HAL Id: halshs-00426146 https://halshs.archives-ouvertes.fr/halshs-00426146 Submitted on 23 Oct 2009 HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci- entific research documents, whether they are pub- lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés. Chromosomes and the origins of Apes and Australopithecines Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé, M.J. Deshayes To cite this version: Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé, M.J. Deshayes. Chromo- somes and the origins of Apes and Australopithecines. Human Evolution, Springer Verlag, 1996, 11 (1), pp.43-60. halshs-00426146
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HAL Id: halshs-00426146https://halshs.archives-ouvertes.fr/halshs-00426146
Submitted on 23 Oct 2009
HAL is a multi-disciplinary open accessarchive for the deposit and dissemination of sci-entific research documents, whether they are pub-lished or not. The documents may come fromteaching and research institutions in France orabroad, or from public or private research centers.
L’archive ouverte pluridisciplinaire HAL, estdestinée au dépôt et à la diffusion de documentsscientifiques de niveau recherche, publiés ou non,émanant des établissements d’enseignement et derecherche français ou étrangers, des laboratoirespublics ou privés.
Chromosomes and the origins of Apes andAustralopithecines
Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé,M.J. Deshayes
To cite this version:Jean Chaline, Alain Durand, Didier Marchand, Anne Dambricourt Malassé, M.J. Deshayes. Chromo-somes and the origins of Apes and Australopithecines. Human Evolution, Springer Verlag, 1996, 11(1), pp.43-60. �halshs-00426146�
J. ChalineA. DurandD. MarchandPaléontologie analytique et Géologiesédimeniuire (UMR CNRS H5561)et Préhistoire et Paléoécologiedu Quaternaire de i'EPHE,Université de Bourgogne,Centre des Sciences de la Terre,6 bd. Gabriel, 21000 Dijon, Franc?
A. Dambricourt MalasséUMR CNRS 9948, InMiiut dePaléontologie humaine,/ rue R. Panhard,75013 Paris, France
M. J. DeshayesRue Pasteur, J814000 Caen, France
Chromosomes and thé originsof Apes and Australopithecines
Comparison of molecular data suggests that thé higher apes (Go-rilla. Pan) and humank ind (Homo) are closely relatcd and thatthey divergcd from thé common ancestor through two speciationevents situated vcry closely togcther in l ime. Examinat ion of Ihechromosomal formulas of thé l i v in g species reveals a paradox inthé distr ibution of mutated chromosomes which can only be re-solved by a model of trichotomic diversif ication. This new modelof divergence from thé common ancestor is characterizcd by thétransi t ion from (1) a monotypic phase to (2) a polytypic phase ofthrec sub-species - p re -go r i l l a, pre-chimpanzee and prc-australopilhecine. The quadruped ancestors of Australoptthecusappear to hâve been one of thé Huée components of (ne commonancestor. The question is whcther ramidus îs an australopilhecineor a pre-australopithecine représentative of thé common ancestor.The new model of diversif ication of thé common ancestor isrcsituatcd in thc paleogeographic and paleoclimatic context which,through Ihe norlh-south pattern of extension of ar idi ty. provides acohérent scénario for thé formation of ex(ant species and sub-species of thé Corilla and Pan gênera.
1. Introductio n
Research into hominoid évolution involves mul t ip le discipl ines. 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 (Chiarell i. 1962; De Grouchy et al.,1972; Dutr i l laux et al., 1986; Dutr i l laux & Couturier, 1986; Stanyon and Chiarell i, 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 trulyail-round approach to Ihe subjcct. Current research into evolut ionary concepts (Gould, 1985;Devillers & Chaline, 1993; Chaline. 1994) indicates that there is a hierarchized structure inthé l i v in g world and that thé relations among thé various levels of intégration are h igh lycomplex, ranging from close dependence to complète dissociation.
44 CHAL1NE, DURAND. MARCHAND. DAMBRICOURT MALASSE and DCSHAYES APES ANH AUSTRAL!
The aim of this paper is:(1) to crit ical ly review progress by analyzing two main levels of organization in
Hominoids: molecular and chromosomal;(2) to put forward explanatory models of chromosomal and morphological évolution
with i n a palaeoclimatic and paleoecological framework;(3) to test thé model using paleontological data.
2- Evolution at thé molecular level
Research at thé molecular level (DNA and protein sequencing. DNA/DNA hybridiza-tion, mitochondrial DNA restriction mapping, protein electrophoresis and immunology, bloodgroupings, etc.) bas confirmed thé proximity between humans and thé hîgher apes, butwithout conclusivcly scltling thc questions of kinship and thé splitt ing of thé différent branches.
