Towards a theory of modern human origins: Geography, demography, and diversity in recent human evolution

Towards a Theory of Modern Human Origins: Geography,Demography, and Diversity in Recent Human Evolution

MARTA MIRAZON LAHR1,3 AND ROBERT A. FOLEY2,3

1Departamento de Biologia, Instituto de Biociencias, Universidade de SaoPaulo, 05508–900 Cidade Universitaria, Sao Paulo, Brasil2Department of Biological Anthropology, University of Cambridge,CB2 3DZ Cambridge, England3King’s College Research Centre Human Diversity Project, King8s College,CB2 3DZ Cambridge, England

KEY WORDS evolutionary theory; geography; Neanderthals;modern human origins

ABSTRACT The origins of modern humans have been the central debatein palaeoanthropology during the last decade. We examine the problem in thecontext of the history of anthropology, the accumulating evidence for a recentAfrican origin, and evolutionary mechanisms. Using a historical perspective,we show that the current controversy is a continuation of older conflicts and assuch relates to questions of both origins and diversity. However, a better fossilsample, improved dates, and genetic data have introduced new perspectives,and we argue that evolutionary geography, which uses spatial distributions ofpopulations as the basis for integrating contingent, adaptive, and demo-graphic aspects of microevolutionary change, provides an appropriate theoreti-cal framework.

Evolutionary geography is used to explore two events: the evolution of theNeanderthal lineage and the relationship between an ancestral bottleneckwith the evolution of anatomically modern humans and their diversity. Weargue that the Neanderthal and modern lineages share a common ancestor inan African population between 350,000 and 250,000 years ago rather than inthe earlier Middle Pleistocene; this ancestral population, which developedmode 3 technology (Levallois/Middle Stone Age), dispersed across Africa andwestern Eurasia in a warmer period prior to independent evolution towardsNeanderthals and modern humans in stage 6. Both lineages would thus sharea common large-brained ancestry, a technology, and a history of dispersal.They differ in the conditions under which they subsequently evolved and theirultimate evolutionary fate. Both lineages illustrate the repeated interactionsof the glacial cycles, the role of cold-arid periods in producing fragmentation ofpopulations, bottlenecks, and isolation, and the role of warmer periods inproducing trans-African dispersals. Yrbk Phys Anthropol 41:137–176,1998. r 1998 Wiley-Liss, Inc.

TABLE OF CONTENTS

Origins and Diversity: Historical Perspectives on Recent Human Evolution .................. 139Evolutionary Geography ..................................................................................................... 145

Population survival, range, and demography ................................................................ 146Modern Human Diversification .......................................................................................... 148

Neanderthals and modern humans ................................................................................ 148Ancestral bottlenecks and the establishment of modern humans outside

sub-Saharan Africa ...................................................................................................... 160

YEARBOOK OF PHYSICAL ANTHROPOLOGY 41:137–176 (1998)

r 1998 WILEY-LISS, INC.

Spatial structure of the ancestral population ............................................................. 160Population structure prior to Upper Pleistocene expansions ..................................... 163Secondary bottlenecks and the differentiation of human populations ...................... 165Human diversity within and out of Africa ................................................................... 167

Discussion and Conclusions ................................................................................................ 168Dispersals of modern humans ......................................................................................... 168Diversity through time .................................................................................................... 168Extinction ......................................................................................................................... 169Microevolutionary events ................................................................................................ 170Role of geography in recent human evolutionary history .............................................. 170

Acknowledgments ............................................................................................................... 171Literature Cited .................................................................................................................. 171

The evolution of modern human originshas dominated the last decade of researchand controversy in palaeoanthropology. Thecharacter of this debate contrasts with thosein the early part of this century, when therewas insufficient data or chronological resolu-tion to separate out confidently distinct evo-lutionary events in hominid evolution, andwith those in the middle part of the century,when early hominid research pushed mod-ern human evolution into the background.The emergence of the ‘‘modern human prob-lem’’ has posed a major challenge to palaeo-anthropology, as is evidenced by the persis-tence of two competing theories. Thisapparent impasse between the so-called mul-tiregional (MM) and single origin (SOM)models has been ascribed to either lack ofdata or a clash between molecular geneticand palaeontological evidence or to compet-ing intellectual paradigms (Clark and Willer-met, 1995). We would argue that the evi-dence now available allows the solution ofthe modern human problem at the level ofthese two models but that much remains tobe done in terms of relating the evolution ofmodern humans to evolutionary theory andmechanism and in integrating models oforigins with the evolution of human diver-sity.

The purpose of this paper is to explore theproblem of modern human evolution in termsof a number of broader issues in evolution-ary theory. The first of these is that prob-lems of phylogenetic origins such as that ofmodern humans cannot be isolated from themore general issue of population diversityand variation; hence, any theory of modern

human origins must also account for chang-ing patterns of diversity across some originthreshold. The problem of modern humanorigins could thus be approached as that ofhuman diversity through time. Second, itmust be recognized that the issue of theorigins of modern humans is essentially amicroevolutionary one. Multiregional mod-els have stressed the lack of speciation inlater hominid evolution (Wolpoff et al., 1994),and single origin models have often de-manded reproductive isolation betweenhominid populations and speciation events(Stringer and Andrews, 1988). In practice,the scale, both in terms of chronology andbiology, is clearly on the edge of wherespecies boundaries may lie. Given the needto explore detailed geographical and tempo-ral patterns within a larger framework,demographic rather than species-based as-pects of evolutionary theory should be consid-ered. Finally, similarly to many interestingproblems in evolution, modern human ori-gins rest as much on geographical patternsas on chronological ones, and the archaeologi-cal and fossil records provide access to these.However, the consideration of spatial pat-terns requires an understanding of thetheory underlying the possible roles playedby geography on the evolution of popula-tions within a lineage.

This paper is divided into three parts.First, we outline how issues of origins havehistorically been intimately related to bothscientific and more general notions of hu-man diversity and how the current debatefits within this history; second, we outlinesome of the principles of evolutionary geogra-

138 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 41, 1998

phy that provide a framework for consider-ing recent human evolution and discuss howthese can be used to explore the complexpattern of modern human diversification;finally, we use these principles to explore theactual patterns and mechanisms involved inthe separation and subsequent diversifica-tion of the populations ancestral to livinghumans today.

ORIGINS AND DIVERSITY:HISTORICAL PERSPECTIVES

ON RECENT HUMAN EVOLUTION

Although the current debate on modernhuman evolution is phrased in terms oforigins, the question of human diversity hasalways been an integral part of it. This isclear in the development of the currentdebate, which, although it emerged as anissue in prehistory (Bowler, 1986; Smith andSpencer, 1984, and papers therein), rapidlybecame a forum for discussions of the ge-netic variation found in the human popula-tion today. This interest is not new. Thediversity of humans around the world haslong been a source of both scientific andreligious discussions, and theories explain-ing how it has arisen are numerous. The riseof evolutionary theory in the last 150 yearsdid little to change the actual perception ofhuman differences. It mainly placed thesewithin a new context, that of proximity ordistance from hominid fossil forms and non-human primates. Interpretations at the turnof the century focused on two alternativeand often extreme models of modern humanorigins. Attempts at asserting the applica-tion of a Darwinian perspective to the originof people saw the rise of the first unilinealmodels—from Pithecanthropus to Neander-thals to humans—such as those of Manou-vrier, Haeckel, Cunningham, and Schwalbe.These were first contested not on the basis ofthe nature of the phylogenetic relationshipsbut on the placing of these fossils in thehuman family by contemporaries like Vir-chow and Turner. However, once the homi-nid character of Neanderthals was accepted,the actual descent of humans from them,particularly Europeans, was questioned. Itwas thus that researchers like Boule, Keith,Breuil, and Elliot Smith argued that Nean-derthals represented an extinct branch of

humanity, a view defended by some, likeVallois, until the middle part of the century.Hrdlicka and Weidenreich, former studentsof the early unilinealists Manouvrier andSchwalbe, were the main dissenting voices.Hrdlicka studied not only the EuropeanNeanderthal remains but traveled to Rhode-sia to examine the newly found fossil ofKabwe. He proposed a new unilineal modelin which there was a Neanderthal phase inthe evolution of humans. Weidenreich, fol-lowing his study of the Sinanthropus fossilsand their comparison to Pithecanthropusremains, proposed a model similar to Hrdlic-ka’s but which stressed the descent of livingAsians from Sinanthropus and living Austra-lians from Pithecanthropus (Weidenreich,1943) (in his model, Neanderthals actuallyrepresent a side branch, and modern Europe-ans are descendants of the Levantine fos-sils). Although drastically different regard-ing the role of archaic hominids in modernhuman evolution, all these early and mid-twentieth-century views highlighted re-gional differences among present humanpopulations and did not emphasize the evo-lutionary mechanisms that were being dis-cussed and explored at the time by foundersof the modern synthesis such as J. Huxley orSimpson.1 These two approaches, one empha-sizing direct ancestry, continuity, and re-gional stability, the other temporal and spa-tial discontinuities, essentially set theframework for the subsequent decades ofresearch on the evolution of human diver-sity.

Each of these models also has implica-tions for broader interpretations of humandiversity, especially whether all humans arevery similar and have virtually identicalevolutionary heritages or not and why differ-ences between populations have evolved. Itis here that ideas on human diversity haveperhaps been most changeable, and it isclear that anthropological studies and theperception of population differences havealso had sociopolitical dimensions. Duringthe early part of this century, the emphasis

1Carleton Coon represents an interesting figure in this water-shed between pre- and post-neo-Darwinism in that, although hismajor works were published in the 1950s and 1960s (Coon, 1962),his framework for considering evolutionary diversity in humanswas essentially that of the prewar anthropologists.

139THEORY OF MODERN HUMAN ORIGINSLahr and Foley]

was on the differences between human popu-lations and the expectation that pure re-gional types or races had once existed. Thisview fueled eugenic and racist movementsin the US and Europe. The fact that anthro-pological research had provided a scientificflag for these movements had a profoundeffect on the future development of the disci-pline. Partly to compensate for earlier ex-cesses, postwar anthropological research hadto prove to the academic world that it had noeugenic and racist tendencies. For the threesubsequent decades, anthropologists fo-cused on research that stressed the geneticsimilarities between human groups, the plas-ticity of the human phenotype and its rela-tion to environmental factors, local adapta-tion rather than migration as the source ofvariation, and the functionally unique as-pects of human societies. Studies on theevolution of human diversity or the role anddirection of migrations in the developmentof diversity became rare or absent. A corol-lary of these developments was the generalabandonment of human morphology as asource of information for phylogenetic stud-ies at the level of human populations. It isinteresting that while the study of fossilhominid skeletal remains received a majorboost from the 1950s to the 1980s, particu-larly all the then newly found australopithe-cines, the study of the evolution of modernhumans and their differences through skel-etal remains was left aside. This is not to saythat no research on modern human skeletalsamples was carried out throughout thistime period. Two areas had a significantdevelopment. On the one hand, the prin-ciples of palaeopathological diagnosis andbioarchaeology were developed, and this fieldbecame and still is a very active one withinanthropology (Larsen, 1997). On the other,the use of multivariate statistics for theanalysis of cranial measurements becameestablished, and a number of studies investi-gated the relationships among present hu-man populations using these methods. How-ever, with the exception of works like thoseof W.W. Howells (1973, 1976, 1989), thesestudies were carried out at the level ofpresent regional populations and did notdwell on the issues of the origin of modernhumans and global human diversity.

Therefore, when palaeoanthropology re-gained a deeper interest in the origin ofmodern humans in the early 1980s, thestatus quo was a theory that stressed thelocal evolutionary character of human popu-lations and variation as a product of immedi-ate environmental adaptation rather thanpopulation history. This view saw humanplasticity in the face of environmental needsas the key mechanism and strongly rejectedhypotheses of wide-ranging migrations anddispersals as a source of diversity. Weiden-reich’s multiregional theory, which lacked atheoretical mechanism for the maintenanceof worldwide parallelisms for the regionalevolution of humans from archaic ancestors,was reworked into a coherent model of clinalevolution in which gene flow homogenizeddifferences and prevented speciation (Wol-poff, 1989; Wolpoff et al., 1984).

Nevertheless, there was a contrast be-tween the widely held belief that in EastAsia and Australia there had been continu-ity of occupation and descent from Homoerectus onwards, as proposed by Weiden-reich in the 1930s–1940s on one hand and onthe other the persistent controversy over thecontribution of Neanderthals to the modernhuman gene pool and the relative age ofmodern humans in Africa and the MiddleEast. Neanderthals are the best-representedfossil hominid in terms of number of fossils,anatomical completeness, and age-sex distri-bution. Various recently dated sites suggestthat there may have been over 100,000years between the first appearance of mod-ern humans in Africa and the last appear-ance of Neanderthals, making these twohominid groups contemporaneous for thegreater part of their history. If the dating ofsites like Saint Cesaire and Zafarraya iscorrect (Leveque and Vandermeersch, 1981;Leveque et al., 1993; Hublin, 1996), it is alsothe case that these two populations mayhave overlapped by some 10,000 years inEurope (Strauss, 1993–1994; Hublin et al.,1995; Grun and Stringer, 1991). Therefore,Neanderthals are also very recent, and theconsensus that grew during the 1980s abouttheir limited geographical distribution andthe apomorphic character of their anatomybecame very difficult to integrate with long-term claims (Brace, 1964) that late Neander-


thals show morphological changes that couldbe interpreted as signs of admixture (Mel-lars, 1996; Stringer and Gamble, 1993). Theredating of the fossil sample from Krapinato 130,000 years ago (Ka) (Rink et al., 1995),long argued as progressive between Neander-thals and Upper Palaeolithic Europeans,and the character of recent fossils like Zafar-raya and St. Cesaire have confirmed thatNeanderthals show no trends towards in-creasing modernity. Thus, the absence oftruly transitional fossils in this area raisedagain the question of extinction and replace-ment vs. admixture. Although the fossils areunlikely ever to rule out any admixture, thecontribution of Neanderthals to Europeanmorphology appears to have been minimalor completely lacking (Brauer, 1992; Holli-day, 1997; Stringer, 1992, 1993; Stringer etal., 1984).

New studies have also brought the notionof regional continuity outside Europe undercloser scrutiny. There is indeed regionalityto be found today in some of the so-calledcontinuity traits (the characters proposed asevidence forAsian andAustralasian morpho-logical continuity from Asian Homo erectusto modern populations) as well as in othertraits not included in the multiregionalmodel. However, the original descriptions ofthe traits and their linkage to a model byWeidenreich were either largely qualitativeor based on relatively small samples. Statis-tical approaches and larger samples havegenerally failed to corroborate the earlierobservations, and greater consideration ofthe polarity of these traits as well as func-tional patterns of human cranial morphol-ogy has greatly limited the evolutionarysignificance of many of them (Groves, 1989;Groves and Lahr, 1994; Lahr, 1994, 1996;Lahr and Wright, 1996; Lieberman, 1996).Indeed, from a historical point of view, morein-depth studies led even some of those whooriginally defended the view of long-termmorphological continuity in Southeast Asiato reject much of the basis for multiregional-ity, as indicated in this passage from Macin-tosh and Larnach (1976):

Macintosh (1963). . .supported Weidenreich’s opinionthat special features of the Pithecanthropus-Soloensisforehead have undergone very little change in theAustralian. We no longer hold any such view....Acompari-

son of Australian skulls with those of Homo erectusshows the complete absence of the Homo erectus cranialpattern in the former....[I]t [is] extremely unlikely thatthey [Ngandong] can be ancestral to Australians.

The problem of both Far Eastern and Euro-pean links of archaic hominids with recenthuman populations hinged on two issues:the relative age of morphologically differentpopulations and the relative proximity ofliving human populations to their supposedregional archaic ancestors. While new dateshave tended to show the contrast betweenAfrica and elsewhere with regard to the ageof the modern population, a number of stud-ies have also established the morphologicalunity of all modern humans. Metric analy-ses have overwhelmingly shown that livinghuman populations share far more witheach other than with their local antecedentpopulations (Howells, 1973, 1989; Stringer,1996a,b; Stringer et al., 1997; van Vark andBilsborough, 1991; van Vark et al., 1992).The modern human morphological homoge-neity, the discontinuities in the fossil recordoutside Africa, the chronological contrastbetween the first appearance of modernhumans in Africa and in the rest of theworld, and the tropical body proportions ofthe earliest modern Europeans in contrastto those of Neanderthals led to a wide accep-tance of a view developed gradually andindependently since the late 1970s of asingle origin, a recent origin, and an Africanorigin (Brauer, 1989; Holliday, 1997; How-ells, 1976, 1989; Lahr, 1996; Lieberman,1996; Stringer et al., 1984; Turbon et al.,1997; Waddle, 1994). In addition, from themid-1980s the uniformity of the modernhuman morphology has found a reflection inthe overall genetic homogeneity of modernhumans.

