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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�
I1UMAN EVOLUTION
J. Chaline A. Durand D. Marchand
Paléontologie analytique et Géologie sédimeniuire (UMR CNRS H5561) et Préhistoire et Paléoécologie du Quaternaire de i'EPHE, Université de Bourgogne, Centre des Sciences de la Terre, 6 bd. Gabriel, 21000 Dijon, Franc?
A. Dambricourt Malassé
UMR CNRS 9948, InMiiut de Paléontologie humaine, / rue R. Panhard, 75013 Paris, France
M. J. Deshayes
Rue Pasteur, J8 14000 Caen, France
Chromosomes and thé origins of Apes and Australopithecines
Comparison of molecular data suggests that thé higher apes (Go- rilla. Pan) and h u m a n k i n d (Homo) are closely relatcd and that they divergcd from thé common ancestor through two speciation events situated vcry closely togcther in lime. E x a m i n a t i o n of Ihe chromosomal formulas of thé l i v i n g species reveals a paradox in thé distribution of mutated chromosomes which can only be re- solved by a model of trichotomic diversification. This new model of divergence from thé common ancestor is characterizcd by thé transition from (1) a monotypic phase to (2) a polytypic phase of t h r e c sub-species - p r e - g o r i l l a , p r e - c h i m p a n z e e and prc- australopilhecine. The quadruped ancestors of Australoptthecus appear to hâve been one of thé Huée components of (ne common ancestor. The question is whcther ramidus îs an australopilhecine or a pre-australopithecine représentative of thé common ancestor.
The new model of diversification of thé common ancestor is 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- species of thé Corilla and Pan gênera.
1. Introduction
Research into h o m i n o i d évolution involves m u l t i p l e disciplines. A l t h o u g h 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; D u t r i l l a u x et al., 1986; D u t r i l l a u x & Couturier, 1986; Stanyon and Chiarelli, 1981, 1982, 1983; Y u n i s h 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 i n t o e v o l u t i o n a r y concepts (Gould, 1985;
Devillers & Chaline, 1993; Chaline. 1994) indicates that there is a hierarchized structure in
thé l i v i n g world and that thé relations among thé various levels of intégration are h i g h l y
complex, r a n g i n g 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 critically 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 within 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, blood groupings, etc.) bas confirmed thé proximity between humans and thé hîgher apes, but without conclusivcly scltling thc questions of kinship and thé splitting of thé différent branches.
It is thé général consensus that cladistically thé chimpanzee groupe w i t h Homo, then with 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 thé same family (Hominidae)(Fig.l). Within this family, thé subfamily Homininae is divided into one tribe for orangutans (Pongini) and another tribe for gorillas, chimpanzees and hu- mans (Hominini). Gorillas are placed in thé subtribe Gorillina, while chimpanzees and hu- mans form thé Hominina subtribe.
Estimated divergence between higher primates based on thé ipY)-globin gène région combined with available nucleotide data ranges from 1.61 % (humans versus common chim- panzees) to 3.52 % (orangutans versus h u m a n s and African gréât apes). Pan diverges from Gorilla by 1.84 % (Miyamoto et al., 1987, 1988), a figure similar 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 thé previous relationships and classification.
The human-chimpanzee clade is corroborated by several other DNA séquence analyses 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 région of thé mt génome containing gènes for tRNA
His, t R N A
Scr, t R N A
Lcuand part of ND4 and ND5 (Hayasaka et al.. 19K8) and thé cytochrome oxidase II locus of mitochondrial gènes (Pruvolo et al., 1991; Horai et al., 1992). Only DNA analysis of thc involucrin locus (Djian and Grccn. 1990) fails to confirm this clade, perhaps as a resuit of polymorphism.
It should be noted that thé molecular analyses of chimpanzees were conducted on individuals labelled Pan troglodytes without specifying to which of thé three l i v i n 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 i n - ship is so difficult to specify, because divergence among thé three sub-specics is probably very différent from that w i t h humans.
We are in thé paradoxical and unfortunately increasingly common situation where thé most sophisticated analytical techniques requiring very thorough expérimentation are applied to samples chosen haphazardly! The population variability of thé study species is over- looked, even though its temporal and paleobiogeographical distribution is often highly com- plex.