I t is thé général consensus that cladistically thé chimpanzee groupe wi t h Homo, thenwith thé gorilla and much further on with thé orangutan. Molecular cladistic classification(Bailey et al., 1991, 1992; Goodman et al., 1994) places ail gréât apes and humans in thésame family (Hominidae)(Fig.l). Within this family, thé subfamily Homininae is dividedinto one tribe for orangutans (Pongini) and another tribe for gorillas, chimpanzees and hu-mans (Hominini). Gorillas are placed in thé subtribe Gori l l ina, whi le chimpanzees and hu-mans form thé Hominina subtribe.
Estimated divergence between higher primates based on thé ipY)-globin gène régioncombined with available nucleotide data ranges from 1.61 % (humans versus common chim-panzees) to 3.52 % (orangutans versus humans and African gréât apes). Pan diverges fromGorilla by 1.84 % (Miyamoto et al., 1987, 1988), a figure simi lar to that obtained by DNA/DNA hybridization analysis (Siblcy and Ahlquist, 1984, 1987; Caccone and PoweL 1989;Sibley et al., 1990). Broader investigation of thé \jrvi-globin gène région (Bailey et al., 1991)and of thé (3-globin gène (Bailey et al., 1992; Perrin-Pecontal et al., 1992) confirms théprevious relationships and classification.
The human-chimpanzee clade is corroborated by several other DNA séquence analysesinvolving 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 kbrégion of thé mt génome containing gènes for tRNA His, tRNA Scr, tRNA Lcu and part of ND4and ND5 (Hayasaka et al.. 19K8) and thé cytochrome oxidase I I locus of mitochondrial gènes(Pruvolo et al., 1991; Horai et al., 1992). Only DNA analysis of thc involucr in locus (Djianand Grccn. 1990) fai l s to confirm this clade, perhaps as a resuit of polymorphism.
It should be noted that thé molecular analyses of chimpanzees were conducted onindiv iduals labelled Pan troglodytes without specifying to which of thé three l iv in g sub-species — P. t. verus. P.t. troglodytes or P.t. schweinfurti — they belonged (M. Goodman,Personal communication). Similarly for gorillas. This imprécision explains in part why k in-ship is so di f f icul t to specify, because divergence among thé three sub-specics is probablyvery différent from that w i t h humans.
We are in thé paradoxical and unfortunately increasingly common situation where thémost sophisticated analytical techniques requiring very thorough expérimentation are appliedto samples chosen haphazardly! The population var iabi l i ty of thé study species is over-looked, even though its temporal and paleobiogeographical distr ibut ion is often highly com-plex.
Specialists generally accept that thé séparation of higher primates and humans results
from a double :cation), thé fir 5Pan and thé setevents looks l iî r ichotomy, orand thé seconcconspecific subextant Homo sa
3- Evolution al
3.1 -ChroA major ac
& Lejeune, 197Opinions c
thé chromosomor that alteratiothé phylogenicgrams entail ac(rearrangement ithé next section
By contrasplacing them inaway from heter(s i l ver nitrate) t>differs from thctures indicate fhï
3.2 -A ne\e comm
by déduction. Tshare a commorthem. This is thmosomal changderived froni arconvergence.
Wc can aitsomcs and thé s
Among anlogically thé ontwhich emigrate(m i l l i o n years (/stable from théoccurred since t
After thé stextant gênera -corresponds to
APEii A M I ) AUSTRALOFITHECINES OR1GINS 45
from a double spl it occurring very close together in time (M. Goodman personal communi-cation), thé first separating thé lineage to Gorilla from thé common ancestor of Homo andPan and thé second separating thé lineages to Homo and Pan. Thèse two ancestral speciationevents looks lik e a trichotomy. But Smouse and Li (1987) suggested there was a truetricholomy, or a pair of ordered dichotomies with a very short time span between thé firstand thé second split. They take thé view that "thé ancestors of ail three taxa were sti llconspecific subséquent to thé second split, perhaps no more différent than thé major races ofextant Homo sapiens". This is an interesting suggestion to which we shall return.
3- Evolution at thé chromosomal levé!
