistan, a genus known fromonly a few isolated teeth that wasdescribed as an amphipithecid,24 but

is placed outside that clade in thesupertree. If Bugtipithecus is movedto be a basal amphipithecid, the bio-geographic reconstruction for theentire anthropoid stem lineagechanges to being ambiguous (that is,

either Afro-Arabian or Asian).At present, I consider it likely thatamphipithecids are stem anthropoidsthat originated and diversifiedentirely in Asia, while the proteopi-thecids, parapithecoids, and crownanthropoids that are known from thePaleogene of Afro-Arabia are derivedfrom a single middle Eocene disper-sal from Asia, with a subsequentdispersal of platyrrhines to SouthAmerica from Afro-Arabia. This pat-tern is consistent with evidence forstrongly filtered trans-Tethyan

exchange between Afro-Arabia andAsia in the middle and late Eocene,leading to competition between new-comers from Asia (anthropoids andhystricognathous rodents) and previ-ously established clades derived fromcolonizing lineages that arrived inthe early-middle Eocene, possiblyfrom Europe (caenopithecines, djebe-lemurines, and zegdoumyid rodents)(Fig. 4). Anthropoids would ulti-mately come to dominate the laterPaleogene primate faunas of north-ern Africa in the same way that

hystricognaths dominated the NorthAfrican rodent faunas (Fig. 7). Atrans-Tethyan dispersal in the oppo-site direction has also been docu-mented, with the anomaluroidrodent Pondaungimys, unambigu-ously of Afro-Arabian origin,45,46

appearing in southeast Asia in the37 Ma fauna that also includesamphipithecids and Bahinia. Hyae-nodontid creodonts probably alsoparticipated in this exchange, thoughthe direction and timing of disper-sal(s) are currently difficult to evalu-

ate because their relationships arepoorly understood. Anthracotheriidartiodactyls, which would also enjoygreat success in the later Paleogeneof Afro-Arabia, dispersed from Asiato Afro-Arabia, apparently in thelater Eocene, after the deposition of BQ-2.85 A close biogeographic con-nection between Afro-Arabia andAsia in the Eocene is also supportedby the shared presence of afrotar-siids.72

By the terminal Eocene, threeanthropoid clades—oligopithecids,parapithecoids, and proteopithe-cids—were present in Afro-Arabia(Figs. 2, 3, 6, and 8) and living along-side the last strepsirrhines known

from the Paleogene of northernAfrica ( Aframonius, ‘‘ Anchomomys’’milleri, Plesiopithecus, and Wadile-mur ).53 All four of these strepsirrhinelineages went extinct, at least locally,near the Eocene-Oligocene bound-ary, and these disappearances havebeen linked to the early Oligoceneglobal cooling event.86 In contrast,

judging from their abundance at the

34 Ma Fayum Locality 41, all of these anthropoid clades were quitesuccessful, presaging the later suc-cess and further diversification of

catarrhines and parapithecids in theearly Oligocene. By the terminalEocene, basal catarrhines, best rep-resented by the oligopithecid Catopi-thecus browni, had already evolved anumber of distinctive dental apomor-phies (notably the loss of P2 /2 andthe presence of sexual dimorphismin P3 /3 size) and postcranial apomor-phies that are shared with propliopi-thecids and crown catarrhines.87–89

Like all other Paleogene anthropoidsknown from crania, Catopithecus andProteopithecus evidently had rela-

tively small brains when comparedwith those of extant anthropoids, butotherwise exhibited anthropoid syna-pomorphies such as full postorbitalclosure, small and convergent orbitalapertures, fused metopic sutures,and intraorbital lacrimal foram-ina.89,90 Unlike crown anthropoids,Catopithecus and Proteopithecusclearly lacked full fusion of the man-dibular symphysis, but the suite of apomorphies that Catopithecusshares with later catarrhines sug-gests that fusion evolved independ-

ently three times – i.e., in platyr-rhines, catarrhines, and parapithe-coids. The postcranial remains of Catopithecus show that it was prob-ably a more cautious climber thansympatric Proteopithecus, whichexhibits postcranial features that areconsistent with more rapid locomo-tion and pronograde leaping. Thesereconstructions have now been sup-ported by analysis of these species’semicircular canal sizes.91 The molar



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teeth of Catopithecus have relativelywell-developed shearing crests, sug-gesting that the species was either afrugivore that supplemented its diet

with insects, or was partially folivo-rous,92 while Proteopithecus wasmore clearly a generalized frugivore.Like parapithecids and propliopithe-

cids, both Catopithecus and Proteopi-thecus had sexually dimorphiccanines that presumably reflect apolygynous mating system.93 These

