Borie) We Reprinted from the Cambridge Encyclopedia of Human Evolution; J. S. Jones, R. D. Martin, D, Pilbeam and Sarah Bunney, eds. Cambridge: Cambridge Univ. Press, 1992 6.3 Evolution of Old World monkeys The group of higher primates called the Old World anthropoid primates, orcatarthines, staxonomically more diverse today but morphologically more homogeneous than is sister taxon, the New World anthropoids or playr rhines. Modern catarrhines are represented by only two superfanilies ~ the Cercopithecoidea (Old World monkeys) and Hominoidea (apes and humans). There is still controversy about the classification and evolutionary relationships ofthese subgroups Living Old World monkeys The living Old World monkeys comprise a single family Cercopithecidae, with wo subfamilies, Cercopithecinae (cheek: pouched monkeys) and Colabinae (leaf monkeys) (see Box). AIL cercopithecids share several distinctive features that make it bikely that they have a common cestry, and they thus constitute a monophyletic group, As with other catarrhines (hhominoids), they have only «vo premolars in each jaw. The three molaes in each quadrant are long and have two crests (lphs) connecting transverse paits of cusps (bilophodoat condition), There is usually con: siderable sexual dimorphism, especially in the size and shape ofthe canines and the front lower premolar, and the upper canine has a deep groove that extends onto the root, panicularly in males. Old World monkeysarenot united by special features ofthe skull, but the rest oftheskeleton does, Ihave some unique and diagnostic characters ~ such as the various structures that aid in rapid quadrupedal locomo- tion along branches oF on the ground, ‘Thetwosubfamiliesalso have diagnostic features, especi- ally in dies, which are reflected in theie vernacular names. The cercopithecines are cheek-pouched monkeys, and hhave buccal sacs used for storing food: they will eat almost anything, but ofien concentrate on fruit. The colobines eat, leaves, which they digest m specialised guts convergently similar to those of ruminant artiodacrylssuchascatle.Diet- ary preferences are also reflected in teeth, Cercopithecines retain more primitive’, rounded bilophodont molars, with rather large incisors, he lower ones having completely lost the enamel on their inner surfaces. By contrast, colobines have relatively smaller incisors and sharper, high-cusped teeth Modem cercopithecines include both tree-climbing and, terrestrial species, whereas living colobines almost all ive, run and leap in trees and have reduced or almost absent ‘humnbs. The skull of colobines has widely spaced orbits, 4 narrow nasal opening and a short face, whereas that of ‘cercapithecines especially in the long-snoured baboons ~ shows the opposite pattern poe A CLASSIFICATION OF LIVING AND FOSSIL OLD WORLD MONKEYS Famiy Cercop thecidse (Ol6World monkeys ‘Suara iy Carcoptncinae chook poucned monkey] Subtibe leropiiecina “Allesopiteus lens wong merkey subtnaeGereapthacne ‘Cerconecusiguenors) Exjtrocebus pats monkey) Tree Popionn| Subtbe Paponins Pape ® Papo baboons) Maren) orimanet 'p.Dinpirecus) comoceoue C cecovebus eesti mangabeys) 6 itemorebus} ooea margnbes) "corgopitecus ‘eropitnecus geese eb00n) oubtteacacis "procynoceanaius "Poradoneropiecus Subtomiy cold a Suotibe co.biea ‘Colobu (ac colobus monkeys) (Pnceoioous)edclabue mone ‘uypanecus ‘Coroptheoides ‘mireolnave subtibe Pestyting Presb (els) Sennopithecus ' iSernopithecu) anaes 5. aenypinecus lat monkeys Prgainen Pratt (so tang) P.Rninopinecis srub-rose angus "i Nasa (geboseismarkey) I (Simas) Pagel sand argu) Subfamily Calooiac uneeroin antes) "esontecss Subfamily Vetorapthecinae Famiy oreopansesaaa "Orvopiecus 278 The primate fossil record Within dhe Cercopithecinae, the Affican guenons and theit celatives make up the telbe Cercopithecini, and the baboons, mangabeys and macaques form the Papionin The latter all have an essentially similar chromosome ‘complement karyotype) with a diploid number of $2. The Cercopithecini have lost the distal (hindmost) cusp on the hird molar, and their diploid chromosome numbers range berween 48 and 72, oRen in groups separated by multiples of 6. This diversity of karyotypes might reflect a