3.1 - Chromosomal dataA major advance in chromosome research was thé development of R banding (Dutril laux
& Lejeune, 1971) and G banding techniques (Sumncr et al., 1971; Dutr i l laux et al., 1971).Opinions differ about thé rôle of heterochromatin. Dutr i l laux and his team consider that
thé chromosome data from primates (Fig.2) provide no évidence either for positional effectsor that altérations in heterochromatin influence gène expression. This idea is materialized atthé 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 eachrearrangement is regarded as unique, implies complex populational évolution as describcd inthé next section.
By contrast, Stanyon and Chiarei li (1982) argue that "gènes can be (1) repressed byplacing them in, or near, blocks of heterochromatin, or (2) activated by a shift in their positionaway 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, whichdiffers 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 modelThe 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 speciesshare a common chromosome, it is l ike l y that some common ancestor transmitted it lo ail orthem. 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 speciesderived from an ancestral form. This is statistically far less l ikely , though it is possible asconvergence.
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 islogically thé one that branched off carliest in thé fami ly history. This is thé orangutan groupwhich emigrated to Asia where it has been eut off from thé African branch for more than 10m i l l i o n years (Andrews & Cronin, 1982; Lipson & Pilbeam, 1982). It has been relat ivelystable from thc chromosomal point of view. only two new chromosome mutations havingoccurred since that time.
After thé séparation of thé orangutan lineage, thé common ancestral lineage of thé threeextant gênera — chimpanzees, gorillas and humans — remained in Africa. This phasecorresponds to thé "common ancestor'" implied by genetic similarities. That there was a
common ancestor is i rrefutably shown by thé formation of seven spécifie mutanl chromo-somes (2q. 3, 7, 10, 11, 17 & 20) and by thé rétention of clcven non-mutated commonchromosomes (1, 4, 5, 8, 9, 12, 13, 14, 15, 16 & 18} inherited by thé three l iv in g species(Cha l inee ta l ., 1991) (Fig. 5).
The occurrence of seven characleristic mutant chromosomes found in thé gorilla, chim-panzee and h u m an descendants implies that thé common ancestor was a single monotypicspecies, not div ided into subspecies. Genetic pooling as a resuit of interbreeding produces afa i r l y even spread of chromosome variety, inc lud ing chromosomal variations that appear inisolated indiv iduals. This first part of thé hislory of thé common ancestor corresponds towhat we shall term thé "first homogcnous common ancestor phase" (Fig. 5).
Thereafter. thé common ancestor diversified and thé lineages separated, leading on théone hand to thé gor i l l a and chimpanzee and on thé other to humans. This divergence raises acomplex popularïonal problem about thé d is t r ibut ion of fiv e new mutaled chromosomes.
I t is reported that chimpanzees and humans share three mutated chromosomes (2p, 7 &9) thaï gorillas do not hâve. Conversely, chimpanzees and gorillas share two other spécifiemulated chromosomes (12 & 16) not found in humans. In other words. chimpanzees sharethree common mutated chromosomes wi l h humans and two common mutated chromosomeswit h gorillas. But gorillas share no spécial rearrangements with humans!
Thîs position is inexplicable by thé standard hypothesis of a spl it into two branches(dichotomie model) leading to thé gorilla/chimpanzee on one side and to humans on théother.
Though there is a possible solution to thé puzzle: thé "second heterogcneous commonancestor phase" (Fig. 5).
To explain th is major paradox, i t must be supposed that al a certain t ime in their history.after thé tïrsf undilïerentiated phase, thé ancestors of chimpanzees and gorillas were able tointerbrecd and acquire two new chromosome mutations they alone possessed, and not hu-mans. This accords w i t h thé suggestion of Smousc and Li (1987) "that thé ancestors of a ilthree taxa were st i l l conspecific".
But iî must also be accepted that for sornc l ime, perhaps différent from thé first period,thé ancestors of chimpanzees and humans were able to interbreed and to incorporate threenew chromosomal mutat ions into thc ir genetic constitution, possessed by them alonc and notgorillas.
However, thé facl that thé ancestors of gorillas and humans do not share exclusivemutations in their chromosomal formulas implies that they did not at that time hâve contactsal lowing hybr id izal ion. They were geographically isolated.
Three hypothèses can be put forward, necessarily broken down into several phases andstages, summarized as follows:
In thé f i rst homogcnous common ancestor phase, thé ancestors of gori l las, chimpanzeesand humans formed a common undi f ferent ia ted monotypic ancestral group in which aili nd i v i dua ls could interbreed. There was a s ingle common species, not yet identif iée in théfossil record, and so nameless.