In 1987, the publication of a phylogeneticanalysis of human mitochondrial DNA(mtDNA) sequences was among the firstattempts to use molecular genetics to ex-plore human (as opposed to hominid) origins(Cann et al., 1987). The surprising claim atthe time was that human populations todayare descended from a small ancestral popu-lation living inAfrica within the last quarter-of-a-million years. In effect, the growingfield of molecular anthropology has con-firmed and elaborated on this claim. The


initial proposition was twofold: that in termsof mtDNA lineages African populations weresignificantly more diverse than others andthat all human mtDNA lineages coalescedbetween 200 and 150 Ka. High levels ofAfrican diversity have now been confirmedfor mtDNA, a number of microsatellites, andfor a number of loci on the Y chromosome(Armour et al., 1996; Bowcock et al., 1991,1994; Hammer, 1995; Hammer et al., 1997;Hasegawa and Horai, 1991; Hasegawa etal., 1993; Horai et al., 1993, 1995; Nei andGraur, 1984; Paabo, 1995; Rogers and Jorde,1995; Stoneking, 1993; Stoneking et al.,1997; Takahata, 1993; Tamura and Nei,1993; Tishkoff et al., 1996; Vigilant et al.,1991; Whitfield et al., 1995). This diversitycan be measured at a number of regionalscales; for example, the Turkana are morediverse than all Europeans, and East Africais the most diverse region (Watson et al.,1997). Diversity is high, whether measuredin terms of the number of lineages present orin terms of the evolutionary distance be-tween haplotypes. Early attempts to repre-sent this diversity in terms of tree struc-tures rooted in Africa were subject tomethodological and sampling criticisms(Maddison et al., 1992; Templeton, 1993,1997), but more sophisticated analyses haveconfirmed the initial results (Nei andTakezaki, 1996; Penny et al., 1995). Recentwork on the beta globins has also shownhigher African diversity, but it has alsoindicated patterns of intercontinental diver-sity that, it has been claimed, do not supporta restricted geographical distribution of hu-man ancestral populations (Harding et al.,1997). However, the ancient populationstructure reflected in this slow mutatingsystem cannot be interpreted spatially fromthe present distribution of b-globin lineages.In this sense, they neither support nor re-fute the out-of-Africa model but can be incor-porated within it.

The second proposition—that the last com-mon mtDNA ancestor of all humans (‘‘Eve,’’or the point of coalescence of lineages) livedin the recent past—has also been supportedby studies of other, independent, fast muta-tion loci. Many analyses, using mtDNA, Ymarkers, and microsatellites, have yieldedestimates between 180,000 and 125,000

years (Hammer et al., 1997; Pandya et al.,1997; Stoneking, 1997; Tishkoff et al., 1997;Wallace et al., 1997). These recent dates ofcoalescence of modern human lineages arein contrast to the single result obtained froma fossil hominid, a Neanderthal, whosesampled part of the mtDNA is calculated tocoalesce with that of living humans between600 and 500 Ka (Krings et al., 1997). Theamplification of 378 bp of the mtDNA controlregion of the Neanderthal type specimenresulted in a lineage that differs from thestandard living human (‘‘Anderson’’) refer-ence sequence by 27 substitutions. Livinghumans differ from each other on average by8–12 substitutions, showing that the Nean-derthal mtDNA obtained is three times moredifferent than the difference between anytwo average modern lineages.

The context in which to interpret thesignificance of these findings is demography.Genetic diversity is a function of ancestralpopulation size and the mutation rate of thesystem under study. Modern humans lackgenetic diversity in relation to other species(Ferris et al., 1981; Horai and Hayasaka,1990; Kocher and Wilson, 1991; Li andSadler, 1991; Morin et al., 1993; Rogers andJorde, 1995; Ruvolo et al., 1993; Wilson etal., 1985), interpreted as the outcome of abottleneck in our relatively recent evolution-ary past, when a significant portion of ances-tral mtDNA diversity was lost (Bowcock etal., 1991; Brown, 1980; Haigh and MaynardSmith, 1972; Harpending et al., 1993; Jonesand Rouhani, 1986; Nei and Graur, 1984;Maynard Smith, 1990; Rogers and Jorde,1995; Takahata et al., 1995; Wills, 1990).Estimates of the size of the effective ances-tral population to all humans suggest thatduring the bottleneck it was composed of.10,000 individuals. Furthermore, it hasbeen estimated using Alu insertion polymor-phism data that the population before thebottleneck took place was not very largeeither, numbering approximately 40,000 in-dividuals (Sherry et al., 1997). Only if ances-tral populations had been very large couldwe accommodate both the Neanderthal andmodern mtDNA diversity within a singlebreeding group, and that was not the case.Therefore, the differences found betweenmodern humans and the Neanderthal


mtDNA sample, together with the estimatesof small ancestral population sizes, providestrong support for the view that humansand Neanderthals represent separate homi-nid lineages. Furthermore, palaeodemo-graphic models have also shown that thehominid population was never large enoughto sustain the gene flow necessary to main-tain the long-term global homogeneity re-quired by the multiregional model (Mander-scheid and Rogers, 1996).

In summary, therefore, empirical evidencehas been accumulating relatively rapidly, inboth palaeontology and genetics, in favor ofa recent, localized, and African origin for theancestors of modern humans. We are thusapproaching a moment of tangible empiricalconsensus over the broad pattern of theevolution of modern humans. This has led toa number of recognizable positions. One is afirm commitment to the maintenance oforthodox views represented by the multire-gional model. This takes the form of bothcritical skepticism and a reevaluation of themeaning of multiregionality (Templeton,1997; Wolpoff and Caspari, 1997). A secondis what may be described as the ‘‘out ofAfrica as normal science’’ position. This isthe view held by some geneticists, who haveattempted to pinpoint the time and geogra-phy of various gene histories as representedby coalescent points and genetic distances. Athird position would be that a single originin Africa in the relatively recent past pro-vides merely the framework for consideringbroader evolutionary issues relating to hu-man diversity and evolutionary mecha-nisms. It is this third position that webelieve requires further elaboration. Amongthe important questions that remain arethose related to the processes involved in theevolution of human diversity from an ances-tral source, the pattern of population differ-entiation, the time span involved, and thelocalized or global character of the mecha-nisms acting upon it. The link between thisthird position and the historical shifts dur-ing this century are perhaps worth mention-ing briefly (Table 1). The trend towardscontinuity gene flow models has been thedominant one and is consistent with bothsociopolitical views emphasizing continuityand overlap between populations and with

some of the neo-Darwinian ideas of popula-tion variability and local adaptive patterns.In contrast, the single origin model has oftenappeared to be a throwback to an earlier andpremodern synthesis view of evolution. Itdemarcates populations geographically andsharply, it depends upon major migratoryevents, and it pays little or no attention toeither mechanisms of gene flow or naturalselection. The early modern populations mi-grating out of Africa may have more incommon with Elliott Smith’s hyper-diffusion-ism than with modern evolutionary biology.

It is these contrasts that lie at the heart ofthe modern human origins problem. Empiri-cally, the SOM is the better model, but it isconsistent with outmoded evolutionary ideas,whereas the multiregional model has littleempirical support but is very much in linewith conventional population genetics andadaptive processes. Resolving these para-doxes requires either a major reworking ofthe empirical evidence or an examination ofhow a broad model of a single origin ofmodern humans in Africa can be brought inline with current and developing views ofmicroevolutionary processes.

There are two reasons why the latter isthe way forward and why we are in a betterposition now than half a century ago to dealwith the evolution of human diversity. Thefirst is empirical and methodological ad-vances. The palaeoanthropological databasenow available, compared to that before thewar when diffusionist models predominated,is greatly improved. The models of Weiden-reich and Elliott Smith were based on ahandful of fossils—the erectus specimensfrom Zhoukoudien, Pithecanthropus, someNeanderthals, and isolated African findslike Kabwe (in addition to the confusioncaused by Piltdown). Today there is a largenumber of fossils from the Middle and Up-per Pleistocene, and these are geographi-cally widespread. However, new methodsare providing new evidence. In the last 15years, major developments have occurredwithin two areas of research with directimplications for the question of modern hu-man origins—palaeochronology and molecu-lar anthropology. Major advances in pal-aeochronology are related to the development


of new dating techniques, like thermolumi-nescence (TL) and electron spin resonance(ESR), which have been essential for thereshaping of the chronology of the period200 to 50 Ka. The wide application of molecu-lar genetics to anthropology can be associ-ated with the development of PCR technol-ogy allowing the fast processing of moleculardata, in this case molecular data regardinghuman population characteristics, while inanalytical terms it is clear that computabil-ity is what gives modern science its edge.However, it is also the case that presentstudies of modern human diversity buildupon the knowledge gathered by both pre-and postwar physical anthropologists, sothat phylogenetic studies of the phenotypi-cal differences among living and fossil mod-ern populations use complex statistical meth-ods in order to include concepts of traitpolarity, identify allometric components of

variation, and investigate how and to whatextent environmental factors contribute tothe observed variance. Although it is not yetwidely recognized, the inclusion of thesecaveats into the phylogenetic analyses ofmodern human skeletal information has re-sulted in the successful applicability of suchdata to the question of modern human ori-gins, as shown by the consistency betweenpatterns of relationships among populationsderived from genetic and cranial data (Lahr,1996) and the similar levels of interpopula-tion variance explained by either source(Relethford and Harpending, 1994).

The second reason is that the gene flowmodel is itself no longer central to the cur-rent understanding of evolutionary patternsamong other animals. Partly this is therecognition that models such as the shiftingbalance model that have been used to under-pin the MM were in fact developed by Wright

TABLE 1. History of studies of human origins1

Date Consensus model for human origins Key anthropologists

1860–1920 Unilineal progressive evolution: all evolution seen as a progressivetrend, driven by orthogenetic processes, leading to modernhumans; no geography and no point of origin; key issues related towhether there were any intermediate steps (Neanderthals, etc.)and how they should be ordered; living human diversity seen asladders along a progressive continuum

ManrouvierCunninghamSchwalbeHaeckel

1900–1950 Typological trees: most fossils seen as side branches away from themain line, generally becoming extinct; lack of continuity and anemphasis on parallel evolution; key controversies related to whichif any fossils (e.g., Piltdown) did lie on the true line of descent;living human diversity seen as part of the tree of hominid varia-tion; the origin of modern humans located with particular fossils

KeithBouleBreuil

1940–1990 Anagenetic polytypic evolution: development of the modern synthesisled to a recognition that variation within populations and speciescould occur and that populations would be transformed graduallyby selection; emphasis placed on continuous variation, gene flow,and progressive adaptive change; living human diversity part of aspectrum of variation; model was transformed into the multire-gional model in the 1980s as a means of accounting for spatiotem-poral patterns within a population genetics framework; no point oforigins; gene flow the principal mechanism of evolutionary changeagainst local adaptive pressures

CoonWeidenreichMayrBraceWolpoff/Thorne

1980– Divergence and replacement: emphasis on geographical variation,mechanisms of speciation, and the role of isolation in evolution ledto renewed interest in more taxonomically diverse models ofhuman evolution; emphasis increasingly placed on localized eventssuch as range fragmentation and genetic bottlenecks underlyingevolutionary processes, with correlated interest in dispersals,replacements, and extinctions; model was very much driven by agreater use of genetics and a more precise chronology; livinghuman diversity as a marker of recent historical patterns; humanorigins located at a particular point in time and space (Africa, latePleistocene)

HowellsStringerWilson, etc.Brauer/Smith (interme-

diate hypotheses ofan African origin withadmixture betweenmodern and archaichominids)

1 Four phases in the history of studies of human origins can be recognized. These overlap considerably in time, and to some extentrepresent an ongoing conflict between unilinearl/progressive/polytypic models stressing gradual transformation and adaptiveradiation models emphasizing the divergence, isolation, and extinction of populations and species. The current conflict betweenmultiregional and single origin models represents the latest manifestation of the debate, which primarily reflects interpretations andapplications of the contemporary interpretation of evolutionary processes in general.


(1931) to deal with small-scale local popula-tion differences, not intercontinental demesover millions of years (Maynard Smith 1989).As such, the MM is in fact not as consistentwith neo-Darwinian mechanisms as has beenclaimed. In contrast, detailed studies of themorphology and genetics of a wide range ofspecies have shown that dispersals, geo-graphical variation, and local events are themeans by which diversity is generated ratherthan uniform and constant gene flow (Avise,1994). In other words, local geographicaland often discrete events structure evolution-ary patterns. Evolutionary mechanisms un-derlying events such as the origins of mod-ern humans are therefore likely to be verymuch linked to detailed geographical pat-terns.

The discussion above suggests that thereis now a consistent chronological and spatialframework for studying modern human ori-gins but that more detailed hypotheses arerequired to explain the relationships be-tween a single localized event and subse-quent population differentiation and dispers-als. The increase in the fossil sample, thegreater temporal and geographical resolu-tion, and the shift in focus in evolutionarytheory towards discrete events show that itis both possible and necessary to look at thesingle origin model of modern humans in thecontext of evolutionary mechanisms. Theseare developed here in terms of evolutionarygeography, which is discussed in the nextsection.

EVOLUTIONARY GEOGRAPHY

Evolutionary geography may be describedas the branch of biology that investigatesthe role of spatial factors in the evolutionaryprocess. It differs from phylogenetic biogeog-raphy in that it operates at a variety ofscales and in that its main aim is not thebiogeographical reconstruction of phyloge-netic patterns but the investigation of theenvironmental (biotic and abiotic) and demo-graphic conditions for both vicariance (abi-otic range disruption) and dispersal eventsin the history of a lineage as well as theevolutionary causes and consequences ofsuch events.

Geography has been conventionally identi-fied as playing three major roles in the

evolutionary process. First, it acts by creat-ing the contingent factors that affect macro-evolutionary processes in terms of large-scale climatic and tectonic events. However,the hidden variance in macroevolutionaryevents strongly suggests that contingentmechanisms do not provide an adequateexplanation for the evolution of individualspecies and populations within them (Foley,1994, in press). The second aspect is its rolein promoting allopatry and consequentlyspeciation or differentiation. The allopatriceffect of geography on evolution is not re-stricted to a taxonomic level, for spatialrelationships at the subspecific, specific, andhigher levels may and have been found.However, a strong case may be made for therole of geography in shaping selective fac-tors that govern microevolutionary pro-cesses in terms of localized pressures onsurvival, range, and demography and there-fore on the evolution of populations or sub-species. Third, environmental variation isstrongly spatial in character and thus pro-vides the actual adaptive framework for thechanges that occur in populations (Foley, inpress). Evolutionary geography, in otherwords, uses spatial patterns to bring to-gether contingent, adaptive, and demo-graphic aspects of evolutionary change.

Three different dimensions—temporal,spatial and demographic— may be attrib-uted to any given population. The first ofthese relates to the duration of a populationas a distinct entity, from the moment of itsfounding or separation from the ancestralsource to its disappearance either by extinc-tion or by reintegration into the ancestral oranother population. Rates of divergencecould also be considered part of the temporaldimension of a population. The spatial di-mension relates to the geographic range of apopulation and its interaction with the envi-ronment, while population size and struc-ture make up the demographic parameters.Geography will affect and in many casesaccount for an important part of the varia-tion in all these. It thus becomes necessaryto understand the relationships betweengeography and the temporal and demo-graphic dimensions of a population in orderto identify certain principles that may helpclarify the evolution of diversity within a


species. The general principles of evolution-ary geography underlying the ways in whichnew populations become established, sur-vive, and/or disappear are considered below.

Population survival, range,and demography

A population of a species becomes anevolutionary entity upon the occurrence ofsome level of genetic separation from anancestral source; in most cases, this involvesa degree of allopatry. Such allopatric popula-tions may be formed without any dispersalson the part of individuals, such as whenbarriers are formed within a species range.The evolutionary outcome in such cases ofvicariance will depend on whether popula-tions become separated permanently or tem-porarily, with large or small daughter popu-lations, and with or without novel selectivepressures. On the other hand, the formationof allopatric populations following range ex-pansions (dispersals) results from popula-tion contraction due to an incapacity tosustain continuously the expanded range.Depending on factors like the duration of thefullest range expansion and the populationdensity supported by the extreme environ-ments occupied at that time, allopatric popu-lations resulting from the breakup of thisrange will be under the influence of bothnew selective pressures and drift. Therefore,one of the first factors to be taken intoaccount in considering the evolution of apopulation is its geographical relationshipto its parental group—whether it lies withinthe overall range or not.