pattern of Narrow incisors speciation in closely adjaceat populations. oro regether Shatow jaw A tong ti! aimsanclegs| er one ta of similarsian Fectures characterising the modern subtamlies of Old Worié monkeys The taxonomy of living colobines fits well with their geographical distribution (see p. 34)- However, the dif ferences between African and Asian forms are not as trong, as between cercopithecine tribes, with only minor con: pinion trasts in teeth and limbs. Molecular primatologists have concentrated on analys- Representative living Olé World monkey: a cercopthecine (blow), {he chacma 93000" (Polo Mamaaryas ursinus fr. usin), Wom ing the relationships among relatively distantly related ete pecnannt io nencocemaee primates and among hominoids, Lite is known of the Bemes genetics of cercoplthecd genera. The difference between Cereopithecines (eheek-pouched monkeys) oy Large, multenamberes storie ‘creek pouches tor string food ‘ordigesing leaves (usualy a)colobines and cercopithecines is comparable in several \waysto that between orang-utans and Affican apes, so that these two phyletic splits may have occurred at about the Early diversification ‘The origin of the Old World monkeys is not well reflected In the fossil record. A form called Proplopthecus, known from early Oligocene deposits in Egypt around 33 milion yeats old, may have been close to the common ancestry of all modern catarthines. With the exception of a single Uuppertooth from Uganda, however to the cercopithecids is known from Oligocene or early Miocene deposits no fossil with clearies Forty cero suvtemly coiohinae = 7 A Tove I | sunrie Prestyina Ing calgina Cy ~ 3 ei. 2 P fige.d 2g. bells feeb 258 55 2 abla Fegee of 2& a £8 EER Miocene 19) ‘Age imulions of years) Evolution of 6 World monkeys. | 219 By early middle Miocene times, 17 to 15 million years ago, several varieties of early cercopithecid existed in northeastern Africa, Prohylobates is represented by parts of {four lower jaws from Egypt and Libya, and Victoriapthecus left afew jaws, some limb bones and hundreds of isolated teeth at Maboko, Kenya, Specimens from other sites have Eolutonaryeatonships, ime ranges and major groupings of Olt World monkeys. The genera and subgenera (and species groups or Trerpitneees) sundwsione. Soa dotted ines ndeatehyptnesinne ‘question marksindeate expecially ed A Band | represent mong specie group As the corepithecines8, he spit fe spt among ving Aslan colabines. secisne Vierouapimecinae —Cercopitecinae Ccercopimecn)———_Papigainy of The wacacina—— Paptonina VY IA | g 35 2 gs 2 Gf ae 82 gise? 28 $, 223 22 PHL diaba abu ESPs EP 25882 80888 FF ESSE SEES SS Fo ok 22 cercootnecina 2 allenopithecina220 The primate fossil ecord been assigned (0 one or the other genus, and it has been suggested that the two may not realy be dierent. These early cercopithecids, best termed the subfaraily Victoriapithecinae, show that monkeys were presen. in ‘more open habitats than those dominated by hominotds They moved on the ground to some extent, and ate more leaves than hominoids. Modern species have a similar way of life, and this may have promoted the divergence of the first cercopithecoids from their ancestors. By the late Miocene (8to9 million yearsago),cercopithe: ccoids were present across the Old World and had replaced most ofthe hominoid and early catarshine lineages that had ‘dominated the earlier Miocene. Atleast six and perhaps as many as 10 independent lineages developed a strong com mitment to life on the ground, and monkeys invaded all types ofhabitat rom the fringes of desertsto snowy forests. The enigmatic European Oveopithecus ambos known from a crushed skeleton and some jaws and limb bones from 810 9 million year-old sitesin lay (see p. 225) Itsteeth are highly distincuve, but some authorssee certain dental similarities to cercopithecids, suggesting that the ‘two lineages shared a common ancestor. However. the postcranium is more like that ofhominoids. Some Aftican species dating to between 19 and a4 million years old resemble Oreopithecus and are placed with it in the family Oreopithecidae. IC is unclear whether this unique group should be placed in the Cercopithecoidea, in the Hominoidea or even ints own