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Chromosomes and the origins of and Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé, M.J. Deshayes

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Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé, M.J. Deshayes. Chromo- somes and the origins of Apes and Australopithecines. Evolution, Springer Verlag, 1996, 11 (1), pp.43-60. ￿halshs-00426146￿

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HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. I1UMAN EVOLUTION

J. Chaline Chromosomes and thé origins A. Durand of Apes and Australopithecines

D. Marchand Comparison of molecular data suggests that thé higher apes (Go- Paléontologie analytique et Géologie rilla. ) and humankind () are closely relatcd and that sédimeniuire (UMR CNRS H5561) they divergcd from thé common ancestor through two et Préhistoire et Paléoécologie events situated vcry closely togcther in lime. Examination of Ihe du Quaternaire de i'EPHE, chromosomal formulas of thé living species reveals a paradox in Université de Bourgogne, thé distribution of mutated chromosomes which can only be re- Centre des Sciences de la Terre, solved by a model of trichotomic diversification. This new model 6 bd. Gabriel, 21000 Dijon, Franc? of divergence from thé common ancestor is characterizcd by thé transition from (1) a monotypic phase to (2) a polytypic phase of threc sub-species - pre-, pre- and prc- A. Dambricourt Malassé australopilhecine. The quadruped ancestors of Australoptthecus appear to hâve been one of thé Huée components of (ne common UMR CNRS 9948, InMiiut de ancestor. The question is whcther ramidus îs an australopilhecine Paléontologie humaine, or a pre- représentative of thé common ancestor. / rue R. Panhard, The new model of diversification of thé common ancestor is 75013 Paris, France rcsituatcd in thc paleogeographic and paleoclimatic context which, through Ihe norlh-south pattern of extension of aridity. provides a cohérent scénario for thé formation of ex(ant species and sub- M. J. Deshayes species of thé Corilla and Pan gênera. Rue Pasteur, J8 14000 Caen, France

1. Introduction

Research into hominoid évolution involves multiple disciplines. Although scparate stud- ics hâve been conducted in various areas molecular analysis (Miyamoto et al.,1988; Bailey et al.,1992; Goodman et al., 1994), hlood serology (Wiener & Moor-Jankovsky, 1965; Socha & Moor-Jankovski, 1986), chromosomal design (Chiarelli. 1962; De Grouchy et al., 1972; Dutrillaux et al., 1986; Dutrillaux & Couturier, 1986; Stanyon and Chiarelli, 1981, 1982, 1983; Yunish and Prakash, 1982), developmental data (Dambricourt Malassé, 1987, 1988, 1992, I993a & h. 1994; Shea, 1988) and thé fossil record (Walker and Leakcy, 1978; Coppens, 1986; Simons, 1989; Coppens and Geraads, 1992) — there has never been a truly ail-round approach to Ihe subjcct. Current research into evolutionary concepts (Gould, 1985; Devillers & Chaline, 1993; Chaline. 1994) indicates that there is a hierarchized structure in thé living world and that thé relations among thé various levels of intégration are highly complex, ranging from close dependence to complète dissociation. CHAL1NE, DURAND. MARCHAND. DAMBRICOURT MALASSE and DCSHAYES 44 APES ANH AUSTRAL!

The aim of this paper is: from a double : (1) to critically review progress by analyzing two main levels of organization in cation), thé fir5 Hominoids: molecular and chromosomal; Pan and thé set (2) to put forward explanatory models of chromosomal and morphological évolution events looks li within a palaeoclimatic and paleoecological framework; îrichotomy, or (3) to test thé model using paleontological data. and thé seconc conspecific sub extant Homo sa 2- Evolution at thé molecular level