Once an allopatric population has becomeestablished, it may follow one of threecourses: maintain population stability, con-tract, or expand. The first of these dependsupon the original population size and itsachievement of a mortality-survival equilib-rium with the carrying capacity of the envi-ronment. In evolutionary terms, such a popu-lation represents a source of discretediversity, for it maintains its own trajectorywithout impinging upon those of other popu-lations of the species for as long as theallopatry is maintained (Fisher, 1930; Avise,1994). This is important, because the issuehere is not whether gene flow can occur butwhether it actually does, and this can be

independent of formal issues having to dowith the process of speciation. The secondcase, population contraction, is the obviousoutcome when mortality exceeds survival,which may take a population towards a newplatform of size in which equilibrium ismaintained or extinction occurs. Extinctionof populations that went through a period ofstrong genetic drift represents an importantloss of interpopulation diversity at the levelof the species. The last case, populationexpansion, may have two outcomes. On theone hand, if the population expands over itsoriginal range, it may again establish con-tact with the parental group and, dependingon the time since separation and the amountof differentiation acquired, be reintegratedinto a single form and thus disappear as anentity. This will result in an increase ofoverall intrapopulation variance. On theother hand, if the population expands intonew territories it may, by subsequent con-traction, give rise to the whole process ofseparation that originated it in the firstplace, originating allopatric populations nowseparated by two branching events from theparental source. An important aspect of thisprocess is that in the sequence of populationa expanding and through subsequent con-traction forming two allopatric populations,a and b, and later population b expandingand through subsequent contraction form-ing allopatric populations b and c, depend-ing on the amount of change (due to eitherselection or drift) that took place during theestablishment of b as a distinct entity, thedifferences between a and c may be verysignificant. Particularly in the case of thesubsequent extinction of b, the relationshipof c and a may be unclear. Therefore, thesecond factor to be taken into account whenconsidering the evolution of a population isthe duration of that population as a localizedunit and its role in subsequent substructur-ing of the species.

A population’s response to selection willdetermine whether it will expand or con-tract and thus the conditions for isolation orcontact. Both contractions and expansions(dispersals) can have major evolutionaryconsequences. Although the causes of con-tractions are likely to be ultimately ecologi-cal and can occur both as part of an expan-


sive process and independently, theirprimary consequences lie in the greaterprobability of genetic change occurring insmaller and more isolated populations. Popu-lations that maintain a private trajectorywithin the species due to isolation representa temporary stable situation, the outcome ofa discrete branching event with the poten-tial for allopatric speciation. Nonetheless, itis dispersals and expansions that bring popu-lations into new territories and in contactwith other populations of the species orclosely related species, affecting existing pat-terns of diversity (Fig. 1).

Range expansions are likely to occur as aresult of the interaction between the charac-teristics of the population and the nature ofthe environment. Either or both may change.Where just the environment changes, theremay be increased population density with-out expansion (a new carrying capacity equi-librium) or range expansion as the result ofshifting barriers as particular environmentsthemselves expand. In either case, the re-sult is demographic changes which main-tain the relationship between resource ex-ploitation and available resources. This kindof fluctuating demography must be the normin evolutionary time. These outcomes, eitherincreased density without range expansionor expansion into new habitats, may alsoresult when some element in the behavior ofthe population changes as a result of someselective shift (e.g., a technological or adap-tive development). However, these are quali-tatively different. The establishment througha behavioral change of a new carrying capac-ity equilibrium within the occupied environ-ment or the occupation of ecologically newenvironments implies a change in resourceexploitation that removes existing barriers(either in terms of dietary composition orresource acquisition). These events are likelyto be rare in comparison. Finally, it is alsopossible for changes in the environment andthe behavior of the population to occur inter-actively.

The key point is the link between demogra-phy and spatial distribution and hence thegeographical nature of evolutionary pro-cesses. Environmental and behavioralchanges induce changes in both populationdensity and carrying capacity, and, after a

new ecological equilibrium is restored,changes in the spatial relationships betweenindividuals, groups, and populations willhave occurred. Such changes affect the cost-benefit ratios of adaptive strategies. How-ever, independent of the immediate effects ofgreater population density or of a greaterexploited area, environmentally inducedchanges in population demography will besubject to the stability of the new environ-mental conditions. Typically, these greaterdemographies and/or areas would not besustained under climatic deterioration, re-sulting in contraction and even populationcrashes. Depending on the magnitude andduration of the contracted phase or bottle-neck, such successive demographic expan-sions and contractions within the history ofa lineage may increase the rate of thatlineage’s divergence due to recurrent peri-ods of drift. On the other hand, it is theappearance of new modes of exploitationthat may transcend particular environ-ments and thus allow significant range ex-pansions or dispersals and occupation of anew environment with the potential for sta-bility of occupation independent of environ-mental fluctuations. For example, Plioceneand Pleistocene hominid species differ intheir relationship between species diversityand range size, paralleling primate and car-nivore patterns, respectively (Foley, 1991).Thus, it may be inferred that the habitualexploitation of a more carnivorous diet earlyin the Pleistocene temporarily removed alevel of environmental barriers that allowedthe dispersal of hominids far beyond theirsub-Saharan range and the establishment ofhominid populations in tropical Asia(Gamble, 1993; Foley, 1991, in press), withmajor consequences for the subsequent evo-lution of the lineage’s diversity. Therefore,the third factor to be taken into accountwhen considering the evolution of a popula-tion is whether an observed population ex-pansion is associated solely with environ-mental changes (either by changing therange of that particular environment or byincreasing resource availability) or with sig-nificant changes in subsistence that led tothe dispersal of the population into an alto-gether different environmental niche.


Therefore, the three key considerationsare 1) the geographical relationship betweenparent and daughter populations, 2) thelongevity of the population and its subse-quent role in further substructuring anddiversification, and 3) the relationship be-tween environmental change and behav-ioral innovations in relation to range expan-sion.

MODERN HUMAN DIVERSIFICATION

If geographical factors play a significantrole in the evolution of populations in gen-eral, how have they affected the particularcase of modern human evolution? This sec-tion attempts to integrate the principles of

evolutionary geography in the formulationof interpretative hypotheses for specificpoints in the evolutionary history of hu-mans. Two of these points will be addressed:first, the phylogenetic relationship of Nean-derthals and modern humans and, second,the ancestral bottleneck in modern humanhistory and the establishment of modernpopulations beyond a sub-Saharan Africanrange.

Neanderthals and modern humans

Neanderthals represent a group ofhominids that may be identified morphologi-cally by a number of apomorphic traits(Klein, 1998; Rak, 1986, 1993; Stringer and

Fig. 1. A: Relationship between the phylogenetichistory of populations and spatial distributions illus-trated in terms of two populations within an evolvinglineage. The top part of the diagram shows the phyloge-netic relationships, the bottom half a schematic represen-tation of population distribution and size. The parentpopulation (lighter shading) gives rise to a daughterpopulation in all examples. However, the outcome variesaccording to changes in spatial distribution of bothparent and daughter populations. In some cases, bothpersist at varying scales, in others only one, eitherthrough extinction or replacement or else through resorp-

tion back into a single population. B: Relationshipbetween phylogenetic history and evolutionary geogra-phy in a single complex example. Over time (t1–t9), thepopulation expands and contracts and becomes frag-mented or homogenized. This can happen repeatedly.Observations of diversity will vary according to the timeslice, and at any one time the overall diversity will be acumulative palimpsest of historical changes in distribu-tion. This model does not take into account the possibil-ity of small-scale background gene flow but emphasizesdispersal events and population contractions/extinc-tions.


Fig. 1.


Gamble, 1993; Trinkaus, 1987; Trinkaus andHowells, 1979). Because of their compar-atively rich record, temporal and spatialdimensions may also be attributed to themwith some certainty. The first forms thatpossess the suite of features that came tocharacterize the group appear during thelast interglacial (or stage 5 of the marineisotope climatic sequence) (Saccopastore,Krapina), but these features are found inmosaic form in fossils from 200 Ka onwards(Biache, La Chaise-Suard, La Chaise Bour-geois-Delauney) (Stringer, 1995). Nean-derthal traits have also been identified inearlier remains—Swanscombe, Steinheim,Atapuerca Sima de los Huesos—but theprecise dating of these remains is uncon-firmed. Nevertheless, we may infer that theselective pressures acting upon these traitsto create the combination of features thatresults in ‘‘a Neanderthal’’ were those im-posed by the harsh environments of stage 6(200 to 125 Ka). This is consistent with theirbody proportions, which show adaptationsto very cold climates (Ruff, 1994). ThatNeanderthals and their specific traitsevolved in Europe contemporaneously withthe evolution of modern humans in Africa istherefore well supported by fossil evidence.The question arises about where the ances-tors of the populations that evolved thedistinctive Neanderthal traits were, and fourpossible answers exist (Fig. 2).

The first (Fig. 2A) is that Europeanhominids had a long-term local evolutionarytrajectory, with continuity from the firstoccupation of the continent—some 800,000years. This model is based on the recentdiscovery of early Middle Pleistocene fossilsin the site of Gran Dolina, Atapuerca, Spain,described as a distinct species (H. anteces-sor) and the interpretation of aspects of theirmorphology as evidence for long-standingcontinuity towards Neanderthals (Bermu-dez de Castro et al., 1997). Three criticismscan be made of this model, however. The firstis that the present record of antecessor com-prises juvenile remains, and therefore themorphology represents both ontogenetic andphylogenetic variation. Second, the otherEuropean hominid fossil from the period 800to 500 Ka (Ceprano, Italy) has been de-scribed as H. erectus (Ascenzi et al., 1996),

without any particular affinities towardseither Neanderthals or modern humans.And finally, palaeontological and archaeologi-cal data suggest periods of important subse-quent exchange withAfrican hominids, argu-ing for important discontinuities andexternal influences in the European MiddlePleistocene record.

The second possibility (Fig. 2B) is that thelate Middle Pleistocene population of Eu-rope ancestral to Neanderthals had a localorigin in the earlier European Middle Pleis-tocene archaic population (composed of fos-sils like Arago, Bilzingsleben, Boxgrove,Mauer, Petralona, Steinheim, Swanscombe,Vertesszollos). There are similarities be-tween this group and the contemporary Afri-can archaic population (composed of fossilslike Bodo, Kabwe, Elandsfontein, Ndutu),like reduced superstructural development,facial projection, and increased endocranialvolume, although postcranially they retainplesiomorphic traits like an external iliacbuttress, large cortical thicknesses, andfemoral shaft width (Rightmire, 1996; Ruffet al., 1993; Stringer, 1995). The similaritiesbetween the European and African mid–Middle Pleistocene fossils have been takento indicate common ancestry and led to theproposal that these fossils, previously calledby the phylogenetically unhelpful name ‘‘ar-chaic’’ Homo sapiens, represent a new spe-cies, Homo heidelbergensis (Groves, 1994;Rightmire, 1988, 1996; Stringer, 1993). Thisspecies would have had an African origin inthe early Middle Pleistocene, with the fossilof Bodo representing the earliest knownspecimen (dating to ,600 Ka [Clark et al.,1994]). The appearance of African animalspecies in southwestern Asian biotas around500 to 450 Ka (Tchernov, 1992a) and the firstappearance in Europe of the Acheulean(mode 2)2 archaeological tradition from Af-

2The archaeological terminology of Clark (1968) is used here.He suggested that stone tool assemblages, regardless of theirtypological details, could be grouped into a series of broadertechnological modes that can be defined as follows: mode 1,chopper tools and flakes; mode 2, bifacially flaked hand axes,usually struck off large flakes; mode 3, tools made from flakesthat have been struck from prepared cores; mode 4, tools madefrom blades, often with reduced platforms; mode 5, microlithicflakes and tools. Mode 1 comprises the Oldowan and persistent


rica (Klein, 1995) are further evidence forthe dispersal of faunas, containing hominids,from Africa into Eurasia at this time (Klein,1995; Foley and Lahr, 1997). As African H.heidelbergensis gave rise to the late MiddlePleistocene African population ancestral tothe first modern humans (Brauer, 1989,1992; Rightmire, 1989; Stringer, 1989), theNeanderthal and modern human lineageswould be separated by at least half-a-millionyears. This hypothesis has two implications.First, periods of contact between Africa andEurope during the approximately 800 Ka ofglacial cycles were rare and fortuitous. Sec-ond, there must have been large levels ofparallelism, particularly in terms of brainsize and behavior, in the evolution of theNeanderthal and modern lineages.

The third possibility (Fig. 2C) is that thelate Middle Pleistocene population of Eu-rope ancestral to Neanderthals and the lateAfrican Middle Pleistocene population ances-tral to modern humans have a closer com-mon origin. This model is based on theobservation that Neanderthals, late Africanarchaic, and early modern humans sharedthe same archaeological tradition (mode 3industries). This tradition was not presentin Africa over half-a-million years ago whenthe second hypothesis would posit a commonancestor. Mode 3 technologies would thushave had to evolve independently, once inEurope and once in Africa, or else therewould have had to be cultural exchange withno genetic admixture over a long period oftime. An alternative explanation is thatthere was a dispersal of populations withLevallois technology (mode 3 industries) fromAfrica to Europe around 250 Ka (the date ofthe fossil from Florisbad, found in associa-tion with Middle Stone Age/mode 3 artefacts[Grun et al., 1996]), when interglacial condi-tions would have again facilitated hominidand faunal dispersals out of Africa (Foleyand Lahr, 1997). This hypothesis has threeimplications. First, dispersal events be-

tween Africa and Europe would have takenplace several times as certain processesduring glacial episodes temporarily removedgeographical barriers and allowed popula-tion expansion. Second, the morphologicalsimilarities between European H. heidelber-gensis and late archaic hominids directlyancestral to Neanderthals reflect a form ofiterative evolutionary process by whichshared traits represent homoplasies, espe-cially facial features associated with coldadaptation. Third, the behavioral parallel-isms between Neanderthals and modernhumans as observed in the archaeologicalMiddle Palaeolithic/Middle Stone Age re-cord (mode 3) reflect synapomorphic cogni-tive change.3

Finally (Fig. 2D), it is possible that therewas in fact continuous contact, gene flow,and exchange of populations between Africaand Europe throughout the middle Pleis-tocene and as such no relatively discreteevents as implied by the previous models.However, such a model is largely inconsis-tent with both the palaeontological and ar-chaeological divergences that can be seen, aswell as with paleoclimatic and paleogeo-graphical reconstructions which imply onlyintermittent contact.

Evolutionary geography provides a frame-work for assessing these competing hypoth-eses. The key element is the conditionspromoted by glacial cycles. Although impor-tant cooling of the Earth’s climate began atthe end of the Pliocene (Denys, 1985;Loubere, 1988; Rea and Schrader, 1985),cyclical glacial fluctuations are believed tohave started around 800 Ka (Roberts, 1984;Shackleton, 1987). The first full glacial stageis recognized in the marine sequences asstage 22, within the Matuyama subchroneand before the Jaramillo event, and there-

Asian pebble tool tradition; mode 2 refers primarily to theAcheulean of Europe, western Asia, and Africa; mode 3 is theMiddle Stone Age in Africa and the Middle Palaeolithic (i.e.,Mousterian and Levallois technology) of Europe; mode 4 is theUpper Palaeolithic of Eurasia and the Middle East, while mode 5covers a global range of late and post-Pleistocene Later StoneAge and Mesolithic assemblages. See Foley and Lahr (1997) for adiscussion of the mode system of archaeological classification.

3This model interprets the development of prepared coretechnologies as a significant phylogenetic and functional eventand posits that the distribution of prepared core technologies asthey develop and evolve during the later Pleistocene reflects bothan apomorphy of a particular population and a unique evolution-ary event. A less extreme interpretation would be that preparedcore technologies developed relatively rarely, spread by a mix-ture of diffusion and population movement, and thus still providea population marker, albeit one less tied into technology. Analternative view would be that prepared core technologies de-velop many times independently and therefore do not serve as apopulation or behavioral marker. The case for treating mode 3technologies as phylogenetically significant is considered in fullby Foley and Lahr (1997).


Fig.2.

fore between 900 and 790 Ka. The succeed-ing glacial cycles are similar in character(i.e., show the slow buildup of continental icesheets and a rapid period of deglaciationfollowed by a warm interglacial stage). How-ever, they differ markedly in degree, extent,timing, and rate of glacial growth, as shownby the details provided by marine isotopecurves (Malatesta and Zarlenga, 1988;Sachs, 1973; Sarntheim et al., 1986; Shack-leton, 1987; Zimmerman et al., 1984) (seeFig. 2). In spite of these differences, theywere cyclical events with recurrent out-comes which affected equatorial and north-ern latitudes in predictably different ways.Maximum cold in the north, with its result-ing reduced areas and southward shift ofclimatic belts, translates globally into maxi-mum coolness and low sea-level stands andespecially aridity in many parts of the trop-ics. This process is followed by the release ofwater trapped in the northern hemisphereglaciers, which is responsible for the globalrise in sea level and for pluvial and high lake

level short episodes in equatorial regions(Bradley, 1985; Hamilton, 1976; Hooghiems-tra and Agwu, 1988; Ritchie and Haynes,1987; Street and Grove, 1979). These fluctua-tions have specific consequences for Africanand European faunal geographical ranges(Fig. 3).