I n thé second heterogeneous common ancestor phase, thé ancestral group spl it in to threesubgroups. Probably i n to three subspecies as only subspecies could hâve retained thé ab i l i tyto interbreed in thé areas where they came into contact and to pool their genetic héritage. Wesha ll call them respect ively pre-chimpanzecs, pre-gori l las and pre-homin ians or pre-australopi thecines. By comparison w i t h thé geographical d is t r ibut ion of present-day species
(Collet, 1988)admit a plausib
— thé préday Lake VictiRiver in a fore:
— thé prénorth of thé Za
— thé prAfrican Rif t V;
This thretforerunncrs of Ilas of thé l i v i n t
The pre-clto interbreed \spread and aremans.
S imi la r l y,As a resuit, théthé chromosom,
However, ]acquire mutat io
This suggewest Cameroonthé pre-gorillas
This hypotadvanced by Sn
3.4 - HypoiThis hypotl
pre-gorillas anddif ferent iated (Fform thé pré-ciaustralopi theciruin micc in Japaitnusculus castai,cannot be ruled i
3.5 - HypotA not lier h y
common mutatkgoril las and pré-wise occurred inl io n seems sfatismodel consistent
(Collet, 1988) (Kig. 6-7), which has probably not changed much over geological t ime, we canadmit a plausible hypothcsis ahout thé distr ibution of thèse three subspecies as follows (Fig. 8):
— thé pre-chimpanzee group must hâve been gcographically ccntred around thé présentday Lake Victoria région. I t stretched to north west Afric a across thé area north of thé ZaireRiver in a forest-savanna mosaic or open woodland environment.
— thé pre-gorilla group must hâve been located on thé western edge of thé former, st i llnorth 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 EastAfrican Rif t Valley, thé gréât crack in thé Earth's crust runn ing 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 l i v i n g species by thé fol lowing scénario.
The pre-chi-mpanzees were in contact in thé hast with thé pre-hominians and were ableto interbreed wi t h [hem. As a rcsult, Ihree chromosomal mutat ions occurred in this région,spread and are now found in thé common chromosomal héritage of chimpanzees and hu-mans.
Similar ly, thé pre-chimpanzees bordered on thé west wi t h thé pre-gorillas and inlerbrcd.As a resuit, thé two chromosomal mutations occurring in thé common zone were included inthé chromosomal héritage of l i v in g goriilas and chimpanzees.
However, pre-gorillas and pre-hominians had no contact at that t ime and were unable toacquire mutat ions common to both gênera.
This suggests that thé pre-chimpanzee group was distributed in a wide arc from northwest Cameroon to thé south of Lake Victoria, separating thé pre-hominians in thé east andthé pre-gorillas in thc west (Fig. 8).
This hypothcsis is consistent with a true trichotomic model in compliance with thé ideasadvanced by Smouse and Li (1987).
3.4 - Hypothesis 2This hypothesis suggests that afterthe first common phase, two subspccies, respeclivclly,
pre-gorillas and pre-australopithecines became geographically separated and chromosomallydifferentiated (Fig. 9). Only then. did two small populations of each subspecies meet andfor 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 reportedin mice in Japan (Mus musculus molossinus results from thé two remixed subspecies Musmusculus castaneus and Mus tnu\cutus tnuscu/us) (Bonhomme et al, 1 984). A theory thatcannot be ruled eut a ptioiil
3.5 - llypothesis 3Another hypoîhesis may be envisaged, that of convergence. This would imp ly that two
common mutat ions occurred at thé saine sites and on thé same chromosomes in both pre-gorillas and pre-chimpanzees. Moreover. three fur ther ident ical chromosomal mutations l ike-wise occurred in pre-chimpanzee and pre-human chromosomes. Althougll possible, th is solu-tion seems statist ical ly less probable than thé previous one. It would be a double-dichotomiemodel consistent with thé results of Bailey et al. (1992) and Goodman et al. (1994).
CHALINE . DURAND. MARCHAND. DAMBRICOURT MAt.ASSF. ;md DKSHAYK S 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 4mi l l ion s years ago thé three subspecies f inal l y became three separate species. Either becausenew 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 l ine, it acquired four spécifie chromo-somal mutations (2 mutations on chromosome 1, 2, 18), inc luding thé l'amous fusion of thétwo chromosomes tliat formed thé human chromosome 2.
To account for thé séparation into distinct species. a new décisive factor must beincorporated 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 andspecies. Figure 8 explains thé logic behind thèse changes.