Research at thé molecular level (DNA and protein sequencing. DNA/DNA hybridiza- 3- Evolution al tion, mitochondrial DNA restriction mapping, protein electrophoresis and immunology, blood groupings, etc.) bas confirmed thé proximity between and thé hîgher apes, but 3.1 -Chro without conclusivcly scltling thc questions of kinship and thé splitting of thé différent branches. A major ac It is thé général consensus that cladistically thé chimpanzee groupe with Homo, then & Lejeune, 197 with thé gorilla and much further on with thé . Molecular cladistic classification Opinions c (Bailey et al., 1991, 1992; Goodman et al., 1994) places ail gréât apes and humans in thé thé chromosom same ()(Fig.l). Within this family, thé subfamily is divided or that alteratio into one for (Pongini) and another tribe for , and hu- thé phylogenic mans (Hominini). Gorillas are placed in thé subtribe Gorillina, while chimpanzees and hu- grams entail ac( mans form thé Hominina subtribe. rearrangement i Estimated divergence between higher based on thé ipY)-globin gène région thé next section combined with available nucleotide data ranges from 1.61 % (humans versus common chim- By contras panzees) to 3.52 % (orangutans versus humans and African gréât apes). Pan diverges from placing them in Gorilla by 1.84 % (Miyamoto et al., 1987, 1988), a figure similar to that obtained by DNA/ away from heter DNA hybridization analysis (Siblcy and Ahlquist, 1984, 1987; Caccone and PoweL 1989; (s il ver nitrate) t> Sibley et al., 1990). Broader investigation of thé \jrvi-globin gène région (Bailey et al., 1991) differs from thc and of thé (3-globin gène (Bailey et al., 1992; Perrin-Pecontal et al., 1992) confirms thé tures indicate fhï previous relationships and classification. The human-chimpanzee is corroborated by several other DNA séquence analyses 3.2 -A ne\e comm involving thé immunoglobin epsilon and alpha pseudogene (Ueda et al., 1989), 12S ribos- omal gène (Hixson and Brown, 1986), 28S ribosomal gènes (Gonzalez et ai., 1990), 0.9 kb by déduction. T région of thé mt génome containing gènes for tRNA His, tRNA Scr, tRNA Lcu and part of ND4 share a commor and ND5 (Hayasaka et al.. 19K8) and thé cytochrome oxidase II locus of mitochondrial gènes them. This is th (Pruvolo et al., 1991; Horai et al., 1992). Only DNA analysis of thc involucrin locus (Djian mosomal chang and Grccn. 1990) fails to confirm this clade, perhaps as a resuit of polymorphism. derived froni ar It should be noted that thé molecular analyses of chimpanzees were conducted on convergence. individuals labelled Pan troglodytes without specifying to which of thé three living sub- Wc can ait species — P. t. verus. P.t. troglodytes or P.t. schweinfurti — they belonged (M. Goodman, somcs and thé s Personal communication). Similarly for gorillas. This imprécision explains in part why kin- Among an ship is so difficult to specify, because divergence among thé three sub-specics is probably logically thé ont very différent from that with humans. which emigrate( We are in thé paradoxical and unfortunately increasingly common situation where thé million years (/ most sophisticated analytical techniques requiring very thorough expérimentation are applied stable from thé to samples chosen haphazardly! The population variability of thé study species is over- occurred since t looked, even though its temporal and paleobiogeographical distribution is often highly com- After thé st plex. extant gênera - Specialists generally accept that thé séparation of higher primates and humans results corresponds to APEii AMI) AUSTRALOFITHECINES OR1GINS 45 from a double split occurring very close together in time (M. Goodman personal communi- cation), thé first separating thé lineage to Gorilla from thé common ancestor of Homo and Pan and thé second separating thé lineages to Homo and Pan. Thèse two ancestral speciation events looks like a trichotomy. But Smouse and Li (1987) suggested there was a true tricholomy, or a pair of ordered dichotomies with a very short time span between thé first and thé second split. They take thé view that "thé ancestors of ail three taxa were still conspecific subséquent to thé second split, perhaps no more différent than thé major races of extant Homo sapiens". This is an interesting suggestion to which we shall return.

3- Evolution at thé chromosomal levé!

3.1 - Chromosomal data A major advance in chromosome research was thé development of R banding (Dutrillaux & Lejeune, 1971) and G banding techniques (Sumncr et al., 1971; Dutrillaux et al., 1971). Opinions differ about thé rôle of heterochromatin. Dutrillaux and his team consider that thé chromosome data from primates (Fig.2) provide no évidence either for positional effects or that altérations in heterochromatin influence gène expression. This idea is materialized at thé phylogenic level by two equally feasible dichotomie diagrams (Fig. 3). Thèse two dia- grams entail acceptance of three convergences or reversions, but a third diagram, where each rearrangement is regarded as unique, implies complex populational évolution as describcd in thé next section. By contrast, Stanyon and Chiareili (1982) argue that "gènes can be (1) repressed by placing them in, or near, blocks of heterochromatin, or (2) activated by a shift in their position away from heterochromatin régions". Thcy set gréât store by active régions detected by Ag-NOR (silver nitrate) type methods. This has repercussions for thé phylogeny shown in figure 4, which differs from thé hypothèses in figure 3. They conclude that common derived karyological fea- tures indicate that Gorilla and Pan share a common descent after thé divergence of Homo.