superfamily, + Preistocene # Miocene [ Princpal sts of lscovry of Olé World monkey oss nte Attican monkeys of the Miocene and Plio-Pleistocene ‘Monkeys from late Miocene times are rare in Affica, but a very small colobine is known from Kenya, and both col: obines and imacaque-like cercopithecines are_ present across the continent's northern fringe. Its likely that the Sahara desert had become a barrier nonth-south move. ‘ment of mammals by 7 million years ago, leading to the separation ofthe Papionin! into sub-Saharan baboons and mangabeys on one side ofthe desert and Noeth Africanand Eurasian macaques on the other, African and Bunsian col- ‘obines may also have been separated at this time. There is no fossil evidence, but the Cercopithecini probably di verged from ancestral cercopithecines even earlier, enter- ing the high canopies ofthe rain forest perhaps around 10 million years ago. The African Pliocene wasa time of great diversification of | (Old World monkeys. Wide expanses of plains alternated with forests in the east and south, offering numerous habitats for both colobines and cercopithecines. The radi ation of the colobines is perhaps the most impressive. with up oseven species present in late Pliocene umes, 2 million years ago, around Lake Turkana in Kenya, Cereopithecides species were terrestrial, medium sized to large colobine monkeys of Kenya and South Affica; their heavily wornPoracotoous (2) “y Loynecus (ct) riacotobus (oh) Ccereopinecoaes(c) Right sae vews of reconstructed shls at exit eobine monkeys. Sceomparied (centre) bythe shals of wo moder species (colabue pobores ana Nasaisarats) for eompanson rm approximately {othe same scale) Notice the ciffrencein size betweonnelsing 3 ceeth probably reflect an abundance of grit in their det, from foraging on the ground where living colobines seldom stay. Even larger were the highly arboreal Rhino colobusand less specialised” Pareolobus ofthe Turkana Basin. Al three forms were larger than any living colobine, in the range of mid- to large-sized baboons. Fossils of several species of smaller colobines, some probably belonging to the living genera, are also known, At the same time, papionins were represented by mem- bers ofseveral lineages. Parapopl rom southern and eastern Africa was partly terrestrial and had alittle derived skull. It ‘was perhaps close to the common ancestry of later papio- nins and was somewhat like Eurasian macaques. Fossils of rmangabeys and guenons are rare, but the extant baboons Papio and Theropithecus are well represented in the Pliocene and Pleistocene. All populations of the common savanna baboons living today appear to interbreed and are thusbest grouped in 2 single species, Papo hamadiyas. This includes not only the maned Hamadryas baboon butalso the guinea, olive, yellow and chacma baboons, which previously were rogaeded as separate species, Fossil populations afthisspe ies first appear by about 2.5 million years ago, alongside a smaller species that persisted for 0.5 10 1 million years. Evolution of Old World monkeys Although P. bamadipas (in its broad sense) is widespread today in Alfiea, 1 was not common in Plio-Pleistocene times, except in South Africa between 2 and 1.5 million ‘years ago. Another large form wis previously placed in its ‘own genus Dinopthecs, but isnow assigned (oasubgenus of Papio itis known only between 3 and ss million years ago. The gelada (Theropithecus gelada) lives today only in the Ethiopian highlands, but in the past it had a much wider distribution. The living gelada, a specialised ground-dwel: Jer, feeds mainly on grass blades and seeds: relatively small as it uses its fingers for food preparation. The first specimens showing distinctive gelada-like molars appeared by 4 million years ago, and at least three exsinet species are known, ‘Thropthecus dort is present in eastern and southern sites older than 2.5 million years and has a fully terrestrial skeleton and somewhat reduced incisors. Populations of | 1. oswaldi increase in size after about 2 million years ago, spreading into northwestern Africa and even India, The large, later Pleistocene animals have very small incisors and short, stout canines. tn this, they show parallels to hominids. The