Large mammalian faunas in both conti-nents undergo a period of range expansionduring interglacials, while only Eurasianfaunas seem to have shifted ranges duringglacial buildup (in Africa, extensive ariditycauses the contraction of available rangesand a level of isolation and endemism). Inthe case of Europe, interglacial faunal expan-sions associated with the retreat of ice andtundra occurred along the Eurasiatic plainsto the northeast and occasionally towardsthe southeast, reaching the Middle East(although the Taurus-Zagros mountain rangeand the interglacial forests of the Greek andTurkish peninsulas acted as important bar-riers to movement in this direction [Heintzand Brunet, 1982]). During glacial periods,European animal ranges shifted south-wards as continental areas became coveredby ice sheets and permafrost terrain. Atthese times, the Middle East acted as a culde sac, for these northern elements could notovercome the Saharan barrier at its maxi-mum extent during glacial stages (Tchernov,1992a,b,c, 1994). Therefore, the main direc-tion of Palearctic expansions was east-west,as reflected by past and present animaldistributions. In the case of Africa, popula-tion expansions were associated with in-creased moisture occurring particularly dur-ing the early phases of interglacials. Theseexpansions were also directional, as forestsexpanded equatorially and savannas in anortherly direction across the Sahara. Dur-ing these episodes, the Ethiopian faunalrange also encompassed the Sahara, north-ern Africa, and the Levant, which showsindications of savanna conditions (Struthiocamelus and Camelus dromedarius fossils[Payne and Garrard, 1983; Tchernov, 1992a]),while movement into Europe would reflect asubsequent dispersal if the Taurus-Zagrosbarrier were transcended. Therefore, themain direction of nonforest Ethiopian expan-sions was north-south, reaching into theLevant through the Sinai peninsula.

Fig. 2. Representation of four models for Neander-thal ancestry. The evolution of the Neanderthal popula-tions is dependent upon a model for the colonization ofEurope and the continuity of the European hominidpopulation. Four models are set out below against thecontext of the marine oxygen isotope core (Shackleton,1987) and Clark’s technological modes (Clark, 1968). A:Dispersal of H. erectus/H. antecessor from Africa withmode 1 industries and long-term regional continuitywithin Europe, resulting in the evolution of EuropeanMiddle Pleistocene populations. Affinities of these andAfrican hominids, both in morphology and behavior,would represent parallelisms. B: Dispersal of H. erec-tus/H. antecessor which does not result in the perma-nent occupation of Europe. Subsequent dispersal in themid–Middle Pleistocene by H. heidelbergensis with mode2/Acheulian tradition from Africa, resulting in the estab-lishment of African and European lineages ,500 Ka,which later differentiate in modern and Neanderthalpopulations. Behavioral and morphological (encephaliza-tion) similarities between modern humans and Neander-thals would represent parallelisms. C: Dispersal of H.erectus/H. antecessor which does not result in thepermanent occupation of Europe. Subsequent dispersalin the mid–Middle Pleistocene by H. heidelbergensiswith the Acheulian tradition from Africa, followed byanother dispersal episode of late Middle PleistoceneAfrican hominids (H. helmei) with mode 3/Middle Palaeo-lithic industries , 250 Ka, resulting in the establish-ment of the immediate ancestors of Neanderthals. Mor-phological similarities between mid– and late MiddlePleistocene fossils in Europe would represent parallel-isms or admixture within Europe. D: Continuous dis-persal of populations across the Mediterranean from H.erectus/H. antecessor, with no marked discontinuities inthe Afro-European populations through the Middle Ple-sitocene.


These expansions are reflected in MiddlePleistocene fossil assemblages of Europeand especially the Middle East (Tchernov,1992a,b,c; Turner, 1984), in which the ap-pearance of African, Paleartic, and Oriental

elements reflects different phases withinglacial cycles. Although there are very fewmid–Middle Pleistocene palaeontologicalsites in the Levant (Gesher Benot Ya’acov,Give’at Shaul—dated to approximately 400

Fig. 3. Schematic representation of the effects of a glacial cycle (slow buildup of continental ice sheetsin high latitudes followed by rapid deglaciation and a relatively short period of interglacial conditions) onAfrican and European faunas.


Ka or stage 11, the beginning of the longInterglacial phase known in terrestrial se-quences as the Holstenian/Hoxnian), theseclearly show evidence of Afro-Eurasian bi-otic exchange (Geraads and Tchernov, 1987;Hooijer, 1959, 1960; Tchernov, 1992a). Unfor-tunately, the number of later Middle Pleis-tocene sites is also small, and their precisedating less certain. The faunas they containshow an influx of Palearctic elements (likeTalpa, Sciurus, Capreolus, Lepus europaeus,Microtus guentheri, Ursus arctos, Mammu-thus primigenius, and Felis syllvestris[Tchernov, 1992a,b]). The sites, associatedwith the geographically restricted Acheulo-Yabrudian (Zuttiyeh, Tabun E) have beententatively dated to the end of stage 7 andstage 6 (220/200 to 150/140 Ka) (Bar-Yosef,1992a,b). The Tabun D levels of the Tabuncave have also been dated to the end of stage6 (Bar-Yosef, 1992a,b, 1994), and it also haspalearctic elements, including recent Euro-Siberian species (Tchernov, 1992a,b). Theassemblage at Qafzeh both lacks thesePalearctic elements present in Tabun E andD and has a large number of East Africansavanna and Arabian species (like Arvican-this ectos, Mastomys batei, Gerbillus dasyrus,Suncus murimus, Alcelaphus busephalus,Equus tabeti, E. africanus?, Struthio cam-elus, and Camelus dromedarius as well assome Eurasian forms like Dicerorhinus hemi-toechus and Capra aegagrus [Tchernov,1992a,b]). It represents evidence of a shortperiod during which the Middle East was againthe northernmost limit of the African biomeand is consistent with Qafzeh’s dating to thelast interglacial, or stage 5 (Bar-Yosef, 1992a,b;Valladas et al., 1988; Schwarcz et al., 1988).The faunas of Hayonim and Kebara show againthe prevalence of Palearctic elements, consis-tent with their stratigraphic position withinthe last glacial cycle (Valladas et al., 1987).

Therefore, significant dispersals of Afri-can faunas into the Middle East occurred atleast twice: first during the mid–MiddlePleistocene (Holstenian/Hoxnian intergla-cial, stage 11) and later during the earlyUpper Pleistocene (Eemian/Ipswichian inter-glacial, stage 5). However, three facts indi-cate that this reconstruction is incomplete.First, the richer European record shows theintroduction of African elements in the early

Middle Pleistocene (Cromerian or stage 19),like Panthera leo and Crocuta crocuta(Turner, 1984), an event that is not recordedin the Middle Eastern sequence. Second, theMiddle East lacks palaeontological sites thatmay be attributed to stage 7 (,250 Ka),4when mode 3 technology seems to appear inthe European archaeological record. Third,the very ephemeral presence of African spe-cies in the Skhul deposits (Tchernov, 1992b)may indicate very short-term shifts of thefaunal ranges that are nevertheless signifi-cant for the reconstruction of hominid dis-persals.

Two conclusions relevant for the hypoth-eses of Neanderthal ancestry outlined abovecan be drawn from the palaeogeographicaldata. First, instead of rare and fortuitousevents, periods of contact between Africanand Eurasian biomes are to be expected aspart of glacial cycles, though with differentextents depending on the specific characterof each cycle. Second, the process is one-way;the direction of movement was always fromAfrica to Eurasia. Eurasian elements thatexpanded into the Levant at the onset ofcolder climates did not permeate into sub-Saharan faunas throughout the period con-cerned, reaching in a few occasions as far aseastern North Africa, or rarely the Maghreb(Jaeger, 1975; Tchernov, 1992a). In terms ofMiddle Pleistocene hominid movements, wemay therefore expect African dispersals intothe Jordan valley to have taken place sev-eral times in association with the early partsof interglacials (stages 19, ?15, 11, ?9, 7a 17b, 5e) (Fig. 4).

The biogeographical evidence would thussuggest that hominids, adapted to moretropical environments, would have expandednorthwards as far as the Middle East asthese habitats themselves expanded duringearly phases of interglacial episodes. Theseexpansions would have consisted of popula-tions tracking the fluctuations of their na-

4Tchernov (1992b) attributes a stage 7 date to Oum Qatafa.The fauna of this site does not contain Palearctic elements(Lepus, Talpa, Sciurus), and the micromammals are most compa-rable with those of the Tabun G levels (Bate, 1943) but which,under the new chronology for the Tabun sequence, could be older(Bar-Yosef, 1992a,b). The first intentional use of Levallois tech-nique (mode 3 technology) within what are called Upper Acheu-lean Levels in the Middle East has a stage 7 date—at the site ofBerekhat Ram, underlying a layer of lava dated K/Ar to 233 Ka(Goren-Inbar, 1985).


Fig.4.


tive habitats. However, it may be arguedthat a combination of biological and behav-ioral evolutionary novelties allowed, in atleast four cases, the invasion of Europe,which would have involved breaking intonew habitats. These four instances would bereflected in the first appearance of hominidsin Europe ,800 Ka, that of H. heidelbergen-sis and the mode 2 Acheulean tradition,500 Ka, that of late archaic hominids andmode 3 technology ,250 Ka, and that ofmodern humans with Upper Palaeolithictechnology ,50 Ka. If primary dispersalsconsist of population expansions in responseto an enlarged distribution of native habitat,then the colonization of Europe representedsecondary dispersals across significant habi-tat boundaries. These secondary dispersalswould have been by genetically distinct popu-lations, as they would have occurred frompopulations in northeastern Africa and theMiddle East that were already peripheral toand distanced from the original ancestralAfrican source. Once in Europe, hominidswould have become subsequently more spe-cialized under allopatric conditions as theyresponded to the selective pressures posedby the onset of glacial climates.

If this reconstruction were correct, it wouldbe most consistent with the third hypothesisregarding Neanderthal ancestry posedabove: that Neanderthals and modern hu-mans share a recent common ancestor withinthe last 250,000 years and the cognitivedevelopment represented by the implemen-tation of Levallois core preparation (Foleyand Lahr, 1997). This view is also consistentwith the mtDNA data from the Neanderspecimen. The history of a population andthat of a gene differ in their reflection ofdemographic parameters; the time of coales-

cence will precede by x generations the timeof population vicariance (Fig. 5). The coales-cence of human and Neanderthal mtDNAlineages ,500 Ka (approximately the timeof separation of African and European H.heidelbergensis) would suggest that the sepa-ration of the population ancestral to bothhumans and Neanderthals occurred sometime afterwards (Krings et al., 1997), consis-tent with a later dispersal, as reflected inthe Middle Stone Age/Middle Palaeolithicarchaeological records.

The model described above, derived fromevolutionary geography, suggests that thereis an additional layer of Afro-European dis-persal in the evolutionary history of Homothan is usually recognized. Evidence for thislayer is mainly archaeological and palaeon-tological, but it also finds support in thehominid fossil record. The immediate ances-tors of the ancestors of European Neander-thals would have dispersed within and out ofAfrica during stage 7 or even possibly duringthe main interstadial of stage 8. Fossils likeFlorisbad, Eliye Springs, and Guomde wouldbe representatives of this population in sub-Saharan Africa, while those of Djebel Irhoudin North Africa, Tabun D in the Middle East,and the diverse group of Atapuerca Sima delos Huesos (currently dated to ,300 Ka, butthis date is under revision [Stringer, 1995]),Pontnewydd, and Ehringsdorf in Europe(the only remains dated to stage 7 [Black-well and Schwarcz, 1986; Green, 1984])would represent descendants from this dis-persal episode. These remains, which wehave called Homo helmei (Foley and Lahr,1997), share a number of features that havelong made their taxonomic affinities ambigu-ous, including a level of encephalization notobserved in the earlier mid–Middle Pleis-tocene hominids (Ruff et al., 1997)5 (Fig. 6).We would expect increasing specializationand decreasing diversity in Europe from 250to 100 Ka (stage 6), when the Neanderthalmorphological pattern is selectively fixed, as

5The species name Homo helmei as used here differs incomposition from that of Stringer (1996b) by specifically includ-ing both African and European hominids of stages 8, 7, and 6associated with mode 3 technologies. The remains from Sima delos Huesos, Atapuerca, do not have associated archaeology andare thus only tentatively included in the group. Similarly, thefossil of Reilingen, Germany, which has been interpreted asshowing Neanderthal features, has no stratigraphic association(Dean et al., 1994).

Fig. 4. Palaeoclimatic information for the last1,000,000 years as derived from deep-sea cores and atentative terrestrial correlation. Sub-Saharan faunas,which dispersed across large areas as savanna habitatsexpanded during early phases of interglacials, couldhave reached the Levant at the end of stages 19 (,790Ka), 12 (, 408 Ka), 10 (,336 Ka), 8 (,145 Ka), and 6(,128 Ka). These expansions and their association withpalaeoanthropological remains are recorded in the Le-vantine sequence for the end of stages 12 and 6, butthose of stages 19 and 8 are indicated by faunal andarchaeological evidence in Europe. (Oxygen isotope datafrom N. Shackleton.)


seen in fossils like Biache, La Chaise-Suard,La Chaise-Bourgeois Delauney, Krapina, andSaccopastore. As it is hypothesized thatfossils like Eliye Springs and Florisbad aremore closely related to the European speci-mens from stage 7 than the earlier Euro-pean sample (Petralona, Arago, Versteszol-los, Bilzingsleben, Mauer, Steinheim,Swanscombe), the ‘‘Neanderthal’’ featuresobserved in some of the latter remains (e.g.,the face of Arago 21, features of the Arago 2mandible, features of the Swanscombe occipi-tal (undated but associated with Acheulean[Barton & Stringer, 1997]), and the facialprognathism of Atapuerca Sima de los Hue-sos AT-5 [Arsuaga et al., 1993]) would repre-sent homoplasic specializations occurring asadaptations to periglacial European condi-

tions. If persistence of Acheulean traditionsis an indication that earlier Middle Pleis-tocene populations did not disappear fromEurope during stages 7 and 6, the likelihood,character, and degree of interaction amongH. heidelbergensis and this later archaichominid population becomes an interestingevolutionary problem. Finally, behaviorallyNeanderthals should share more with theAfrican descendants of Florisbad, includinganatomically modern humans, than they dowith the early Middle Pleistocene hominidsassociated with mode 2 technologies andthus the claims for derived behavior amongthem are far less anomalous.

Recent discussions have focused on therelationship between the evolution of mod-ern humans and the extinction of Neander-

Fig. 5. Schematic representation of the relationship between the population history of humans andNeanderthals and mtDNA genealogy highlighting the likelihood that the time of mtDNA coalescencebetween a Neanderthal and modern lineages preceded population vicariance, whereas the time ofcoalescence of human mtDNA, Y-chromosome loci, and microsatellites could coincide with the demo-graphic bottleneck that separated early modern humans from late archaic African hominids.


Fig. 6. Variation in body mass and cranial capacity in African and European Homo. For each group of fossils, hereclustered as H. erectus, H. heidelbergensis, H. helmei, H. neanderthalensis, early H. sapiens, and recent H. sapiens,the estimated body mass (in kilograms) is plotted on the left and the measured or estimated cranial capacity (in cubiccentimeters) on the right (data from Ruff et al., 1997 [www.nature.com]). Encephalization quotients (EQs) were notcalculated given the paucity of associated cranial and postcranial remains, particularly for the Middle Pleistoceneremains, but the relation between average body mass and average cranial capacity is represented by the thicker bar.However, the range and mean of body mass and cranial capacity in the various groups clearly shows the increasedbrain volumes observed in the late Middle Pleistocene specimens (here grouped as H. helmei in terms of theirassociation to mode 3 archaeological remains) in relation to earlier hominids. The relatively larger body mass ofNeanderthals in relation to modern humans (early and recent) results in their comparative smaller encephalization(Ruff et al., 1997).

thals. However, in evolutionary terms, Nean-derthal extinction is not the outcome of theevolution of modern humans, which hadoccurred some 100,000 years before in an-other continent, but of the dispersal of aparticular regional population of humanswith powerful biological and technologicaladvantages. The extinction of Neanderthalsrepresents the extinction of one among manyregional populations that competed for spaceand resources, although, as they repre-sented the latest surviving nonmodernhominids, it affected global levels of hominiddiversity to a greater extent than most. Onthe other hand, the evolutionary geographyof African and European Middle Pleistocenehominids suggests an intimate relationshipnot between the evolution of modern hu-mans and Neanderthal extinction but be-tween the origins of both modern humanand Neanderthal lineages.