3.2 - A new trichotomic chromosomal model The common ancestral chromosome formula of ail thèse species can be reconstructed by déduction. The reconstruction is based on thé principle that if two, three or four species share a common chromosome, it is likely that some common ancestor transmitted it lo ail or them. This is thé simplesl relationship. We may also take thé view that two identical chro- mosomal changes occur in thé same way on thé same chromosome in two related species derived from an ancestral form. This is statistically far less likely, though it is possible as convergence. We can attempt to reconstruct thé chronology of thé formation of thé various chromo- somes and thc successive events that marked thé history of thé family (Chaline et al., 1991). Among anlhropoid apcs, thé group with thé most primitive chromosomal formula is logically thé one that branched off carliest in thé family history. This is thé orangutan group which emigrated to Asia where it has been eut off from thé African branch for more than 10 million years (Andrews & Cronin, 1982; Lipson & Pilbeam, 1982). It has been relatively stable from thc chromosomal point of view. only two new chromosome mutations having occurred since that time. After thé séparation of thé orangutan lineage, thé common ancestral lineage of thé three extant gênera — chimpanzees, gorillas and humans — remained in Africa. This phase corresponds to thé "common ancestor'" implied by genetic similarities. That there was a common ancestor is irrefutably shown by thé formation of seven spécifie mutanl chromo- (Collet, 1988) somes (2q. 3, 7, 10, 11, 17 & 20) and by thé rétention of clcven non-mutated common admit a plausib chromosomes (1, 4, 5, 8, 9, 12, 13, 14, 15, 16 & 18} inherited by thé three living species — thé pré (Chalineetal., 1991) (Fig. 5). day Lake Victi The occurrence of seven characleristic mutant chromosomes found in thé gorilla, chim- River in a fore: panzee and human descendants implies that thé common ancestor was a single monotypic — thé pré species, not divided into subspecies. Genetic pooling as a resuit of interbreeding produces a north of thé Za fairly even spread of chromosome variety, including chromosomal variations that appear in — thé pr isolated individuals. This first part of thé hislory of thé common ancestor corresponds to African Rift V; what we shall term thé "first homogcnous common ancestor phase" (Fig. 5). This thret Thereafter. thé common ancestor diversified and thé lineages separated, leading on thé forerunncrs of I one hand to thé gorilla and chimpanzee and on thé other to humans. This divergence raises a las of thé livint complex popularïonal problem about thé distribution of five new mutaled chromosomes. The pre-cl It is reported that chimpanzees and humans share three mutated chromosomes (2p, 7 & to interbreed \ 9) thaï gorillas do not hâve. Conversely, chimpanzees and gorillas share two other spécifie spread and are mulated chromosomes (12 & 16) not found in humans. In other words. chimpanzees share mans. three common mutated chromosomes wilh humans and two common mutated chromosomes Similarly, with gorillas. But gorillas share no spécial rearrangements with humans! As a resuit, thé Thîs position is inexplicable by thé standard hypothesis of a split into two branches thé chromosom, (dichotomie model) leading to thé gorilla/chimpanzee on one side and to humans on thé However, ] other. acquire mutatio Though there is a possible solution to thé puzzle: thé "second heterogcneous common This sugge ancestor phase" (Fig. 5). west Cameroon To explain this major paradox, it must be supposed that al a certain time in their history. thé pre-gorillas after thé tïrsf undilïerentiated phase, thé ancestors of chimpanzees and gorillas were able to This hypot interbrecd and acquire two new chromosome mutations they alone possessed, and not hu- advanced by Sn mans. This accords with thé suggestion of Smousc and Li (1987) "that thé ancestors of ail three taxa were still conspecific". 3.4 - Hypoi But iî must also be accepted that for sornc lime, perhaps différent from thé first period, This hypotl thé ancestors of chimpanzees and humans were able to interbreed and to incorporate three pre-gorillas and new chromosomal mutations into thcir genetic constitution, possessed by them alonc and not differentiated (F gorillas. form thé pré-ci However, thé facl that thé ancestors of gorillas and humans do not share exclusive australopitheciru mutations in their chromosomal formulas implies that they did not at that time hâve contacts in micc in Japai allowing hybridizalion. They were geographically isolated. tnusculus castai, Three hypothèses can be put forward, necessarily broken down into several phases and cannot be ruled i stages, summarized as follows: 3.5 - Hypot A not lier h y In thé first homogcnous common ancestor phase, thé ancestors of gorillas, chimpanzees common mutatk and humans formed a common undifferentiated monotypic ancestral group in which ail gorillas and pré- individuals could interbreed. There was a single common species, not yet identifiée in thé wise occurred in fossil record, and so nameless. lion seems sfatis In thé second heterogeneous common ancestor phase, thé ancestral group split into three model consistent subgroups. Probably into three subspecies as only subspecies could hâve retained thé ability to interbreed in thé areas where they came into contact and to pool their genetic héritage. We shall call them respectively pre-chimpanzecs, pre-gorillas and pre-hominians or pre- australopithecines. By comparison with thé geographical distribution of present-day species (Collet, 1988) (Kig. 6-7), which has probably not changed much over geological time, we can admit a plausible hypothcsis ahout thé distribution of thèse three subspecies as follows (Fig. 8): — thé pre-chimpanzee group must hâve been gcographically ccntred around thé présent day Lake Victoria région. It stretched to north west Africa across thé area north of thé Zaire River in a forest-savanna mosaic or open woodland environment. — thé pre-gorilla group must hâve been located on thé western edge of thé former, still north of thé Zaire River, in thé very wet tropical rain forest zone. — thé pre-hominian group musl hâve been located furthcr east in thé t'a mous East African Rift Valley, thé gréât crack in thé Earth's crust running north-south through Africa. This three-way division of thé common ancestor into three geographical subspecies, forerunners of thé three extant gênera, accounts for thé formation of thé chromosomal formu- las of thé living species by thé following scénario. The pre-chi-mpanzees were in contact in thé hast with thé pre-hominians and were able to interbreed with [hem. As a rcsult, Ihree chromosomal mutations occurred in this région, spread and are now found in thé common chromosomal héritage of chimpanzees and hu- mans. Similarly, thé pre-chimpanzees bordered on thé west with thé pre-gorillas and inlerbrcd. As a resuit, thé two chromosomal mutations occurring in thé common zone were included in thé chromosomal héritage of living goriilas and chimpanzees. However, pre-gorillas and pre-hominians had no contact at that time and were unable to acquire mutations common to both gênera. This suggests that thé pre-chimpanzee group was distributed in a wide arc from north west Cameroon to thé south of Lake Victoria, separating thé pre-hominians in thé east and thé pre-gorillas in thc west (Fig. 8). This hypothcsis is consistent with a true trichotomic model in compliance with thé ideas advanced by Smouse and Li (1987).