distinction between T. esaldi and its prob: able ancestor, T. drt, is fairly arbitrary, but the later has larger front ceeth, Theropchecusbrumpd, which haseven larger \esors and a distinctive facial shape. is known only in the Lake Turkana region between 3.3 and 2.3 million yearsago. construction ofthe skeleton of nig male Thrspthecusoswal, nl lant baer of the East AcanPleistaeae. The shall female In ttm Soh 2222 The primate fos record ‘This female specimen assembled rom many unassocated prt) was {oundin Greece ands about 8 ailonyearsld, The separate shile sromale tt) and tomate gh) ‘The oldest members ofthis lineage have skulls and teeth similar to those of Papia, suggesting a close phyletic kink between these genera, as well as much parallel evolution within Theopthecus. The T. brumps lineage probably div- cerged early from the common ancestor of T.gelada,T. dart and T. aswell Eurasian monkeys of the Miocene to Pleistocene ‘The colobines entered Eurasia long before the cercopithe- ines, and diverged into European and Asian subgroups. Dozens of skulls and posteranial elements of Mespithecus have been found, especially inthe Balkans in deposits dat ingto between gand million years ago. Other populations ‘extended as far east as Afghanistan and perhaps India, and ‘westwards to France and England as recently as 3 millon years ago. Mesopthecus was probably similar to the living Hanuman Tangur (Semnopithecus oF Preshyis entells) in its adaptation to life in forests and on the ground; ts thumb is less reduced than in any other colobine, but mote than in cercopithe- cines. A possible descendant of Mesopithecusis Dolichopthecs, a larger, longer-aced and more terrestrial colobine from deposits in central and southern Europe dating to between 6 and 3 million years ago, and perhaps somewhat later in Mongolia. Other Asian fossil colobines are mainly mem bers of the living genera, whose relationships are still unclear, The only Eurasian cercopithecines (other than a single mpthecis maailla) are the macaques and their extinct relatives. There are four main groups of macaque species: the North African (and extinet European) Barbary macaque (Macaca sylvan); the ion-tailed macaque (M. sienus) group ‘of India and Southeast Asia; the Toque macaque (M.snie) ‘group of South and East Asia; and the widespread group of cerab-eating macaques (M. fescculais. Both morphology and biochemistry agree in distinguish Ing these groups, although the details of their relationships are not yet cleat. Macaque-like papionins first appear in North Africa in the late Miocene when the Mediterranean Sea dried up, and had entered Europe by the earliest Pio cene, when it had refilled. Many European populations between England and the Caucasus have been nazned, but none can readily be distinguished from M, splanus Macaques persisted in Europe until the last interglacial, about 100000 years ago, afier which they were restricted to North Africa Im Asia, macaques spread to India by around 3 million yeats ago; «wo Chinese teeth may be ¢ million yeats old. Crania from the Pleistocene of China probably represent a member ofthese group, and the several living species on Sulawesi are probably derived feom asilenus group popula tion that crossed from Borneo on a land bridge when sea levels were lower, and then speciated in isolated pacts of the island, Macaques are not particularly specialised for life on the ground. In this, they are comparable to mangabeys and to Porapopio. In the late Pliocene and early Pleistocene of Europe, a larger, more terrestrial lineage flourished as the genus Parudolichopithewus. Less well-preserved specimens from China and India may represent a second macaque ‘experiment’, of an extension of the range of Paradolicho- pitheus, which is also known ftom Central Asa ‘The entry of humans into Asia by Imillion years ago may have driven these large monkeys to extinction, perhaps because they, like the lage geladas of Africa, were hunted for food Bic Delon ‘Seals Clasiteaton and wolaonsy lations 47) -N | teat 3.56), Det and gut (p60). Primate locomotion and porte, 78). Landmoveranis and species dipere! ip. 169) Reconstucting past eritonmert’ 9.191), The fossa of ues a eltedness pp 293-3)