Ancestral bottlenecks and theestablishment of modern humans

outside sub-Saharan Africa

Modern human genetic diversity is, rela-tive to that of a closely related species likePan, very small. This has been interpretedas the result of a recent loss of variability—ademographic bottleneck (see discussionabove). Although human populations differin their levels of diversity (Africans beingmore diverse than others in fast mutationloci), all humans share this overall lack ofdiversity in relation to other species, imply-ing that the main demographic bottleneckoccurred in the population ancestral to allliving humans. On the basis of the relation-ship between diversity, ancestral populationsize, and mutation rates, the approximatesize of the effective ancestral populationduring the bottleneck has been estimated as.10,000 individuals (Bowcock et al., 1991;Brown, 1980; Haigh and Maynard Smith,1972; Harpending et al., 1993; Jones, 1986;Hammer, 1995; Nei and Graur, 1984; May-nard Smith, 1990; Rogers and Jorde, 1995;Takahata et al., 1995; Wills, 1990). Othercalculations have led to the suggestion thatover the long term (the last 1 million years),the lineage ancestral to modern humans inAfrica fluctuated between 100,000 and40,000 individuals (Sherry et al., 1997; Taka-hata et al., 1995), and so the bottleneck

would have represented a reduction of be-tween 75–90%. Recent studies using pair-wise comparisons of mtDNA differences inhuman populations have suggested that thedistributions of these differences at a popula-tion level reflect the effect of very significantdemographic expansions between 70 and 50Ka (Di Rienzo and Wilson, 1991; Harpend-ing et al., 1993; Rogers, 1995; Rogers andHarpending, 1992; Rogers and Jorde, 1995;Watson et al., 1997). The different relativeposition of the peak of these distributionsbetween and within populations further sug-gests that the ancestral population had sub-divided into those ancestral to Africans,Asians, and Europeans before the expan-sions took place (Harpending et al., 1993;Rogers and Jorde, 1995).

Although a bottleneck is a demographicevent, it has both spatial and temporalcomponents that may strongly affect theoutcome. These can be phrased in terms ofthree questions. First, did the bottleneck inhuman history reflect a population reduc-tion into a number of small breeding popula-tions or a reduction into a single breedinggroup? Second, how can we explain thepopulation subdivision and relative isola-tion of the populations ancestral to Africans,Asians, and Europeans before the demo-graphic expansions reflected in the mis-match results? And third, are the differencesbetween large modern human clusters theresult of the long-term effects of small popu-lation size or of subsequent bottlenecks thataffected the proportion of shared ancestraldiversity?

Spatial structure of the ancestral popu-lation. The first question, that of thestructure of the population during the bottle-neck, can be formulated into two hypoth-eses. Both hypotheses imply demographicvicariance but differ regarding the numberof late Middle Pleistocene hominid popula-tions that survived such a period of popula-tion contraction. In the first case, the sub-Saharan African hominid population wouldhave divided into several geographicalgroups, some of which would have becomeextinct while others survived. The summedeffective population size of all those separatepopulations that survived would have to-taled less than ,10,000 people (i.e., each


subdivided population would have been verysmall) (Fig. 7, bottom). Rogers and Jorde(1995) estimated that if the ancestral popu-lation was structured, the sum of all groupscould not have been more than approxi-mately 4,000–5,000 genetic ancestors. Inthis model, survivorship would have beendue partly to the area occupied by eachreduced group and its resource potential andpartly to the evolutionary response of eachgroup to the selective pressures posed bystringent conditions as well as the interac-tion of these with the novelties introducedby genetic drift. As more than one of thesesmall groups would have survived to thepresent, the duration of the bottleneck be-comes important for estimating the processof drift in originating interpopulation diver-sity. If this hypothesis were correct, ob-served palaeoanthropological African diver-sity between 200 and 100 Ka could representtrue ancestral diversity.

The second hypothesis would postulatethat of all the hominid populations in sub-Saharan Africa undergoing contraction atthe time, only one survived (Fig. 7, top).However, this one group would have beenlarger, composed of .10,000 genetic ances-tors in continuous genetic exchange. Again,survivorship would have been related to theinteraction between the size of differentpopulations and the potential of differentAfrican environments for supporting smallhominid groups during a period of loss oflarger-scale ranges and social networks, butin this case the model suggests an effect ofminimum population sizes in populationextinction. The duration of the bottleneckbecomes important for estimating the effectsof drift in the ancestral population, theoutcomes of which would be shared by allliving humans. Although new selective pres-sures would have accompanied the processthat caused the bottleneck in the first place,the overall environmental component wouldhave been maintained, as differentiationwould have taken place over the range of theparental group. If this hypothesis were cor-rect, archaeological and hominid fossil diver-sity in Africa between 200 and 100 Ka wouldnot represent ancestral diversity but ratherthe diversity of several small distinct popula-tions, each under the effects of drift and local

selective pressures, but only one of whichwas ancestral to present Homo sapiens.

The two hypotheses lead to very differentinterpretations of the African 200 to 100 Kahominid fossil record, but they also point todifferent implications for the shared loss ofgenetic diversity observed in living humans.Recent simulations by A. Rogers show thatpopulation subdivision, with its generationof interpopulation differences, prevents theloss of diversity even during a major demo-graphic bottleneck (in these simulations,with subdivision into three groups, thechange from u 5 1,000 to u 5 1 (where u 52Nµ [N 5 effective population size and µ 5mutation rate]) results in almost no diver-sity loss (mean pairwise differences (mpd)change from 158.61 to 124.26), while thechange from u 5 1000 to u 5 1 with survivor-ship of a single group results in the loss of70% of the group’s diversity (mpd 5 47.23)[Ambrose, 1998; Rogers, personal communi-cation]). These simulations strongly suggestthat only one geographical population sur-vived this period of population contractionand that hominid African diversity in thelate Middle Pleistocene does not representtrue ancestral variability but that of a num-ber of groups, most of which later becameextinct. Only one, and perhaps or even prob-ably one not yet palceontologically sampled,is directly ancestral.

If the correct model for a bottleneck is thatof a single surviving population, then infra-African archaeological and palaeontologicalvariability becomes significant. Unfortu-nately, the fossil sample for most of theperiod concerned (stage 6) is nonexistent(from the very end of the period, all withdates approximating 130 Ka, there are thefossils of Omo Kibish, Ethiopia, and thecranium from Singa, Sudan, and the latearchaic fossil of Ngaloba, Tanzania). There-fore, an assessment of hominid morphologi-cal variability during the latest AfricanMiddle Pleistocene is restricted to an indica-tion that by the very end of the period earlymodern humans had evolved in at leastnortheastern sub-Saharan Africa, with thepossibility that late archaic groups were stillpresent. Archaeological diversity should bemore informative, as several Middle StoneAge (MSA) sites are known. However,chronological resolution is poor for much of


Fig. 7. Schematic representation of the two hypotheses of population structure during an extremebottleneck discussed in the text. Top: Population contraction results in the survival of a single refugium,which would have contained approximately 10,000 genetic ancestors. Bottom: Population contractionresults in a number of refugia, which would have contained less than 10,000 genetic ancestors (calculatedas ,4,300 people in all by Rogers and Jorde [1995]).


this time. What we know of the AfricanMiddle Stone Age (mode 3) is that it appearsaround 250 Ka and possibly somewhat ear-lier, from which time it is found in a numberof sites—in the late Acheulian Victoria Westtradition of Kenya and in Florisbad, south-ern Africa, where it is associated with a latearchaic fossil recently dated to ,250 Ka(Grun et al., 1996). In Kapthurin, Kenya,one of the few Middle Pleistocene sites witha radiometrically known sequence, the time,250 Ka coincides with the disappearanceof typical Acheulian (McBrearty et al., 1996).Those areas in sub-Saharan Africa wherethere is the early appearance of mode 3techniques were characterized by the over-all substitution of Acheulian industries gen-erally (McBurney, 1960; Phillipson, 1985).There is only one site that has been securelydated to stage 6—the Gademotta Formationin Ethiopia, where early prepared core arte-facts (M3) have been dated to 180 Ka (Wen-dorf and Schild, 1974). By the last intergla-cial (stage 5e), great diversification andregionalization of the stone tool assem-blages, broadly within what may be de-scribed as variants of the MSA, is observedthroughout Africa—the Howieson’s Poort insouthern Africa, the Bambatan in Zambia,the Mumba tradition in Eastern Africa, theSebilian along the Upper Nile, the Lupem-ban in western Africa, the Aterian of theMaghreb and Sahara, and the pre-Aurigna-cian of Lybia (Allsworth-Jones, 1993; Clark,1992; Deacon, 1989; McBurney, 1960; Vig-nard, 1923). All these show, besides regional-ization, certain technological innovations likeblades, small backed blades, tanged points,and harpoons but within a mode 3 contextand are consistent with the expansion ofearly modern humans within Africa at thistime (see discussion below). We are left withan almost complete lack of palaeoanthropo-logical evidence that can be attributed withcertainty to stage 6. This picture mightchange as more sites are found and dated.On the other hand, it may be that the lack ofstage 6 MSA sites, the disappearance of theAfrican Acheulian (in contrast to what isobserved in Europe), and the later expan-sion and diversification of the African MSAin stage 5 reflect the population contractionseen in the genetic data, from which only

one relatively large population, with novelbiology and behavior, survived and ex-panded at the onset of the last interglacial.

Population structure prior to UpperPleistocene expansions. Using empiri-cally obtained values of diversity, these com-puter simulations raise another issue. Theloss of variability through an ancestralbottleneck in a single breeding populationwould be very large but not as large as thatactually observed in and inferred from livinghumans. Results broadly concordant withempirically derived human mpds are ob-tained only by simulating various historiesthat include the effects of later subdivisionduring the small size phase and secondarybottlenecks (Ambrose, 1998).6 The issue ofsecondary bottlenecks brings us to the sec-ond question posed above: how the popula-tions ancestral toAfricans,Asians, and Euro-peans became subdivided before thedemographic expansions reflected in the mis-match results took place. In order to answerthis question, we must consider the tempo-ral and spatial context of the events involvedto integrate the genetic and palaeoanthropo-logical evidence.

The genetic evidence reviewed above indi-cate that a number of fast mutating genes,like mtDNA and Y chromosome microsatel-lite loci, show coalescent times between 180and 120 Ka, 154,000 for nuclear gene haplo-types (CD4, DM PLAT) (Tishkoff et al.,1997), 130,000–170,000 for global mtDNA(Wallace et al., 1997), 185,000 for nine siteson the Y chromosome (Hammer et al., 1997),and 112,000 6 34,000 to 123,000 6 39,000for 18 microsatellite markers on the Y chro-mosome [Pandya et al., 1997]), as well asages derived from Alu insertion polymor-phisms (137,000 6 15,000 [Stoneking, 1997]).The key question is what this congruity ofcoalescent times means in terms of popula-tion history. With regard to the Neander-

6The simulations performed by Rogers give the outcome ofthree scenarios. One of these posits that after the original loss ofdiversity the population subdivides into three and then expandsfrom u 1 1 to u 1 1,000 without further bottlenecks; the resultingmpd 5 13.36. The second possibility is a secondary bottleneckafter the subdivided population expands from u 5 1 to u 5 1,000,resulting in an mpd of 11.4. Finally, the last scenario would haveonly one population surviving the secondary bottleneck, result-ing in an mpd of 9.3 (Ambrose, 1998; Rogers, personal communi-cation).


thals, it was argued that the time of coales-cence of a given gene must precedepopulation divergence by x generations(Krings et al., 1997), an unknown number ofgenerations that disassociates the time ofcoalescence of a single gene from populationparameters. However, as the number of lociconsidered is increased, there will be anincreasing probability that their combinedhistory reflects population history (Aviseand Wollenberg, 1997). Therefore, the rela-tive contemporaneity of coalescent eventsbetween 180 and 120 Ka may be taken toreflect the probabilistic effect of a concomi-tant loss of lineage diversity in varioussystems associated with demographic con-traction and therefore a broad parameter ofwhen the ancestral bottleneck occurred. Thisperiod corresponds to a glacial phase, peak-ing around 130 Ka (stage 6). In ecologicalterms, population contraction reflects a re-sponse to conditions that lead to deathsoutnumbering births. In the absence of catas-trophes, the conditions that alter a birth-death ratio in a population are mainly eco-logical (reduced food availability), which canalso lead to social mechanisms associatedwith intergroup competition (warfare). Inequatorial regions, the ecological conditionsthat lead to food scarcity and increasedcompetition are related to periods of aridity,which occurred as part of the effects ofhigher latitude continental glaciation. There-fore, the ecological evidence is consistentwith the genetic estimates that the popula-tion ancestral to humans suffered a demo-graphic bottleneck during stage 6, possiblyculminating at the maximum glacial,130,000 years, from which only one geo-graphical refugium survived. Using the low-est recorded hunter-gatherer density (forthe !Kung, two individuals per 100 km2

[Kelly, 1995]), we find this ancestral popula-tion would have ranged over an area of atleast 700 3 700 km (approximately the sizeof Kenya).7

These considerations of the genetic evi-dence in the context of palaeoclimatic pat-terns lead to the conclusion that the bottle-neck at the base of modern human ancestry

lies in stage 6, the same time that theNeanderthals seem to have been evolving asa distinctive population. The timing of theancestral bottleneck is also consistent withthe available evidence on the morphologicalevolution of humans. If only one populationsurvived the ancestral bottleneck, thenchanges that occurred in this group wouldbe shared by all humans. Homo sapienscrania share a morphological pattern thatdifferentiates them from archaic hominids,the characteristics that make a skull mod-ern. The definition of modern humans is initself a controversial question (Brown, 1987;Day and Stringer, 1991; Kidder et al., 1992;Smith, 1994; Wolpoff, 1986), as the differ-ences acquired by human populations underallopatric conditions in the Upper Pleis-tocene mean that the proportion of featuresshared by all recent humans is small (Lahr,1996). Nevertheless, modern humans arecharacterized by a certain cranial shape(high vault in relation to vault length andbreadth), short facial height (secondarilychanged to a certain extent in recent Mongol-oids), a number of basicranial traits, a changeof shape in supraorbital superstructures,and a chin on the mandible. This morphologi-cal combination appears first in the fossils ofOmo Kibish from Ethiopia, dated to approxi-mately 130 Ka, and, from the perspective ofthe genetic data discussed above, wouldhave been the result both of selection actingon a decreasing population living with in-creasingly scarce resources and of the effectsof drift once population size decreased signifi-cantly.

Modern humans also share behavioraltraits not observed in the archaeologicalrecord of archaic hominids, even Neander-thals. These are related to flexibility, inven-tiveness, and perception of self (be it group-self or individual-self). The first is reflectedin the much broader use of raw materials(bone, antler, shell, ivory, etc.), the second inthe innovative solutions for practical prob-lems (blades, tanged points, composite tools,boats, bows and arrows, etc.), and the thirdin art and ornamentation. The difficultyarises in that these are mainly expressedtens of thousands of years after the firstappearance of morphologically modern hu-mans. This time lag has been interpreted asan indication that the earliest African Homo

7This area would correspond to ,10,000 individuals, whichrepresent more closely effective rather than census size, andconsequently an under-estimation of the area occupied by thepopulation.


sapiens were modern morphologically butnot behaviorally (Klein, 1992, 1995).

This discrepancy should be considered inthree perspectives. The first is that there aremany aspects of modern human cognitionand thought that are clearly under stronggenetic control and are universal. Lan-guage, with its deeply embedded syntax anduniform pattern of development, is one(Pinker, 1994). Since both genetics andpalaeoanthropology indicate the early subdi-vision of the modern human gene pool intopopulations that later colonized differentparts of the world, it should be inferred thatthe capacity for modern syntactical lan-guage must have been present in the veryearliest modern humans. Were it to havespread by later gene flow, the genetic struc-ture of human populations would have beenvery different. It has also been argued thatsocial and planning aspects of the actualmodern human dispersals out of Africa,which included the use of watercraft, repre-sent evidence of the universal human capac-ity to speak (Noble and Davidson, 1996). Thesecond is that the earliest modern groups doshow a number of novel behavioral traits—the persistent exploitation of certain marineresources, the first evidence of novel practi-cal solutions (blades in the Howieson’s Poorttradition of southern Africa (Deacon, 1989;Klein, 1994), tanged elements in the Aterian(Clark, 1993; McBurney, 1960; Wendorf etal., 1990), microliths in sites in the NileValley (McBurney, 1967), barbed points andharpoons at the Katanda sites in the Sem-liki Valley in Zaire [Brooks et al., 1995;Yellen et al., 1995]), and the earliest evi-dence of the use of ochre. These would implythat the biological cognitive changes thatunderlie shared human behavior had al-ready taken place. Finally, while the biologi-cal basis for modern human behavior wouldbe in place early, its material expressionwould vary in relation to local social andecological conditions, such as differing com-binations of individual mental attributes,social structure, technological pressure, andintra- and intergroup competition. The moreintense expressions of modern human com-plexity found in the later dispersals of popu-lations across both Africa and Eurasia wouldthus be the outcome of particular demo-graphic and socioecological histories rather

than fundamental biological shifts and inno-vations.