3.4 - Hypothesis 2 This hypothesis suggests that afterthe first common phase, two subspccies, respeclivclly, pre-gorillas and pre-australopithecines became geographically separated and chromosomally differentiated (Fig. 9). Only then. did two small populations of each subspecies meet and for m thé pre-chimpanzee stock! Chimpanzees could be hybrids of pre-gorillas and pre- australopithecines. A dichotomie model followed by genetic re-melding as has been reported in mice in Japan (Mus musculus molossinus results from thé two remixed subspecies Mus musculus castaneus and Mus tnu\cutus tnuscu/us) (Bonhomme et al, 1 984). A theory that cannot be ruled eut a ptioiil

3.5 - llypothesis 3 Another hypoîhesis may be envisaged, that of convergence. This would imply that two common mutations occurred at thé saine sites and on thé same chromosomes in both pre- gorillas and pre-chimpanzees. Moreover. three further identical chromosomal mutations like- wise occurred in pre-chimpanzee and pre-human chromosomes. Althougll possible, this solu- tion seems statistically less probable than thé previous one. It would be a double-dichotomie model consistent with thé results of Bailey et al. (1992) and Goodman et al. (1994). CHALINE. DURAND. MARCHAND. DAMBRICOURT MAt.ASSF. ;md DKSHAYKS APF.S AND AUSTR,