The original common area in central Africa is currently a favoured cl imatic zone wherethé inter-tropical front (east-west) corresponding to thé thermal and meteorological equatorcrosses thé inter-oceanic confluence (north-south) (Leroux, 1983). Very schematically wefind thé permanent Atlantic monsoon domain and thé tropical rain tbrcst in thé west; théforest 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 At lant ic monsoon domain and thésavannah; in Nigeria a seasonal subtropical climate is reported since thé Oligocène-Miocèneboundary (Takashi & Jux, 1989). Further north st i l l is Ihe Sahara zone; évidence of a largearid zone in North Afric a 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 Océanmonsoons and trade winds; tropical rain forest, open woodlands and montane forests arerecorded 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 toform an environmental mosaicthat is sensitiveto climatic fluctuations (White, 1983; Pickford,1990).
Our hypothesis is that d i f ferent iat ion occurred in connection with thc environment asdetermined by cl imate (fig. 8). Starting from a monotypic common stock (acquisition of 7chromosomal changes), thc pre-gorillas splil avvay in thé permanent monsoon domain northof thé Zaire River barrier. The pre-australopithecines developed on thé eastern margin underthé inf luence of thé Indian Océan monsoons and trade winds and spread north-south alongthé inter-oceanic confluence which roughly coincides with thé eastern arm of thé rif t val ley(fig.8) and may be westward around thé permanent At lant ic monsoon range. The prc-chimpanzees spread widely east-west, on thé northern boundary of thé permanent At lant icmonsoon domain, ranging from Central to West Africa.
This geographical pattern of climates underwent many large changes. First becauseAfric a 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 UpperMiocène tropical north Afric a experienced at Icast four épisodes ol substantial climaticdétérioration leading to ar id i ty, thé last at thé top of thé Miocène (ça. 6-5.3 Myrs) coincidingwit h a very dist inct 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 andthus 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, australopîthecinesand chimpanzees to become isolated, as evidenced by thé autapomorphic features which hâvesince appearcd.
From thé Upper Pliocène (ça. 3.2 Myrs) général atmospheric circulat ion changed radi-cally for geodynamic reasons. Events such as thé closure of thé Panama isthmus, thé openingof thé Bering Straits and mountain building in North West America and Asia are thought tohâve been décisive factors in conjunction with variations in planetary orbit in triggering thénorthern hémisphère ice âges (Ruddiman & Raymo, 1988; Berger, 1992). Each glacial periodis 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 changesoccur suddenly. After thé last glacial maximum it is thought that thé arid zone extendedseveral hundred kilomètres furlhcr South on three occasions betwcen about 19,000 and15,000 years 1JC B.P. with each épisode lasting only 500 to 1000 years (Durand, 1993). Thedense humid forest became fragmented and mountain biotopes spread as a resuit of thé fall intempératures (Maley, 1987).
The répétition of thèse biogeographica! mechanisms dur ing thé Pliocene-Pleistocenefluctuations is thought lo be responsible for thé current diversification of chimpanzees andgorillas, each characterized by three sub-species.
Starting from thé init ial pre-chimpanzee distribution, i t is thought that common chim-panzees then diversified into three suhspecies. One subspecies (Pan troglodytes verus) isisolated in Guinea (Collet, 1988; Fig. fi) , probably as a resuit of a break in thé forest causedperhaps by a southward shift of thé Sahara désert zone in Quaternary times engenderingaridity in what is now Nigeria.
This mechanism of séparation of species into western and eastern populations may hâvebecn compounded because thé prc-gorilla and pre-chimpanzee populations were unable tocross thé gréât natural barrier of ihe marshland basin of thé River Zaïre. Only thé pigmyehimpanzee (Pan paniscus) made thé crossing or perhaps negotiated thé river upstream. It isimpossible at présent to provide détails and a chronology of what might hâve happened, bulthis 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 longeroccur from thé Ivory Coast to Nigeria.
Kinal ly , 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 théRiver Zaire (Collet, 1988) (Fig.8).
Scarce Pre-hominians are known in thé fossil record (Lothagam, Lukeino, Ngorora) andare more or less unrelated. They can be considered as pre-australopithecines, one of thécomponents of Ihe common ancestor.
This new model introduces australopithecines as a missing-l ink between thé commonancestor 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 theyformed a necessary intermediate stage, they must be included in thé model. By déduction, théchromosomal formula of thé extinct pre-human form Australopithecus can be evaluatedfai r l y accurately, except for thé four chromosomes that appeared after il s genetic isolation.
50 CHALINC. DURAND. MARCHAND. DAMBR1COURT MA I .ASSh and DESHAYES
The model ot'séparation into three gênera is therefore not s imply one of divergence intotwo groups, as ordinarily occurs in thé animal 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 theirhistory proper (Fig.H)).