Secondary bottlenecks and the differen-tiation of human populations. Studiesof the pairwise differences in mtDNA within(mismatch distributions) and between (inter-match distributions) human populations in-dicate that human populations divided intoat least three groups that later expandedseveralfold, known as the Weak Garden ofEden Hypothesis. The subdivision wouldhave taken place around 100 Ka, and popu-lations would have remained small until theexpansions between 70 and 50 Ka (Harpend-ing et al., 1993; Rogers and Jorde, 1995;Sherry et al., 1994). The integration of thepalaeoanthropological evidence into thismodel poses an interesting question. Thebeginning of the last interglacial ,125 Ka(stage 5) was characterized by a period ofmarkedly increased rainfall, which resultedin the expansion of the range of equatorialforests and that of savannas over previousdeserts. At this time, the range of Africanfaunas reached northern Africa and theMiddle East, as shown by the presence ofsub-Saharan African species, including mod-ern humans, in the Levantine sites of Skhuland Qafzeh (Grun and Stringer, 1991;Stringer et al., 1989; Tchernov, 1992a; Valla-das et al., 1988; Vandermeersch, 1982) andof modern humans in southern Africa (DieKelders 1, Equus Cave, Klasies River Mouth,Sea Harvest, and the somewhat later BorderCave [Deacon, 1989; Grine and Klein, 1993;Grine et al., 1991; Klein, 1994; Morris, 1992;Rightmire and Deacon, 1991; Singer andWymer, 1982]) and the Maghreb, as shownby the fossil of Dar es-Soltan associated withthe Aterian (Hublin, 1993; Wendorf et al.,1991, 1993). All these early modern speci-mens show the changes in skeletal propor-tions and craniofacial and superstructuralshape that characterize Homo sapiens whilestill retaining some plesiomorphic traits andskeletal robusticity to a larger extent than isobserved in most recent populations(Churchill et al., 1996; Lahr, 1996; Lahr andWright, 1996; Pfeiffer and Zehr, 1996;Stringer, 1992). If this geographical expan-sion represented an early demographic ex-pansion of humans, then the pooled mis-


match and intermatch distributions shouldcoincide instead of the intermatch leadingthe mismatch waves, as is observed. Thisraises the issue of how to interpret demo-graphically the early geographical expan-sion of humans observed in the fossil record.

Two hypotheses can be proposed to ac-count for the fact that this early expansionof humans is not observed in the meannumber of pairwise genetic differenceswithin recent human groups. The first isthat the last interglacial expansion of mod-ern humans was genetically insignificant incomparison to the scale of the demographicexpansions around 70 to 50 Ka (estimated tohave been at least 100-fold [Rogers andJorde, 1995]) and thus invisible in geneticterms. Expansions are the result of either anincrease in population as available re-sources expand or a change in the mode ofexploitation that allows either more individu-als to survive in the same environment or tocolonize new ones. In the case of the earlyhumans of the last interglacial, the palaeocli-matic information regarding the expansionof habitats, together with the absence of achange in exploiting capabilities (as shownby the stability in the archaeological MiddleStone Age/Middle Palaeolithic record), sug-gests that there was no major change insubsistence strategies and that this earlygeographical expansion resulted from theexpansion of the environments being ex-ploited. By extrapolating from a modeledreconstruction ofAfrican environments 8,000years ago (Adams and Faure, unpublishedmanuscript) to those of 125 Ka and assum-ing that early humans could have occupiedareas of savanna and tropical grasslands ata relatively low hunter-gatherer density (5/100 km2) and areas of thorn-scrub wood-lands at a slightly smaller density (4/100km2), we reach a conservative estimate of,500,000 individuals as the size of thepopulation that could have ranged over thearea available during early phases of theinterglacial represented by stage 5 (with thesmallest values for ethnographic hunter-gatherers (2/100 km2), the number of pre-dicted individuals during the beginning ofthe last interglacial in Africa would be,225,000). However, Rogers and Jorde(1995) estimate that the effective size of the

subdivided modern population after thebottleneck was less than 66,000 (dividedinto at least three populations of ,20,000individuals each), while the postexpansionpopulation must have been composed ofmore than 300,000 adults. Therefore, eitherthe population estimates for occupation ofearly interglacial African environments arewrong by an order of magnitude (implyingthat MSA human populations could notachieve even the lowest densities of recenthunter-gatherers or that there were verysignificant gaps in the hominid distribution)or the hypothesis that this event should beinsignificant in terms of diversity is notsupported.

The second hypothesis to explain why theearly interglacial expansion of modern hu-mans is not represented in the genetic datais that, once conditions deteriorated andpopulations could not maintain the ex-panded range, peripheral groups contractedin size and became extinct at various pointsin the subsequent tens of thousands of years.Therefore, the increased diversity that wouldhave been generated by the demographicexpansion at this time was subsequentlylost through secondary bottlenecks and isnot represented in the mismatch data ofliving groups. Among the fossil populationsof early modern humans from the last inter-glacial, several seem to have subsequentlybecome extinct. In the Middle East, theearly modern population is replaced by Ne-anderthals after 70 Ka (Bar-Yosef, 1993). Innorthwestern Africa, the Aterian MSA tradi-tion (associated with the modern fossil ofDar es-Soltan [Hublin, 1993]) seems to havedisappeared before the appearance of theIberomaurusian in the area 22 Ka (Klein,1995). In southernmost Africa, the earliestmodern humans associated with the Howie-son’s Poort MSA tradition also seem to havesuffered a considerable reduction around 60Ka, when the area becomes virtually depopu-lated (Klein, 1992, 1994). However, not all ofthe peripheral populations would have be-come extinct. The later expansion in parts ofEurasia of modern humans with Upper Pal-aeolithic technology around 50 Ka is likelyto have been derived from one of theseperipheral populations. Its location is a mat-ter of debate; while the earliest Upper Pal-


aeolithic tools are found in southwest Asia,an area previously occupied by Neander-thals, the source area could lie equally innortheast Africa, the Arabian peninsula, oreven across towards Iran and northwestIndia. Other surviving peripheral popula-tions may have been in north Africa as wellas central and eastern Africa that wouldhave given rise to African and Asian groups.Therefore, the subdivision of the early mod-ern human gene pool would have resultedfrom this process of early expansion followedby fragmentation as early interglacial habi-tats contracted and barriers like the Saharadesert formed again. The extinction of sev-eral of these early populations, togetherwith a possible reduction of those that sur-vived, would explain why the early expan-sion of modern humans throughout Africadid not leave a signature in the mismatchdistribution of mtDNA pairwise differencesof living groups.

It should be noticed, however, that it couldwell be a combination of the expectations ofboth hypotheses that approximates theevents in stage 5. It is likely that several ofthe early modern localized populations thatwere formed within Africa after the expan-sion 125 Ka became subsequently extinct.However, it has also been suggested thatthese early modern humans, associated withMiddle Stone Age industries, could not sup-port demographic densities similar to morerecent hunter-gatherers, associated with theLater Stone Age, in the same area (Kleinand Cruz-Uribe, 1996). Therefore, it couldbe that the population estimates using re-cent hunter-gatherer densities are indeedgross overestimations, a fact that wouldonly increase the probability of group extinc-tion and reduction explored by the secondhypothesis above.

Therefore, the best interpretation of thepalaeoanthropological and genetic evidenceof the early history of our species wouldsuggest that the ancestors of humans under-went a population bottleneck sometime dur-ing stage 6 (200 to 130 Ka) that reducedthem to a single population of .10,000genetic ancestors; that around 125 Ka thisearly human population underwent a demo-graphic expansion that led to the occupationof a savanna belt along 10–15° latitude as

well as northern and southern Africa; thatsubsequent population contraction and ex-tinction led to the establishment of a num-ber of regional-local populations within sub-Saharan and northern Africa and furtherloss of diversity; and that these localizedhuman populations remained separate forsome 50,000 years before new expansionsoccurred. In other words, the ancestors ofEuropeans and Asians lived in Africa forsome 50,000 before they dispersed.

Human diversity within and out of Af-rica. This model for the early history ofmodern human evolution would explain sev-eral aspects of the palaeoanthropologicalrecord of humans outside Africa (Lahr andFoley, 1994). First, it explains the differ-ences in morphology observed at the time ofthe first appearance of modern regionalworld populations as resulting from inter-populational differences acquired during thephase in which populations were alreadysubdivided and still small (i.e., the featuresof the main human races would have beendefined by a combination of ancestral Afri-can diversity and diversity accumulated dur-ing allopatric conditions because of reducedpopulation sizes, evolutionarily frozen bythe expansion events). Second, it accountsfor the archaeological diversity observed, asit proposes the derivation of the southernAsian industries directly from African mode3 technologies, while the Upper Palaeolithicwould have resulted from a localized north-easternmost African development, whichcame to have a major impact in the dispersalof the population throughout Eurasia. Third,it would explain the early occupation ofAustralia through the dispersal of an east-ern African population along the southernAsian coast at a time when the Levantinecorridor was closed to African groups (60 to50 Ka, as suggested by the sites of Malaku-nanja and Nawabilla [Roberts et al., 1994]).The latter has recently received genetic sup-port from studies of Alu insertion polymor-phisms that show that Australian aborigi-nes are as distant to the ancestral source asrecent Africans (Stoneking et al., 1997).Finally, this model in its broader contextexplains both the evolution of modern hu-mans and their sister clade, the Neander-thals, within the context of a general theo-


retical framework rather than the result of aunique event.

DISCUSSION AND CONCLUSIONS

This paper set out to explore a singleorigin of modern humans in the context ofevolutionary theory, in particular the way inwhich the principles of evolutionary geogra-phy can be applied to the evolution to ananimal lineage, and through this providethe basis for formulating hypotheses aboutphylogenetic patterns.

Three broader theoretical issues in evolu-tionary theory were raised in the introduc-tion: the need to account for changes indiversity through origin thresholds, the needfor demographically based models of popula-tion diversification, and the need to considerthe effects of geography in interpreting evo-lutionary change. In this final section, wewill use the discussions presented above toaddress these points.

Dispersals of modern humans

This paper has derived two primary con-clusions about the role of dispersals in mod-ern human evolution and origins. The firstof these is that dispersals are one of theprimary evolutionary mechanisms, themeans by which successful species adaptand expand as their native habitats expandand break through into new environmentsand adaptive plateaus. The second is thatthe dispersal events underlying human di-versity are detached from the processes lead-ing to the origins of the species. The latteroccurred during stage 6, while the formerare primarily associated with stages 5, 4,and 3. Furthermore, we have seen that thereare underlying biogeographical reasons, con-tingent upon the nature of glacial cycles,which result in hominid dispersals beingpredominantly from Africa and that suchdispersals have occurred.

The primary underlying basis for thispattern is that populations are expanding asthe habitat in which they can survive ex-pands and that, for climatic reasons, thisoccurs first in Africa during an interglacial.However, the question should be posedwhether there are specific behavioral factorsthat led to the success of the dispersals ofmodern humans. At this stage, it is impos-

sible to give any form of definitive answer,but a number of possibilities may be pro-posed. The first of these is that if there is adispersal based on a fundamentally new anddifferent cognitive capacity (such as lan-guage or symbolic thought), then this wouldbe the original stage 5 dispersals. Dispersalsoccurring after the fragmentation of thepopulation after the last interglacial wouldbe population-specific and therefore couldnot be based on fundamental biologicalchange such as language. Second, the earlydispersals in stage 5 and those occurringbefore stage 3 along the southern coast ofAsia may well have been specifically coastaland involved the use of certain marine re-sources, particularly shellfish (fish and birdsapparently not being exploited [Klein andCruz-Uribe, 1996]). Aquatic specializationsmay have provided a predictable resourcebase that, combined with a tendency tooverexploit easily obtainable resources andthe ability to move on, led to rapid popula-tion spread without major demographic ex-pansion. Third, the dispersal that is bestdocumented, that of the Upper Palaeolithicacross Eurasia and the Mediterranean, is ofspecific interest because it appears to occuragainst the grain of climatic change. There-fore, it may well be a dispersal associatedwith either social or technological innova-tions that gave the populations a majoradvantage. Large group size and social net-works may be proposed for the former, thebow and arrow for the latter. And finally, itshould not be forgotten that the presentinterglacial has seen a very large scale pat-tern of dispersals associated primarily withagriculture—dispersals that, as occurred instage 5, have radically altered the pattern ofhuman diversity.

Diversity through time

The reconstruction of the evolutionaryhistory of humans has traditionally beenfocused on events—the point of separation ofmodern and archaic hominids, the point oforigin of morphologically and behaviorallymodern humans, the point of expansion ofhumans out of Africa. However, these eventsare not evolutionarily discrete but ratherrepresent the outcome of demographic pro-cesses that affected the levels of population


diversity in ways that allow us to identifythem. We have argued that the contractionof African populations and their subsequentexpansion and dispersal into Eurasia haveevolutionary precedents and are to be ex-pected as part of the biogeographical changesof glacial cycles. This offers an interpreta-tion for the different evolutionary trajecto-ries of African and European populations.African hominids would have repeatedlyundergone periods of population contractionduring arid phases—bottlenecks whichwould have combined the effects of rapidchange through genetic drift and of selectionfor energetically more efficient bodies andmore efficient technologies as resources be-came scarce. These changes, which wouldrepresent either an increase in diversitywithin a period if several fragmented popu-lations survived or a loss of diversity ifextinction of most groups took place, wouldbe frozen and magnified by the subsequentpopulation expansion during the earlyphases of interglacials. It would be thesediverse populations that reached the Medi-terranean, taking with them the biologicaland behavioral innovations acquired in thepreceding tens of thousands of years. WithinEurope, the processes would have been dif-ferent. Once allopatric conditions in relationto African hominids were established at theonset of glacial climates, European hominidswould be under the pressure of directionalselection leading towards morphological spe-cializations that improved survivorship inperiglacial habitats. Directional selection re-duces diversity in that it attempts to movethe population close to a new adaptive peakand therefore a level of homogenization re-flected morphologically in the fixation ofapomorphic traits.

Evolution within the modern human lin-eage can also be expressed in terms ofchanging levels of diversity. The stringencyof the period preceding the ancestral bottle-neck has to be measured by the effect it hadon population survivorship. By implication,we may infer that the selective pressure forenergetic economy and efficiency acting onthese African populations was very strong,as must have been the effects of drift aspopulation numbers fell. Therefore, the popu-lation ancestral to all humans became both

different and, for a short period of time,homogeneous. Why is it difficult to establishthresholds between successive hominidgroups in Africa? One possible answer tothis question is that morphological changein Middle Pleistocene Africa was stronglyinfluenced by periods of significant geneticdrift altering the combination of preexistingtraits, while the selective pressure directedtoward survivorship under scarce resourceswould have favored the evolution of behav-ioral and cognitive novelties not reflectedmorphologically.

However, the ancestral modern popula-tion was not homogeneous for long, as popu-lation expansion, subdivision, and contrac-tion subsequently took place. Depending onthe balance of ancestral polymorphismsthroughout the range of the ancestral popu-lation prior to subdivision, the pattern ofsynapomorphism among subdivided groupsmay have been very different. In the case ofmodern human differentiation, early frag-mentation of the ancestral population led tothe establishment of at least three groupsthat, during a long period of populationisolation and relatively small size, changedboth the level and pattern of ancestral vari-ability in different ways. It is thus thatgroups like the Australians seem to haveretained a larger proportion of ancestraltraits than others and that Europeans andAsians show directional changes towardsnew morphotypes, while Pleistocene Afri-cans show the effects of large interpopula-tion differences. This is hardly surprising;although gene flow has played a significantpart in homogenizing the human populationover the last ten thousand years, for most ofour species history it has been survival inparticular environments as relatively smallpopulations that would have been the princi-pal selective pressure. The evolution of thehuman species may thus be universal, but itis made up of a myriad of local histories.

Extinction

In the course of the debate on modernhuman origins, there has been considerableemphasis on the idea of competing speciesand the subsequent extinction of some ofthese. The framework adopted here has


placed the emphasis on populations ratherthan species, as these are the units in whichdifferentiation and novelty will occur. Wehave been able to track the history of thespecies in terms of populations that haveexpanded and contracted, and the geneticstructure and the palaeontological recordare the product of these multiple events.What has emerged is a picture of smallhominid populations becoming extinct andthe subsequent history of the species as theresult of only one or a small number ofpopulations surviving and expanding. Thisimplies that population-level extinctions mayhave been an important part of our evolution-ary history. This is not just a question ofdifferent species and of archaics vs. modernsbut of both modern and nonmodern popula-tions, both African and non-African. Themodels discussed here have imputed thatpre-Neanderthal European populations, ar-chaic and modern African groups, and earlymodern humans (Skhul/Qafzeh, southernAfrican) as well as the Neanderthals them-selves all became extinct. These are likely tobe just a sample. Our evolutionary history,even in the last 100,000 years, is likely tohave been structured as much by extinctionas by innovation.