4- Evolution at thé ecological levcl: a climatological model

The model of trichotomic divergence also implies that at some point between 5 and 4 millions years ago thé three subspecies finally became three separate species. Either because new chromosomal mutations prevented them from interbreeding by abortion of hybrids or, more probably, because they had become geographically and ethologically isolated. Since this séparation, chimpanzees hâve acquired six chromosomal mutations (4c, 5, 9, 15, 17, 13) that they alone possess. Similarly, gonflas hâve six différent chromosomal mutations (1, 4b, 5, 17, 8, 10, 14) peculiar to their chromosomal make-up. As for thé pre-australopithecine and then human line, it acquired four spécifie chromo- somal mutations (2 mutations on chromosome 1, 2, 18), including thé l'amous fusion of thé two chromosomes tliat formed thé human chromosome 2. To account for thé séparation into distinct species. a new décisive factor must be incorporated hère, that of climatic change. This would hâve induced changes in thé environ- menl lhat must hâve been instrumental in thé geographical isolation of thé subspecies and species. Figure 8 explains thé logic behind thèse changes. The original common area in central Africa is currently a favoured climatic zone where thé inter-tropical front (east-west) corresponding to thé thermal and meteorological equator crosses thé inter-oceanic confluence (north-south) (Leroux, 1983). Very schematically we find thé permanent Atlantic monsoon domain and thé tropical rain tbrcst in thé west; thé forest is known in thé Congo, Gabon and Cameroon basins from thé onsel of Ihe Miocène (Boltenhagen et al., 1985). To thé north lies thé seasonal Atlantic monsoon domain and thé savannah; in Nigeria a seasonal subtropical climate is reported since thé Oligocène-Miocène boundary (Takashi & Jux, 1989). Further north still is Ihe Sahara zone; évidence of a large arid zone in North Africa i'rom Middle Miocène times is provided by rodents (Jaeger, 1975) and by flora (Boureau et. al.,1983). In thé south and east is thé domain of thé Indian Océan monsoons and trade winds; tropical rain forest, open woodlands and montane forests are recorded to hâve co-existed since 19 Myrs and savannahs since 14-12 Myrs (Bonnefille, 1987; Retallack et al-, 1990). Local reliefs are superimposed on this background pattem to form an environmental mosaicthat is sensitiveto climatic fluctuations (White, 1983; Pickford, 1990). Our hypothesis is that differentiation occurred in connection with thc environment as determined by climate (fig. 8). Starting from a monotypic common stock (acquisition of 7 chromosomal changes), thc pre-gorillas splil avvay in thé permanent monsoon domain north of thé Zaire River barrier. The pre-australopithecines developed on thé eastern margin under thé influence of thé Indian Océan monsoons and trade winds and spread north-south along thé inter-oceanic confluence which roughly coincides with thé eastern arm of thé rift valley (fig.8) and may be westward around thé permanent Atlantic monsoon range. The prc- chimpanzees spread widely east-west, on thé northern boundary of thé permanent Atlantic monsoon domain, ranging from Central to West Africa. This geographical pattern of climates underwent many large changes. First because Africa has drifted relative to thé equator which lay 5° further north about 10 Myr ago (Scotese et al, 1988). But also because of changes in atmospheric circulation. In thé Upper Miocène tropical north Africa experienced at Icast four épisodes ol substantial climatic détérioration leading to aridity, thé last at thé top of thé Miocène (ça. 6-5.3 Myrs) coinciding with a very distinct cooling of thé Atlantic (Diester-Haass & Chamley, 1982; Sarnthein et ai, 1982). Schematically, since Chudeau (1921) it has been accepted that extensions of thé arid APESAND AUSTRALOPITHECINESORIGIISS 49