Figure 7. Changing models of Paleogene primate evolution in northern Africa. At far left, a popular view in the early 1990s, based on

the interpretation of late Paleocene Altiatlasius and early-middle Eocene Algeripithecus and Tabelia as anthropoids. Middle, revised

view following the identification of Algeripithecus and Tabelia as azibiid strepsirrhines and the recognition of a diverse Afro-Arabian

adapid radiation that probably extends back well into the middle Eocene. At right, an analogous dispersal-replacement scenario in

the Afro-Arabian rodent fauna, in which later arriving hystricognathous rodents from Asia replace earlier immigrants from Europe (Zeg-

doumyidae/Anomaluroidea). [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]

Figure 8. Crania of A) the early Oligocene parapithecid anthropoid Parapithecus grangeri ; B) the late Eocene stem catarrhine Catopi-

thecus browni (note that this specimen has undergone extreme post-depositional distortion); and C) the early Oligocene stem

catarrhine Aegyptopithecus zeuxis . [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]



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genera occur alongside Arsinoea, stillknown only from very limitedremains, and Serapia, which is verysimilar to Proteopithecus and prob-ably a close relative.31

Propliopithecids such as Aegyptopi-

thecus, Moeripithecus, and Propliopi-thecus appear in northern Africa inthe early Oligocene, and have teethlike those of generalized crown catar-rhines from the early Miocene of EastAfrica. Aegyptopithecus has long beenknown from well-preserved cranialand postcranial remains,31 the latterof which closely resemble those of extant howler monkeys. A small juve-nile female Aegytopithecus craniumhas recently helped to confirm thepresence of extreme sexual dimor-phism in molar size, body mass, and

craniofacial morphology within thespecies94 – a pattern that is continuedin early Miocene catarrhines. The

recently discovered facial and basicra-nial remains of Saadanius hijazensis,from the late Oligocene of Saudi Ara-bia, strongly suggest that the facialmorphology of propliopithecids wascharacteristic of advanced membersof the catarrhine stem lineage.95

The parapithecid clade is repre-sented at L-41 by the tiny Abuqatra-nia, whose bulbous molar cusps are

very similar to those of 1 Ma

younger Qatrania and the highlyderived genera Apidium and Parapi-thecus, which are well-known fromsites that are 3-4 Ma younger.Parapithecids were apparently largelyfrugivorous,92,96 and abundant post-cranial remains have been interpretedas indicating that these forms wereagile leapers, though semicircularcanal size suggests a ‘‘slow’’ mode of locomotion.91 At the time of deposi-tion of the youngest primate-bearingsites in the Fayum succession (the29-30 Ma Quarries I and M),

Apidium and Parapithecus were verycommon in northern Africa, but untilrecently members of this clade werenot known from younger beds. Para-pithecids have now been foundfarther south, possibly in the latestOligocene of Tanzania97 and defini-tively from the late early or lateOligocene Lokone site in Kenya,which has yielded a mandible andisolated upper teeth of a form called Lokonepithecus.98 It appears that

parapithecids did indeed continue todiversify, at least in sub-SaharanAfrica,86 but have never been foundin the Miocene. Parapithecids wereonce thought to be closely related tocercopithecoid catarrhines due todental and postcranial similaritiesthat the two groups shared, but arenow generally placed as stem anthro-

poids (Fig. 6). Perhaps competitionwith cercopithecoids played a role intheir final extinction near the Oligo-cene-Miocene boundary.86

EVOLUTION OF AFRO-ARABIAN

PRIMATE COMMUNITIES IN THE

PALEOGENE

It is now clear that primate com-munities in Afro-Arabia underwent

several major phases of restructuringduring the Paleogene. During the latePaleocene and Eocene, individualcolonists from northern continentswould make it into Afro-Arabia viachance dispersals across the TethysSea, go on to adapt to local environ-ments and diversify, and, millions of years later, be faced with competi-

tion from another immigrant lineage.Later, environmental change associ-ated with global cooling appears tohave played an important role, as itprobably constricted the latitudinalrange of thermophilic crown strepsir-rhine clades (e.g., galagids), and, insome cases, might have driven stemstrepsirrhine lineages into extinction(adapids, plesiopithecids, and djebe-lemurines).86 Anthropoids persistedinto the Oligocene in northern Africa

Figure 9. Principal coordinates analysis (calculated in PAST100) of pairwise distances (calcu-

lated in PAUP 4.0b10101) derived from the 373-character morphological matrix of Patel and

coworkers34 (which includes postcranial, dental, cranial, and soft- tissue characters), with

Algeripithecus , Azibius , Nosmips , and Plesiopithecus added. ‘‘Prosimian’’ taxa from the Afro-

Arabian Paleogene are invidually labeled; other groups are enclosed by convex polygons.