This has implications for considering diver-sity. First, the diversity of modern humanstoday is likely to be just a subset of Homosapiens diversity that could have beensampled across the last 100,000 years. Sec-ond, patterns of diversity, particularly therelationship between inter- and intrapopula-tion diversity, are likely to have varied con-siderably over time. Third, the fact thatpopulations may have become extinct, eitherliterally or as distinct units identifiable cul-turally or genetically, suggests that we needto know more about the dynamics of popula-tion interactions over the long term and inparticular how boundaries are formed, main-tained, and lost.

Microevolutionary events

We have argued that human evolution,like the evolution of other animal lineages,has been largely governed by microevolution-ary mechanisms and therefore that demo-graphically- based patterns should be sought.However, the demography of populations in

time and space forms the basis for changesthat lead to speciation. Defining palaeonto-logical species is dependent upon the con-cept of species used and the interpretation ofthe significance of the differences betweenpopulations observed. Under the constraintof being unable to test reproductive isolationbetween fossil populations, many palaeon-tologists use the evolutionary species con-cept developed by Simpson (1950), in whicha species is a population with an indepen-dent evolutionary trajectory. On the basis ofthis, several authors raise the differencesbetween lower and Middle Pleistocene ar-chaic hominids and between Neanderthalsand modern humans to specific level, result-ing in four Pleistocene species of Homo —H.erectus, H. heidelbergensis, H. neandertha-lensis, and H. sapiens. We have introduced apopulation intermediate between Africanand European H. heidelbergensis and theNeanderthal and modern populations of theearly Upper Pleistocene, for which we haveresurrected the name H. helmei (Foley andLahr, 1997). This population would havedifferentiated in Africa during a glacial-aridepisode between 300 and 250 Ka, primarilyreflected in the evolution of behavioral traits.

Whether H. helmei represents a biologicalspecies (sensu Mayr, 1963) or not is not thecenter of the argument. In reality, whetherany of these larger-brained late Pleistocenehominids represented a biological speciesthat could not interbreed with others isquestionable. The key point is what biologi-cal and behavioral heritage the individualswithin each of these groups shared thatallowed them to undergo assortative matingand to compete as social units with otherhominid groups for space and resources.

Role of geography in recent humanevolutionary history

Darwin’s greatest difficulty was to con-vince his readers that the effect of small-scale mechanisms could explain the incred-ible magnitude of evolutionary change. Thisremains the most challenging aspect of evo-lutionary studies, and accordingly large-scale contingent and punctuated events arecommonly proposed instead. Catastrophicexplanations can account for drastic change,and, given their sudden nature, their effects


are rarely represented in geological scale.Recently, Ambrose (1998) has proposed thatthe secondary bottlenecks in the popula-tions ancestral toAfricans,Asians, and Euro-peans were related to the effects of thevolcanic winter resulting from the eruptionof the Toba volcano 70 Ka. The Toba Volcanodid erupt 70 Ka, and, as argued by Rampinoand Self (1993), it may have been the largestvolcanic eruption in the last 100,000 years.Nevertheless, however attractive such acatastrophic explanation, we cannot confirmit or refute it at present. We would arguethat alternative explanations, relying on theprocesses that generate change in evolution-ary time—natural selection, genetic drift,mutations, and gene flow—can account forthe evolution of human populations. Thediscussions above have attempted to showhow strong geographic and demographicmechanisms can be in explaining evolution-ary patterns, even when the outcome ofthese is as extraordinary as human diver-sity.

Finally, we have argued that the model ofa recent African origin of modern humans isempirically strong and have tried to showhow, when treated as the complex evolutionof populations in time and space, it is consis-tent with current thinking on evolutionarytheory. Such theory emphasizes small-scaledemographic processes and allopatry as theappropriate scale and dispersals and contrac-tions as the primary demographic mecha-nisms underlying both differentiation anddiversity. We have referred to the combina-tion of a microevolutionary perspective andthe spatial considerations as evolutionarygeography and have found it a useful meansfor integrating genetic and palaeoanthropo-logical data and for bringing together biologi-cal processes and historical context. Much ofthe debate about modern human origins hasfoundered on the lack of integration of differ-ent approaches. We would hope that agreater emphasis on the broader theoreticalunderpinnings, and in particular popula-tions rather than species and microevolu-tion rather than macroevolution, of a singleorigin and multiple dispersals model willopen the way for new questions to be ad-dressed.

ACKNOWLEDGMENTS

We thank E. Harris, R. Klein, C. Ruff, M.Stoneking, and anonymous reviewers fortheir helpful comments on earlier drafts.Thanks also to A. Rogers for the informationregarding computer simulations on the evo-lution of diversity and to N. Shackleton forthe original isotope data. M.M.L.’s researchis supported by FAPESP, Brazil. R.A.F. andM.M.L. have received financial support fromthe King’s College Research Centre, Cam-bridge.

LITERATURE CITED

Allsworth-Jones P (1993) The archaeology of archaicand early modern Homo sapiens: an African perspec-tive. Cambridge Archaeological Journal 3:21–39.

Ambrose S (1998) Late Pleistocene human populationbottlenecks, volcanic winter, and differentiation ofmodern humans. J. Hum. Evol. 34:623–651.

Armour JAL, Anttinen T, May CA, Vega EE, Sajantila A,Kidd JR, Kidd KK, Bertranpetit J, Paabo S, andJeffreys AJ (1996) Minisatellite diversity supports arecent African origin for modern humans. NatureGenetics 13:154–160.

Arsuaga J-L, Martinez I, Gracia A, Carretero J-M, andCarbonell E (1993) Three new human skulls from theSima de los Huesos Middle Pleistocene site in Sierrade Atapuerca, Spain. Nature 362:534–537.

Ascenzi A, Biddittu I, Cassoli PF, Segre AG, and Segren-aldini E (1996) Calvarium of late Homo erectus fromCeprano, Italy. J. Hum. Evol. 31:409–423.

Avise JC (1994) Molecular Markers, Natural Historyand Evolution. New York: Chapman & Hall.

Avise JC, and Wollenberg K (1997) Phylogenetics andthe origin of species. Proc. Natl. Acad. Sci. U. S. A.94:7748–7755.

Bar-Yosef O (1992a) Middle Palaeolithic chronology andthe transition to the Upper Palaeolithic in southwestAsia. In G Brauer and FH Smith (eds.): Continuity orreplacement? Controversies in Homo sapiens evolu-tion. Rotterdam: Balkema, pp. 261–272.

Bar-Yosef O (1992b) Middle Paleolithic human adapta-tions in the Mediterranean Levant. In T Akazawa, KAoki, and T Kimura (eds.): The Evolution and Dis-persal of Modern Humans in Asia. Tokyo: Hokusen-sha, pp. 189–215.

Bar-Yosef O (1993) The role of western Asia in modernhuman origins. In MJ Aitken, CB Stringer, and PAMellars (eds.): The origins of modern humans and theimpact of chronometric dating. Princeton: PrincetonUniversity Press, pp. 132–147.

Barton JC, and Stringer CB (1997) An attempt at datingthe Swanscombe skull bones using non-destructivegamma-ray counting. Archaeometry 39:205–216.

Bar-Yosef O (1994) The Lower Palaeolithic of the NearEast. Journal of World Prehistory 8:211–265.

Bate DMA (1943) Pleistocene Cricetinae from Palestine.Annals and Magazine of Natural History 11:823–838.

Bermudez de Castro JM, Arsuaga J-L, Carbonell E,Rosas A, Martınez I, and Mosquera M (1997) Ahominid from the Lower Pleistocene of Atapuerca,Spain: Possible ancestor of Neandertals and modernhumans. Science 276:1392–1395.

Blackwell B, and Schwartz H (1986) U-series analyses ofthe lower travertine at Ehringsdorf, DDR. Quater-nary Research 25:215–222.


Bowcock AM, Kidd JR, Mountain JL, Hebert JM, Carot-enuto L, Kidd KK, and Cavalli-Sforza LL (1991) Drift,admixture, and selection in human evolution: A studywith DNA polymorphisms. Proc. Natl. Acad. Sci. U. S.A. 8:839–843.

Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E,Kidd JR, and Cavalli-Sforza LL (1994) High resolu-tion of human evolutionary trees with polymorphicmicrosatellites. Nature 368:455–457.

Bowler PJ (1986) Theories of Human Evolution: ACentury of Debate, 1844–1944. Oxford: Blackwells.

Brace CL (1964) The fate of the ‘classic’ Neanderthals: Acase of hominid catstrophism. Current Anthropology5:3–43.

Bradley RS (1985) Quaternary Paleoclimatology: Meth-ods of Paleoclimatic Reconstruction. Boston: Allen &Unwin.

Brauer G (1989) The evolution of modern humans: Acomparison of the African and non-African evidence.In P Mellars and CB Stringer (eds.): The HumanRevolution: Behavioral and Biological Perspectives onthe Origins of Modern Humans. Edinburgh: Edin-burgh University Press, pp. 123–154.

Brauer G (1992) Africa’s place in the evolution of Homosapiens. In G Brauer and FH Smith (eds.): Continuityor replacement? Controversies in Homo sapiens Evolu-tion. Rotterdam: Balkema, pp. 83–98.

Brooks AS, Helgren DM, Cramer JS, Franklin A,Hornyak W, Keating JM, Klein RG, Rink WJ, SchwarczHP, Smith JNL, Stewart K, Todd NE, Verniers J, andYellen JE (1995) Dating and context of three MiddleStone Age sites with bone points in the Upper SemlikiValley, Zaire. Science 268:548–553.

Brown WM (1980) Polymorphism in mitochondrial DNAof humans as revealed by restriction endonucleaseanalysis. Proc. Natl. Acad. Sci. U. S. A. 77:3605–3609.

Brown P (1987) Pleistocene homogeneity and Holocenesize reduction: The Australian human skeletal evi-dence. Archaeology and Physical Anthropology inOceania 22:127–143.

Cann RL, Stoneking M, and Wilson AC (1987) Mitochon-drial DNA and human evolution. Nature 325:31–35.

Churchill SE, Pearson OM, Grine FE, Trinkaus E, andHolliday TW (1996) Morphological affinities of theproximal ulna from Klasies River main site: Archaicor modern? J. Hum. Evol. 31:231–237.

Clark GA, and Willermet CM (eds.) (1995) ConceptualIssues in Modern Human Origins Research. NewYork: Aldine de Gruyter.

Clark JD (1992) African and Asian perspectives on theorigins of modern humans. Philos. Trans. R. Soc.Lond. [Biol.] 337:148–178.

Clark JD (1993) The Aterian of the Central Sahara. In LKrzyzaniak, M Kobusiewicz, and J Alexander (eds.):Environmental Change and Human Culture in theNile Basin and Northern Africa Until the SecondMillennium B.C. Poznan: Museum Archeologiczne WPoznaniu, pp. 49–68.

Clark JD, de Heinzelin J, Schick KD, Hart WK, WhiteTD, WoldeGabriel G, Walter RC, Suwa G, Asfaw B,Vrba E, and H.-Selassie Y (1994) African Homo erec-tus: Old radiometric ages and young Oldowan assem-blages in the Middle Awash valley, Ethiopia. Science264:1907–1910.

Clark JGD (1968) World Prehistory: A New Outline.Cambridge: Cambridge University Press.

Coon C (1962) The Origin of Races. New York: A.A.Knopf.

Day MH, and Stringer CB (1991) Les restes craniensd’Omo-Kibish et leur classification a l’interieur dugenre Homo. L’Anthropologie 95:573–594.

Deacon HJ (1989) Late Pleistocene palaeoecology andarchaeology in the southern Cape, South Africa. In P

Mellars and CB Stringer (eds.): The Human Revolu-tion. Edinburgh: Edinburgh University Press, pp.547–564.

Dean D, Hublin JJ, Ziegler R, and Holloway R (1994)The Middle Pleistocene preneandertal partial skullfrom Reilingen (Germany). Am. J. Phys. Anthropol.18(Suppl.):77.

Denys C (1985) Palaeoenvironmental and palaeobiogeo-graphical significance of the fossil rodent assemblagesof Laetoli (Pliocene, Tanzania). Pal., Pal., Pal. 52:77–97.

Di Rienzo A, and Wilson AC (1991) Branching pattern inthe evolutionary tree for human mitochondrial DNA.Proc. Natl. Acad. Sci. U. S. A. 88:1597–1601.

Ferris S, Brown W, Davidson W (1981) Extensive poly-morphism in the mitochondrial DNA of apes. Proc.Natl. Acad. Sci. U. S. A. 78:6319–6323.

Fisher RA (1930) The Genetical Theory of NaturalSelection. Oxford: Oxford University Press.

Foley RA (1991) How many species of hominid shouldthere be? J. Hum. Evol. 20:413–427.

Foley RA (1994) Speciation, extinction and climaticchange in hominid evolution. J. Hum. Evol. 26:275–289.

Foley RA (in press) Pattern and process in hominidevolution. In J Bintliff (ed.): Structure and Contin-gency in the Evolution of Life and Human History.Cassells.

Foley RA, and Lahr MM (1997) Mode 3 technologies andthe evolution of modern humans. Cambridge Archaeo-logical Journal 7:3–36.

Gamble CS (1993) Timewalkers: The Prehistory of Glo-bal Colonization. Cambridge: Harvard UniversityPress.

Geraads D, and Tchernov E (1987) Femurs humains duPleistocene Moyen de Gesher Benot Ya’akov (Israel).L’Anthropologie 87:138–141.

Goren-Inbar N (1985) The lithic assemblage of theBerekhat Ram Acheulian site, Golan Heights. Paleori-ent 11:7–28.

Green HS (ed.) (1984) Pontnewydd Cave: A LowerPalaeolithic Hominid Site in Wales: The First Report.Cardiff: National Museum Wales.

Grine FE, and Klein RG (1993) Late Pleistocene humanremains from the Sea Harvest Site, Saldanha Bay,South Africa. S. Afr. J. Sci. 89:145–152.

Grine FE, Klein RG, and Volamn TP (1991) Dating,archaeology and human fossils from the Middle StoneAge levels of Die Kelders, South Africa. J. Hum. Evol.21:363–395.

Groves CP (1989) A regional approach to the problem ofthe origin of modern humans in Australasia. In PMellars and CB Stringer (eds.): The Human Revolu-tion. Princeton: Princeton University Press, pp. 274–285.

Groves CP (1994) The origin of modern humans. Inter-disc. Sci. Rev. 19:23–34.

Groves CP, and Lahr MM (1994) A bush not a ladder:Speciation and replacement in human evolution. Per-spectives in Human Biology 4:1–11.

Grun R, and Stringer CB (1991) Electron spin resonancedating and the evolution of modern humans. Archae-ometry 33:153–199.

Grun R, Brink JS, Spooner NA, Taylor L, Stringer CB,Franciscus RG, and Murray AS (1996) Direct dating ofFlorisbad hominid. Nature 382:500–501.

Haigh J, and Maynard Smith J (1972) Population sizeand protein variation in man. Genet. Res. 19:73–89.

Hamilton AC (1976) The significance of patterns ofdistribution shown by forest plants and animals intropical Africa for the reconstruction of Upper Pleis-tocene environments: A review. Palaeoecol. Afr. 9:63–97.


Hammer MF (1995) A recent common ancestry forhuman Y chromosomes. Nature 378:376–378.

Hammer MF, Karafet T, Rasanayagam A, Wood ET,Altheide TK, Griffiths RC, Templeton AR, Jenkins T,and Zegura SL (1997) The evolutionary history of Ychromosome haplotypes in human populations. In:Abstracts of Papers Presented at the Cold SpringHarbor Laboratory, New York, October 1997. p. 52.

Harding RM, Fullerton SM, Griffiths RC, Bond J, CoxMJ, Schneider JA, Moulin DS, and Clegg JB (1997)Archaic African and Asian lineages in the geneticancestry of modern humans. Am. J. Hum. Genet.60:772–789.

Harpending HC, Sherry ST, Rogers AR, and StonekingM (1993) The genetic structure of ancient humanpopulations. Current Anthropology 34:483–496.

Harpending HC, Relethford J, and Sherry ST (1996)Methods and models for understanding human diver-sity. In AJ Boyce and CGN Mascie-Taylor (eds.):Molecular Biology and Human Diversity. Cambridge:Cambridge University Press, pp. 283–299.