Sahara zone are relatcd in part to a reduced summertime advance of thé monsoon front (FIT- 1; Fig. 8) which may even remain blocked in thé southern hémisphère. Such variations entailed changes in thé seasonal and permanent monsoon ranges and thus in thé three sub-species and could hâve separated them in a yet unknown history. Allopatric break up of thé ancestral form would hâve allowed gorillas, australopîthecines and chimpanzees to become isolated, as evidenced by thé autapomorphic features which hâve since appearcd. From thé Upper Pliocène (ça. 3.2 Myrs) général atmospheric circulation changed radi- cally for geodynamic reasons. Events such as thé closure of thé Panama isthmus, thé opening of thé Bering Straits and mountain building in North West America and Asia are thought to hâve been décisive factors in conjunction with variations in planetary orbit in triggering thé northern hémisphère ice âges (Ruddiman & Raymo, 1988; Berger, 1992). Each glacial period is related to aridily, Jn Africa north of thé equator (Chudeau, 1921; Tongiori & Trevisan, 1942; Dubief, 1953; Tricart, 1956). For more récent times where chronology is relatively précise, we now know that changes occur suddenly. After thé last glacial maximum it is thought that thé arid zone extended several hundred kilomètres furlhcr South on three occasions betwcen about 19,000 and 15,000 years 1JC B.P. with each épisode lasting only 500 to 1000 years (Durand, 1993). The dense humid forest became fragmented and mountain biotopes spread as a resuit of thé fall in températures (Maley, 1987). The répétition of thèse biogeographica! mechanisms during thé - fluctuations is thought lo be responsible for thé current diversification of chimpanzees and gorillas, each characterized by three sub-species. Starting from thé initial pre-chimpanzee distribution, it is thought that common chim- panzees then diversified into three suhspecies. One subspecies (Pan troglodytes verus) is isolated in Guinea (Collet, 1988; Fig. fi), probably as a resuit of a break in thé forest caused perhaps by a southward shift of thé Sahara désert zone in Quaternary times engendering aridity in what is now Nigeria. This mechanism of séparation of species into western and eastern populations may hâve becn compounded because thé prc-gorilla and pre-chimpanzee populations were unable to cross thé gréât natural barrier of ihe marshland basin of thé River Zaïre. Only thé pigmy ehimpanzee (Pan paniscus) made thé crossing or perhaps negotiated thé river upstream. It is impossible at présent to provide détails and a chronology of what might hâve happened, bul this mechanism is plausible. It can furthermore be tested, since if it is correct, fossils of pre- chimpanzees should be found in Tertiary deposits in areas where chimpanzees no longer occur from thé Ivory Coast to Nigeria. Kinally, gorillas also split from thé prc-gorilla stock into three subspecies, correspond- ing respectively to thé lowland and Ihe two mountain gorillas separated by thé bend in thé River Zaire (Collet, 1988) (Fig.8). Scarce Pre-hominians are known in thé fossil record (Lothagam, Lukeino, Ngorora) and are more or less unrelated. They can be considered as pre-australopithecines, one of thé components of Ihe common ancestor. This new model introduces australopithecines as a missing-link between thé common ancestor and thé human lineage proper. They are never considered by chromosome special- ists for thé obvious reason that, being extinct, their chromosomes are unknown. But as they formed a necessary intermediate stage, they must be included in thé model. By déduction, thé chromosomal formula of thé extinct pre-human form can be evaluated fairly accurately, except for thé four chromosomes that appeared after ils genetic isolation. 50 CHALINC. DURAND. MARCHAND. DAMBR1COURT MAI .ASSh and DESHAYES

The model ot'séparation into three gênera is therefore not simply one of divergence into two groups, as ordinarily occurs in thé world. Thcrc is a true trichotomy.