The ‘‘anthropoid-like adapiforms’’ polygon encloses the space occupied by Adapis , Afra-

dapis , Aframonius , Caenopithecus , Darwinius , Hoanghonius , Leptadapis , Mahgarita , Protoa-

dapis , Rencunius , and Wailekia , all of which are here considered to be adapiform stem

strepsirrhines. Note that the possible stem anthropoids Bahinia and Nosmips also occupy this

space, while late Paleocene Altiatlasius and late Eocene/early Oligocene Afrotarsius clusterwith tarsiiforms. The ‘‘Paleogene Afro-Arabian anthropoids’’ polygon encloses the extant

platyrrhines Aotus and Saimiri and the extinct platyrrhines Branisella and Dolichocebus .

[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]



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in what might have been relativelymarginal, unpredictable environ-ments.

One interesting way of envisioningadaptive trajectories within thesecommunities is to analyze a large

morphological character matrix witha phenetic approach, such as amultivariate analysis of pairwise dis-tances between taxa. In this case, thedistances between species providean approximation of the overallsimilarity or difference of speciesbased on the character states thatthey have been assigned, withouttaking into account the polarity of traits or the historical (phylogenetic)basis for how they came to exhibitsuch a character complex. Speciesthat share many character states are

separated by short pairwise distan-ces, while those that share few char-acter states are separated by largepairwise distances. Analysis of onesuch matrix of morphological fea-tures from the dentition, cranium,and postcranium34 (Fig. 9) revealsthat known living and extinct prima-tes occupy a fairly restricted charac-ter space, and that one zone of thatspace was repeatedly occupied bydistantly related lineages thatconverged on an ‘‘anthropoid-like’’pattern, either on northern conti-

nents or in Afro-Arabia. On northerncontinents, this zone was occupiedby several adapiforms that have, atone time or another, been identifiedas candidate anthropoids (forinstance, adapines, caenopithecines, Darwinius, and sivaladapids). InAfro-Arabia, this zone was first occu-pied by azibiids – one of which, Algeripithecus, was initially identifiedas an anthropoid43 – and later by thecaenopithecine clade that would giverise to Afradapis and Aframonius, thelatter of which was also initially

identified as a possible anthropoidrelative.66 Plesiopithecus occupiesthis zone, and it, too, was firstidentified as an anthropoid.65 Finally,the enigmatic Nosmips, a taxon thatshows both anthropoid-like andstrepsirrhine-like features, is alsoplaced in this general zone. Thoughthe oldest eosimiids fall close totarsiiforms on this plot, the younger(and, in my opinion, more con-

vincingly anthropoid-like) Bahinia

later came to occupy the same‘‘anthropoid-like’’ character space.Could it be that a form like Bahiniadispersed into Afro-Arabia in themiddle Eocene, faced competitionwith adaptively similar, but distantly

related, ‘‘endemic’’ forms such ascaenopithecines and plesiopithecids,and that this competition played acritical role in determining theadaptive trajectory of later anthro-poid evolution? The oldest Fayumanthropoid, Biretia, falls closest tothis zone, and later – via independ-ent phylogenetic pathways – themembers of sequentially youngeranthropoid communities docu-mented in the Fayum area divergealong a seemingly predictable trajec-tory, taking this generalized pattern

to an extreme by convergentlyevolving craniodental features thatwere long thought to define Anthro-poidea as a whole. The Afro-Arabianrecord is, unfortunately, simply notyet complete enough to allow forlarge-scale, temporally constrainedtests of hypotheses related to com-petitive exclusion or characterdisplacement, but these are certainlyintriguing possibilities, and are ideasthat could not have even beenproposed without the wealth of surprising fossil evidence that has

accumulated over the course of thelast two decades.

ACKNOWLEDGMENTS

I thank all of my collaborators onthe Fayum paleontological projectfor their friendship and guidance,particularly E. Simons, T. Bown, andP. Chatrath. I also thank G. Gunnellfor loan of fossils; D. Boyer forproviding casts; T. Ryan for provid-ing scans; C. Gilbert, J. Fleagle, G.Gunnell, K. Reed, and C. Seiffert forcomments on the manuscript, and J.Fleagle for his great patience as aneditor. Research in the Fayum areahas been supported by the U.S.National Science Foundation andThe Leakey Foundation.

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