As said above, thé apc group wi t h thé most primit ive chrornosomal formula is logicallythé orangutan group which emigrated to Asia where it has heen eut off from thé Africanbranch for more than 10 mi l l io n years. It is now accepted that Ramapiihecus and Sivapithecusarc thé mâle a-n'd female of a single species related to orangutans (Andrews & Cronin, 1982;Lipson & Pilbeam, 1982). Our morphological analysis (Chaline, 1994), suggests thé same istrue of Ouranopiîhccus tnacedoniensis (Bonis and Melentis, 1977; Bonis et al., 1990) whichhas thé same facia! af f in i t ies with orangutans.
After thé séparation of thé orangutan lineage, thé common ancestral lineage of thé threeextant gênera remained in Africa. But fossil remains dating frorn 10 to 5 Myrs are vcrysparse. Only four f inds hâve been made to date. Two molars from Lukeino and Ngorora(Kenya) (Pickfbrd, 1975) and a fragment of jaw with a molar Lothagam, again in Kenya,dated to 5,5 Myrs. The latest discoverv is thé most interesting, that of Ardipithecus ramidusfound by Whilc el al. (1994, 1995) in thé Pliocène of thé Middle Awash (Ethiopia) and datedto 4,4 Myrs. Most data about thé teeth (metric, morphology. enamcl thickness) and evenfealures of thé cranium "evincing a s t r ik ing ly chimpanzee-l ikc morphology" are very s imi larlo chimpanzee form (Bonobo ?), but also hâve australopithecinc characters. It may be thatthèse fossils are of one of thé components of thé common ancestor - thé pre-chimpanzee orpre-australopithecine!
The chrornosomal model described hère entails several anatomical implications that canbe tested by paleontology. The first is thaï thé cranial and dental morphologies of thé threesub-species of thé common ancestor should be highly simian. The discovery of ramidus isfu l l y consistent with th is hypothesis and is a first favorable test. The second implicationconcerns thé shapc of thé pelvis. As gorillas and chimpanzees are quadrupeds and as bipedalismis thé apomorphic feature characteristic of australopithecines and their human descendants,thé three components of thé common ancestor must therefore st i l l hâve walked on ail fours.
ACKNO\VU;DGMENTS — Wc arc indchtcd to thé anonymous revjewers and thé editor Bru nette Cliiarelli for hclpfulcriticism. commcnts and suggestions, and to M. Goodman for pcrsonal communications. This woik was supporledby thé Laboratoire de Paléontologie analytique' et Géologie sédimentaire du CNRS (UMR 5561; Université deBourgogne. Dijon). We are also grateful to A. Bussicrc for thc drawings and lo C. Sulcliffc for help withtranslation.
Fig. 1 - The most
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CIIALINE. DURAND, MARCHAND, DAMBRICOURT MAI.ASSK and DESHAYCS APES AND AUSTRALOPm-
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Fie.7 - D i s t r i bu t i on of thé ihree but>-spccics ot gori l las. Oori l las are divided in lo western lowland gori l las (Coi-'illuL'onllti goiiHn) in Congo, Gabon, Equalonal Guinea and southern Cameroon and eastcrn mountam «orillas (GurUtagonllu graiit'fi (Burundi and Rwanda). A third sub-species, thé mounta in goi' i l l a ol' Rwanda and Ijgand.i (Gnritltit>orilla hcringri) is in danger of imminent ext inct ion (al'ter Collet, 19XS).
CHALINE. DURAND. MARCHAND. DAMBRICOURT MAI.ASSÉ and DESHAYES APKS AND AUSTRAI.OP1T
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Recchvfi Nm-ember 3, 1V95 Accepted April 25, 7996
M. L. A. HamR. A. FoleyHominid EvolulionaryResearch GroupDepartment ofBîologiiAnthropologyDowning Street, Camb<3DZ, U.K.
Kcy words: Hominid elongevity, Australopilhbody weighl, brain siztlif e history.
Introduction
Lif e history théterns, and ihe underltion of hominid evoliMcHcnry(1994)atteing thé values of vaestimâtes. While supwe would l i k e to piparameters. In partiesignificance of extentance of selecling thidatabases in making
Lif e history théévolution can and olparticular stages in ttion and longevity rcomponent is that li ftwo structural variât1981; Peters, 1983; <Harvey éta l ., 1987;body size altow lif e \. Thiis in th