5- Tcsting with paleontological data

This model can be tested from a paleontological point of view, as it is for palaeontolo- gists to find thé ancestors, to date their appearance in thé fossil record and to reconstruct their history proper (Fig.H)). As said above, thé apc group with thé most primitive chrornosomal formula is logically thé orangutan group which emigrated to Asia where it has heen eut off from thé African Fig. 1 - The most branch for more than 10 million years. It is now accepted that Ramapiihecus and PTR: Pan traRludyt arc thé mâle a-n'd female of a single species related to orangutans (Andrews & Cronin, 1982; al., 19S7) Lipson & Pilbeam, 1982). Our morphological analysis (Chaline, 1994), suggests thé same is true of Ouranopiîhccus tnacedoniensis (Bonis and Melentis, 1977; Bonis et al., 1990) which has thé same facia! affinities with orangutans. After thé séparation of thé orangutan lineage, thé common ancestral lineage of thé three extant gênera remained in Africa. But fossil remains dating frorn 10 to 5 Myrs are vcry sparse. Only four finds hâve been made to date. Two molars from Lukeino and Ngorora PPY (Kenya) (Pickfbrd, 1975) and a fragment of jaw with a molar Lothagam, again in Kenya, PTR~ dated to 5,5 Myrs. The latest discoverv is thé most interesting, that of ramidus found by Whilc el al. (1994, 1995) in thé Pliocène of thé (Ethiopia) and dated to 4,4 Myrs. Most data about thé teeth (metric, morphology. enamcl thickness) and even fealures of thé cranium "evincing a strikingly chimpanzee-likc morphology" are very similar PPY- lo chimpanzee form ( ?), but also hâve australopithecinc characters. It may be that thèse fossils are of one of thé components of thé common ancestor - thé pre-chimpanzee or pre-australopithecine! PPY- The chrornosomal model described hère entails several anatomical implications that can be tested by . The first is thaï thé cranial and dental morphologies of thé three sub-species of thé common ancestor should be highly . The discovery of ramidus is fully consistent with this hypothesis and is a first favorable test. The second implication HSA- concerns thé shapc of thé pelvis. As gorillas and chimpanzees are quadrupeds and as is thé apomorphic feature characteristic of australopithecines and their human descendants, thé three components of thé common ancestor must therefore still hâve walked on ail fours. PPY HSA ACKNO\VU;DGMENTS — Wc arc indchtcd to thé anonymous revjewers and thé editor Bru nette Cliiarelli for hclpful criticism. commcnts and suggestions, and to M. Goodman for pcrsonal communications. This woik was supporled by thé Laboratoire de Paléontologie analytique' et Géologie sédimentaire du CNRS (UMR 5561; Université de Bourgogne. Dijon). We are also grateful to A. Bussicrc for thc drawings and lo C. Sulcliffc for help with PPY— translation.

PTR HSA~ APES AND AUSTRALOPITHECINF.S OKIGINS

trqglodytes Hominini Gorzlla gorïlla ~\i

Tig. I - The most parsimoniou.s arrange me ni of ihe séquence dala of PPY: Pongo pygmneits; GGO: Gorilia gorilla; PTR: Pan troglodytes; HSA: Homo sapiens. Branch lenj-ths based only un unambiguuus thanges (afler Mivamoto cl al., 19K7)

HSA GGO PPY_ PPY_ GGO -PTR PTR HSA PTR - HSA -PPA PPY- -GGO h" 10 2 PPY PTR HSA" "GGO PTR 12 3 11 HSA PPY GGO -PTR HSA 13 15 ^-PPY PTR 4 ^-o^. ^GGO PPY •GGO HSA~ 16 ^--GGO PPY ^**~ HSA HSA s ^~o-. PTR 17 GGO PPA PPY PPY- PTR HSA GGO HSA PTR 18 PPY PTR -GGO HSA 20 PTR 8 14 HSA GGO

Fig. 2 - Companson of chromosomal mutations in orangutan, gorilla, chimpanzee and man. l'I'Y: l'onga pygmaeus; GGO: Gorilia gorilla; PTR: Pan troglodytes; HSA: Homo xapiens. White dois: pcriccntric inversion; black dots: paraccntric inversion: triangles: gain in hctcrochromalinc: bïack squares: rcciprocal or terminal-terminal translocation (afler Dulrillaux and Couturier. I9S6). CIIALINE. DURAND, MARCHAND, DAMBRICOURT MAI.ASSK and DESHAYCS APES AND AUSTRALOPm-

PTR PPY (S) PI GGO -PPA

Pa3* PPY !! s r O ^

a —f\ — • — i HSA

GGO PTR PPA Pa Pa Pa.