Specialists generally accept that thé séparation of higher primates and humans results
from a double : cation), thé fir5 Pan and thé set events looks li îrichotomy, or and thé seconc conspecific sub extant Homo sa
3- Evolution al 3.1 -Chro A major ac
& Lejeune, 197 Opinions c thé chromosom or that alteratio thé phylogenic grams entail ac(
rearrangement i thé next section By contras placing them in away from heter (s il ver nitrate) t>
differs from thc tures indicate fhï
3.2 -A ne\e comm by déduction. T share a commor them. This is th mosomal chang derived froni ar convergence.
Wc can ait somcs and thé s Among an logically thé ont which emigrate(
m i l l i o n years (/
stable from thé
occurred since t
After thé st
extant gênera -
corresponds to
APEii A M I ) 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 m i l l i o n 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 m u t a n l chromo- somes (2q. 3, 7, 10, 11, 17 & 20) and by thé rétention of clcven non-mutated common chromosomes (1, 4, 5, 8, 9, 12, 13, 14, 15, 16 & 18} inherited by thé three living species ( C h a l i n e e t a l . , 1991) (Fig. 5).
The occurrence of seven characleristic mutant chromosomes found in thé gorilla, chim- panzee and h u m a n descendants implies that thé common ancestor was a single monotypic species, not divided into subspecies. Genetic pooling as a resuit of interbreeding produces a fairly even spread of chromosome variety, i n c l u d i n g chromosomal variations that appear in isolated individuals. This first part of thé hislory of thé common ancestor corresponds to what we shall term thé "first homogcnous common ancestor phase" (Fig. 5).
Thereafter. thé common ancestor diversified and thé lineages separated, leading on thé one hand to thé gorilla and chimpanzee and on thé other to h u m a n s . This divergence raises a complex popularïonal problem about thé distribution of five new mutaled chromosomes.
It 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 spécifie mulated chromosomes (12 & 16) not found in humans. In other words. chimpanzees share three common mutated chromosomes wilh humans and two common mutated chromosomes with gorillas. But gorillas share no spécial rearrangements with humans!
Thîs position is inexplicable by thé standard hypothesis of a split into two branches (dichotomie model) leading to thé gorilla/chimpanzee on one side and to h u m a n s on thé other.
Though there is a possible solution to thé puzzle: thé "second heterogcneous common ancestor phase" (Fig. 5).
To explain this major paradox, it must be supposed that al a certain t i m e in their history.
after thé tïrsf undilïerentiated phase, thé ancestors of chimpanzees and gorillas were able to interbrecd 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 i l three taxa were still conspecific".
But iî must also be accepted that for sornc lime, perhaps différent from thé first period, thé ancestors of chimpanzees and humans were able to interbreed and to incorporate three new chromosomal m u t a t i o n s into thcir genetic constitution, possessed by them alonc and not gorillas.
However, thé facl that thé ancestors of gorillas and h u m a n s do not share exclusive mutations in their chromosomal formulas implies that they did not at that time hâve contacts allowing hybridizalion. They were geographically isolated.
Three hypothèses can be put forward, necessarily broken down into several phases and stages, summarized as follows:
In thé first homogcnous common ancestor phase, thé ancestors of gorillas, chimpanzees and h u m a n s formed a common undifferentiated monotypic ancestral group in which ail i n d i v i d u a l s could interbreed. There was a single common species, not yet identifiée in thé fossil record, and so nameless.
In thé second heterogeneous common ancestor phase, thé ancestral group split into three subgroups. Probably i n t o three subspecies as only subspecies could hâve retained thé a b i l i t y to interbreed in thé areas where they came into contact and to pool their genetic héritage. We s h a l l call them respectively pre-chimpanzecs, pre-gorillas and p r e - h o m i n i a n s or pre- australopithecines. By comparison w i t h thé geographical d i s t r i b u t i o n of present-day species
(Collet, 1988) admit a plausib
— thé pré day Lake Victi River in a fore:
— thé pré north of thé Za
— thé pr African Rift V;
This thret forerunncrs of I las of thé l i v i n t The pre-cl to interbreed \ spread and are mans.