HSA

PTR GGO PPA

HSA

Fig. 3 - Threc models explaining thé distribution of mulaled chromosomes in orangutans, gorîllas. chimpanzees and humans. a - common mulalions vicwed as convergence in GGO and PTR; b - commnn mutations vie\ved as conver- gence in PTR and HSA; c - individual population évolution. PPY: Pongo pygtnaeu.r, GGO: GoiïIIu gorillct; PTR: Pan trogiodyte\\: Pan paniscits; HSA: Homo supcns. White dots: pcricentric inversion; black dots: paraccnlrîc inversion; triangles: gain in helerochromaiine; hlack squares: reciprucal or terminal-terminal transiocation (after Dutrillaux and Couturier, 1986). APES AND AUSTRALOPITHECINES ORICINS 53

PPY (S) PPY (B) GGO PTR PPA HSA

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l-ig.-l - Chromosoiiial phylogeny for thé llominoidea. Cx: complex change; De: delerion; Pa: paracentric inversion: Pc: pericentric inversion; 5-McC: 5-methyI-cytosine. PPY: Ptiiiga pygmaeus (S: Sumatra; B: Bornéo); GGO: Gorillti gorillu: PTR: Pan troglodytes: PPA: l'an /Hmr.svuv; HSA: Homo sapiens, (aftcr Stanyon and Chiarelli, ]9S1). 2 *"* 2 ?ï~ •^ 2 '£ g i 3 £ <£ &. ri ,_ 3 ,^ § ;r , r"g » o ^ "9. -4 =- H phase 1 phase 2 polytypic phase 3 II CI3 7T ^ r, =T. -1 2. 3 o — — o -1 n monotyplc 3 subspecies of distinct species 0 - =r '-< ~3 - ? oCL sn- «- -2_; =r£ qS 4, o;i 3 i: -> D w 3~ 3 tfl ^Srew^fîon" n ci = ri Q. n SP g^w^odn * t."5 K ~"f œ3r )1 1 r ^""£-""2n"- o »*MU ^ " / S* p* W3^,.'X^^3 3 ' l S g g pre-gorttla •-• S "rt 5' 5" 3 3 - o ï; en n ?v* tro 5 S s ai i à £' -. -• § °- p s » ta 5 As irS S s tr s?-3D"5E.3 w P en rgft§ 1 Ë. & * f » S g > i-> CB ff L^- A U1 Oy,^, OJ- V] S" 3~. R?3 = o^ hj . 3 a. G -• - hJ 1 /« "^"•^0^"=' A? to a S / M H> «• ï "" 7 | "g- S g "' n jre-chtmpanzee td 0, i tt * ^.5^-ë-jw-S! O JO gA i ff W M (râ:?S2-ë§-ëB t> o W 5?-o^2oS"- "^ - rt- M 3-S3'3o;D. = 9 O « ^ ^ a " ta yj g_ — i Q ^ rï CR >1 a § 3* S* \

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Fig.G - Distribution of thé thrce sub-species of common chimpanzees. The western-most sub-species, thé black chim- panzee (Pan troglodytes l'crus). inhabits (iuinea while ihe other arc found norlh ot Ihe River Zaïre (or Congo): ihc typicat common cliimpan/.ee (Pan troglodytes troglodyte^ in thé wesl in Congo, Gabon, T.quaiorial Cîuînea and Camcroon ;ind Schweinîïirl'5 cliinipanxee (Pan troglodytes \chweinfunhi) furtlier ea^l in northcrn /aire (at'ler Collet,

Fie.7 - Distribution of thé ihree but>-spccics ot gorillas. Oorillas are divided inlo western lowland gorillas (Coi-'illu L'onllti goiiHn) in Congo, Gabon, Equalonal Guinea and southern Cameroon and eastcrn mountam «orillas (GurUta gonllu graiit'fi (Burundi and Rwanda). A third sub-species, thé mountain goi'illa ol' Rwanda and Ijgand.i (Gnritlti t>orilla hcringri) is in danger of imminent extinction (al'ter Collet, 19XS). CHALINE. DURAND. MARCHAND. DAMBRICOURT MAI.ASSÉ and DESHAYES APKS AND AUSTRAI.OP1T

Fig.K - Distribution of thé tommon ancestor at thé start of thé polytypic phase, Prc-gorillas must hâve occupied (he wel Atlantic monsoon zone (dense foresl), prc-chi m pansées thé less rmmid Atlantic monsoon zone (open foresl} and pré- australopithccines thé Indian Océan monsuons zone (accacta savannah). 1: Sumnier; 2: Wmtcr; thick solid line: Inter Tropical Front; pointed line: Inier Oceanie Confluence.

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