S i m i l a r l y , As a resuit, thé thé chromosom,
However, ]
acquire mutatio
This sugge
west Cameroon
thé pre-gorillas
This hypot
advanced by Sn
3.4 - Hypoi
This hypotl
pre-gorillas and
differentiated (F
form thé pré-ci
australopitheciru
in micc in Japai
tnusculus castai,
cannot be ruled i
3.5 - Hypot
A not lier h y
common mutatk
gorillas and pré-
wise occurred in
lion seems sfatis
model consistent
(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 r u n n i n g 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 following scénario.
The pre-chi-mpanzees were in contact in thé hast with thé pre-hominians and were able to interbreed w i t h [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 w i t h thé pre-gorillas and inlerbrcd.
As a resuit, thé two chromosomal mutations occurring in thé common zone were included in thé chromosomal héritage of l i v i n g 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 i m p l y 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, t h i s 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. D A M B R I C O U R T 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 h u m a n 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 Atl an tic 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 d o m a i n , 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 u n k n o w n 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 Pliocene-Pleistocene 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 Australopithecus 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 si mply one of divergence into two 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 their history proper (Fig.H)).
As said above, thé apc group w i t h thé most primitive chrornosomal formula is logically thé orangutan group which emigrated to Asia where it has heen eut off from thé African branch for more than 10 million years. It is now accepted that Ramapiihecus and Sivapithecus arc 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 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 (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 ramidus found by Whilc el al. (1994, 1995) in thé Pliocène of thé Middle Awash (Ethiopia) and dated to 4,4 Myrs. Most data about thé teeth (metric, morphology. enamcl thickness) and even fealures of thé cranium "evincing a s t r i k i n g l y chimpanzee-likc morphology" are very s i m i l a r lo chimpanzee form (Bonobo ?), 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!
The chrornosomal model described hère entails several anatomical implications that can be tested by paleontology. The first is thaï thé cranial and dental morphologies of thé three sub-species of thé common ancestor should be highly simian. The discovery of ramidus is f u l l y consistent with t h i s hypothesis and is a first favorable test. The second implication concerns thé shapc of thé pelvis. As gorillas and chimpanzees are quadrupeds and as bipedalism is thé apomorphic feature characteristic of australopithecines and their h u m a n descendants, thé three components of thé common ancestor must therefore still hâve walked on ail fours.
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 translation.
Fig. 1 - The most PTR: Pan traRludyt al., 19S7)
PPY PTR~
PPY-
PPY-
HSA-
PPY HSA
PPY—
PTR HSA~
APES AND AUSTRALOPITHECINF.S O K I G I N S
trqglodytes Gorzlla gorïlla
Hominini
~\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)
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13 15
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16 HSA
17
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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 t e r m i n a l - t e r m i n a l translocation (afler Dulrillaux and Couturier. I9S6).
CIIALINE. DURAND, MARCHAND, DAMBRICOURT MAI.ASSK and DESHAYCS
APES AND AUSTRALOPm-
PTR
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a
PPY !
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!
O
s
— f\ — • — i
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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
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l-ig.-l - Chromosoiiial phylogeny for thé llominoidea. Cx: complex change; De: d e l e r i o n ; 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).
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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 - D i s t r i b u t i o n 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 ( B u r u n d i and Rwanda). A third sub-species, thé m o u n t a i n goi'illa ol' Rwanda and Ijgand.i (Gnritlti t>orilla hcringri) is in danger of i m m i n e n t 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.
Fig.9 - Dichotomie model cxplaining thc di.stribution of chromosomes in living species. Tliis most parcimonious model suggests thaï at'ter ihe monohpic phaie. thc common ancestor split into two sub-species - pre-gorilla and pre- australopithecine - and that thé populations from thc two sub-species interbred to produce thc third. hybrid, sub-spccies - thc pre-chimpanzees
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C H A L i N K , DURAND, MARCHAND. DAMBRICOURT MALASSE and DESHAYES