Hasegawa M, and Horai S (1991) Time of the deepestroot for polymorphism in human mitochondrial DNA.J. Mol. Evo. 32:37–42.

Hasegawa M, di Rienzo A, and Wilson AC (1993) Towarda more accurate timescale for the human mitochon-drial DNA tree. J. Mol. Evol. 37:347–354.

Heintz E, and Brunet M (1982) Role de la chıne alpineasiatique dans la distribution spatio-temporelle desCervides. C. R. Acad. Sci. II 294:1391–1394.

Holliday TW (1997) Body proportions in late PleistoceneEurope and modern human origins. J. Hum. Evol.32:423–447.

Hooghiemstra H, and Agwu COC (1988) Changes in thevegetation and trade winds in equatorial northwestAfrica 140,000–70,000 yr b.P. as deduced from twomarine pollen records. Pal., Pal., Pal. 66:627–664.

Hooijer DA (1959) Fossil mammals from Jisr BanatYaqub, south lake Huleh, Israel. Bulletin of the Re-search Council of Israel G8:177–179.

Hooijer DA (1960) A Stegodon from Israel. Bulletin of theResearch Council of Israel G9:104–107.

Horai S, and Hayasaka K (1990) Intraspecific nucleotidesequence differences in the major noncoding region ofhuman mitochondrial DNA. Am. J. Hum. Genet.46:28–42.

Horai S, Kondo R, Nakagawa-Hattori Y, Hayashi S,Sonoda S, and Tajima K (1993) Peopling of the Ameri-cas, founded by four major lineages of mitochondrialDNA. Mol. Biol. Evol. 10:23–47.

Horai S, Hayasaka K, Kondo R, Tsugane K, and Taka-hata N (1995) Recent African origin of modern hu-mans revealed by complete sequences of hominoidmitochondrial DNAs. Proc. Natl. Acad. Sci. U. S. A.92:532–536.

Howells WW (1973) Cranial Variation in Man. Cam-bridge: Harvard University Press.

Howells WW (1976) Explaining modern man: Evolution-ists versus migrationists. J. Hum. Evol. 5:477–495.

Howells WW (1989) Skull Shapes and the Map: Cranio-metric Analyses in the Dispersion of Modern Homo.Papers of the Peabody Museum of Archaeology andEthnology 79. Cambridge: Harvard University Press.

Hublin J-J (1993) Recent human evolution in northwestAfrica. In MJ Aitken, CB Stringer, and PA Mellars(eds.): The Origin of Modern Humans and the Impactof Chronometric Dating. Princeton: Princeton Univer-sity Press, pp. 118–131.

Hublin J-J (1996) Beyond the Garden of Eden. Nature381:658–659.

Hublin J-J, Barroso Ruiz C, Medina Lara P, FontugneM, and Reyss J-L (1995) The Mousterian site ofZafarraya (Andalusia, Spain)—dating and implica-

tions on the paleolithic peopling processes of WesternEurope. C. R. Acad. Sci. III 36:931–937.

Jaeger MJ-J (1975) The mammalian faunas and homi-nid fossils of the Middle Pleistocene of the Maghreb.In KW Butzer and GLL Isaac (eds.): After the Austra-lopithecines. The Hague: Mouton, pp. 399–418.

Jones JS, and Rouhani S (1986) How small was thebottleneck? Nature 319:449–450.

Kelly RL (1995) The Foraging Spectrum: Diversity inHunter-Gatherer Lifeways. Washington, DC: Smithso-nian Institution Press.

Kidder JH, Jantz RL, and Smith FH (1992) Definingmodern humans:Amultivariate approach. In G Brauerand FH Smith (eds.): Continuity or Replacement?Controversies in Homo sapiens Evolution. Rotterdam:Balkema, pp. 157–177.

Klein RG (1992) The archaeology of modern humanorigins. Evolutionary Anthropology 1:5–14.

Klein RG (1994) Southern Africa before the Iron Age. InRS Corruccini and RL Ciochon (eds.): IntegrativePaths to the Past: Paleoanthropological Advances inHonor of F. Clark Howell. Englewood Cliffs: PrenticeHall, pp. 471–519.

Klein RG (1995) Anatomy, behaviour, and modern hu-man origins. Journal of World Prehistory 9:167–198.

Klein RG (1998) The Human Career, 2nd ed. Chicago:Chicago University Press.

Klein RG, and Cruz-Uribe K (1996) Exploitation of largebovids and seals at Middle and Later Stone Age sitesin South Africa. J. Hum. Evol. 31:315–334.

Kocher T, and Wilson A (1991) Sequence evolution ofmitochondrial DNA in humans and chimpanzees:Control region and a protein-coding region. In SOsawa and T Honjo (eds.): Evolution of Life: Fossils,Molecules, and Culture. New York: Springer-Verlag,pp. 391–413.

Krings M, Stone A, Schmitz RW, Krainitzki H, Stone-king M, and Paabo S (1997) Neanderthal mtDNAsequences. in: Abstracts of Papers Presented at theCold Spring Harbor Laboratory, New York, October1997. p. 41.

Lahr MM (1994) The multiregional model of modernhuman origins: A reassessment of its morphologicalbasis. J. Hum. Evol. 26:23–56.

Lahr MM (1996) The Evolution of Modern HumanDiversity. Cambridge: Cambridge University Press.

Lahr MM, and Foley RA (1994) Multiple dispersals andmodern human origins. Evolutionary Anthropology3:48–60.

Lahr MM, and Wright RVS (1996) The question ofrobusticity and the relationship between cranial sizeand shape. J. Hum. Evol. 31:157–191.

Larsen CS (1997) Bioarchaeology: Interpreting Behav-ior From The Skeleton. Cambridge: Cambridge Univer-sity Press.

Leveque F, and Vandermeersch B (1981) Le neander-talien de Saint-Cesaire. Recherche 12:242–244.

Leveque F, Backer AM, and Guilbaud M (eds.) (1993)Context of a Late Neandertal: Implications of Multidis-ciplinary Research for the Transition to Upper Paleo-lithic Adaptations at Saint-Cesaire, Charente-Mari-time, France. Madison, WI: Prehistory Press.

Li W-H, and Sadler LA (1991) Low nucleotide diversityin man. Genetics 129:513–523.

Lieberman DE (1996) How and why humans grow thinskulls: Experimental evidence for systemic corticalrobusticity. Am. J. Phys. Anthropol. 101:217–236.

Loubere P (1988) Gradual Late Pliocene onset of glacia-tion: A deep-sea record from the Northeast Atlantic.Pal., Pal., Pal. 63:327–334.

Macintosh NWG, and Larnach SL (1976) Aboriginalaffinities looked at in world context. In RL Kirk andAG Thorne (eds.): The Origin of Australians. Can-


berra: Australian Institute of Aboriginal Studies, pp.113–126.

Maddison DR, Ruvolo M, and Swofford DL (1992) Geo-graphic origins of human mitochondrial DNA: Phylo-genetic evidence from control region sequences. Syst.Biol. 41:111–124.

Malatesta A, and Zarlenga F (1988) Evidence of MiddlePleistocene marine transgressions along the Mediter-ranean coast. Pal., Pal., Pal. 68:311–315.

Manderscheid EJ, and Rogers AR (1996) Genetic admix-ture in the Late Pleistocene. Am. J. Phys. Anthropol.100:1–5.

Maynard Smith J (1989) Evolutionary Genetics. Cam-bridge: Cambridge University Press.

Maynard Smith J (1990) The Y of human relationships.Nature 344:591–592.

Mayr E (1963) Animal Species and Evolution. Cam-bridge: Harvard University Press.

McBrearty S, Bishop L, and Kingston J (1996) Variabil-ity in traces of Middle Pleistocene hominid behaviourin the Kapthurin Formation, Baringo, Kenya. J. Hum.Evol. 30:563–580.

McBurney CBM (1960) The Stone Age of NorthernAfrica. London: William Clowes & Sons Ltd.

McBurney CBM (1967) Haua Fteah and the Stone Age ofthe Southeast Mediterranean. Cambridge: Cam-bridge University Press.

Mellars P (1996) The Neanderthal Legacy: An Archaeo-logical Perspective from Western Europe. Princeton:Princeton University Press.

Morin PA, Wallis J, Moore J, Chakraborty R, andWoodruff D (1993) Noninvasive sampling and DNAamplification for paternity exclusion, community struc-ture, and phylogeography in wild chimpanzees. Pri-mates 34:347–356.

Morris AG (1992) Biological relationships between Up-per Pleistocene and Holocene populations in southernAfrica. In G Brauer and FH Smith (eds.): Continuityor Replacement: Controversies in Homo sapiens Evo-lution. Rotterdam: Balkema, pp. 131–143.

Nei M, and Graur D (1984) Extent of protein polymor-phism and the neutral mutation theory EvolutionaryBiology 17:73–118.

Nei M, and Takezaki N (1996) The root of the phyloge-netic tree of human populations. Mol. Biol. Evol.13:170–177.

Noble W, and Davidson I (1996) Human Evolution,Language and Mind. Cambridge: Cambridge Univer-sity Press.

Paabo S (1995) The Y chromosome and the origin of all ofus (men). Science 268:1141–1185.

Pandya A, Santos RR, Zerjal T, Ferak V, Mitchell RJ,Thangaraj K, Singh L, Harding R, Jobling MA, andTyler-Smith C (1997) Use of Y-chromosomal DNAhaplotypes to investigate human population history.In: Abstracts of Papers Presented at the Cold SpringHarbor Laboratory, New York, October 1997. p. 59.

Payne S, and Garrard A (1983) Camelus from the UpperPleistocene of Mount Carmel, Israel. Journal of Ar-chaeological Science 10:243–247.

Penny D, Steel M, Waddell PJ, and Hendy MD (1995)Improved analyses of human mtDNA sequences sup-port a recent African origin of Homo sapiens. Mol.Biol. Evol. 12:863–882.

Pfeiffer S, and Zehr MK (1996) A morphological andhistological study of the human humerus from BorderCave. J. Hum. Evol. 31:49–59.

Phillipson D (1985) African Archaeology. Cambridge:Cambridge University Press.

Pinker S (1994) The Language Instinct. London: Pen-guin.

Rak Y (1986) The Neanderthal: A new look at an old face.J. Hum. Evol. 15:151–164.

Rak Y (1993) Morphological variation in Homo neander-thalensis and Homo sapiens in the Levant: A biogeo-graphic model. In WH Kimbel and LB Martin (eds.):Species, Species Concepts, and Primate Evolution.New York: Plenum Press, pp. 523–536.

Rampino MR, and Self S (1993) Climate-volcanismfeedback and the Toba eruption of ,74,000 years ago.Quaternary Research 40:269–280.

Rea DK, and Schrader H (1985) Late Pliocene onset ofglaciation: Ice-rafting and diatom stratigraphy ofNorth Pacific DSDP Cores. Pal., Pal., Pal. 49:313–325.

Relethford JH, and Harpending HC (1994) Craniomet-ric variation, genetic theory, and modern humanorigins. Am. J. Phys. Anthropol. 95:249–270.

Rightmire GP (1988) Homo erectus and later MiddlePleistocene humans. Annu. Rev. Anthrop. 17:239–259.

Rightmire GP (1989) Middle stone age humans fromeastern and southern Africa. In P Mellars and CBStringer (eds.): The Human Revolution. Edinburgh:Edinburgh University Press, pp. 109–122.

Rightmire GP (1996) The human cranium from Bodo,Ethiopia: Evidence for speciation in the Middle Pleis-tocene. J. Hum. Evol. 31:21–39.

Rightmire GP, and Deacon HJ (1991) Comparativestudies of late Pleistocene human remains from Kla-sies River Mouth, South Africa. J. Hum. Evol. 20:131–156.

Rink WJ, Schwartz HP, Smith FH, and Radovcic J(1995) ESR ages for Krapina hominids. Nature 378:24.

Ritchie JC, and Haynes CV (1987) Holocene vegetationzonation in the eastern Sahara. Nature 330:645–647.

Roberts N (1984) Pleistocene environments in time andspace. In R Foley (ed.): Hominid Evolution and Com-munity Ecology. London: Academic Press, pp. 25–53.

Roberts RG, Jones R, Spooner NA, Head MJ, MurrayAS, and Smith MA (1994) The human colonisation ofAustralia: Optical dates of 53,000 and 60,000 yearsbracket human arrival at Deaf Adder Gorge, NorthernTerritory. Quaternary Science Reviews 13:575–586.

Rogers A (1995) How much can fossils tell us aboutregional continuity? Current Anthropology 36:674–676.

Rogers AR, and Harpending HC (1992) Populationgrowth makes waves in the distribution of pairwisegenetic differences. Mol. Biol. Evol. 9:552–559.

Rogers AR, and Jorde LB (1995) Genetic evidence onmodern human origins. Hum. Biol. 67:1–36.

Ruff CB (1994) Morphological adaptation to climate inmodern and fossil hominids. Yearbook of PhysicalAnthropology 37:65–107.

Ruff CB, Trinkaus E, Walker A, and Larsen CS (1993)Post-cranial robusticity in Homo 1: Temporal trendsand mechanical interpretation. Am. J. Phys. Anthro-pol. 91:21–53.

Ruff CB, Trinkaus E, and Holliday T (1997) Body massand encephalization in Pleistocene Homo. Nature387:173–176.

Ruvolo M, Zehr S, von Dornum M, Pan D, Chang B, andLin J (1993) Mitochondrial COII sequences and mod-ern human origins. Mol. Biol. Evol. 10:1115–1135.

Sachs HM (1973) Late Pleistocene history of the NorthPacific: Evidence from a quantitative study of radio-laria in core V21–173. Quaternary Research 3:89–98.

Sarntheim M, Stremme HE, and Mangini A (1986) TheHolstein interglaciation: Time-stratigraphic positionand correlation to stable-isotope stratigraphy of deep-sea sediments. Quaternary Research 26:283–298.

Schwarcz HP, Grun R, Vandermeersch B, Bar-Yosef O,Valladas H, Tchernov E (1988) ESR dates for hominidburial site of Qafzeh in Israel. J. Hum. Evo. 17:733–737.


Shackleton NJ (1987) Oxygen isotopes, ice volume andsea level. Quaternary Science Review 6:183–190.

Sherry S, Rogers AR, Harpending HC, Soodyall H,Jenkins T, and Stoneking M (1994) Mismatch distribu-tions of mtDNA reveal recent human population ex-pansions. Hum. Biol. 66:761–775.

Sherry ST, Harpending HC, Batzer MA, and StonekingM (1997) Alu evolution in human populations: Usingthe coalescent to estimate effective population size.Genetics 147:1977–1982.

Simpson GG (1950) Some principles of historical biologybearing on human origins. Cold Spring Harbor Symp.Quant. Biol. 15:55–66.

Singer R, and Wymer J (1982) The Middle Stone Age atKlasies River Mouth in South Africa. Chicago: Univer-sity of Chicago Press.

Smith FH (1994) Samples, species, and speculations inthe study of modern human origins. In MH Niteckiand DV Nitecki (eds.): Origins of Anatomically Mod-ern Humans. New York: Plenum Press, pp. 227–249.

Smith FH and Spencer F (eds.) (1984) The Origins ofModern Humans: A World Survey of the Fossil Evi-dence. New York: Alan R. Liss.

Stoneking M (1993) DNA and recent human evolution.Evolutionary Anthropology 2:60–73.

Stoneking M (1997) Alu insertion polymorphisms inhuman populations. In: Abstracts of Papers Presentedat the Cold Spring Harbor Laboratory, New York,October 1997. p. 7.

Stoneking M, Fontius JJ, Clifford SL, Soodyall H, ArcotSS, Saha N, Jenkins T, Tahir MA, Deininger PL, andBatzer MA (1997) Alu insertion polymorphisms andhuman evolution: Evidence for a larger populationsize in Africa. Genome Research 7:1061–1071.

Strauss LG (1993–1994) Upper Paleolithic origins andradiocarbon calibration: More new evidence fromSpain. Evolutionary Anthropology 2:195–198.

Street FA, and Grove AT (1979) Global maps of lake-level fluctuations since 30,000 B.P. Quaternary Re-search 12:83–118.

Stringer CB (1989) The origin of modern humans: Acomparison of the European and non-European evi-dence. In P Mellars and CB Stringer (eds.): TheHuman Revolution. Edinburgh: Edinburgh Univer-sity Press, pp. 232–244.

Stringer CB (1992) Replacement, continuity and theorigin of Homo sapiens. In G Brauer and FH Smith(eds.): Continuity or replacement: Controversies inthe evolution of Homo sapiens. Rotterdam: Balkema,pp. 9–24.

Stringer CB (1993) New views on modern human ori-gins. In DT Rasmussen (ed.): The Origin and Evolu-tion of Humans and Humanness. Boston: Jones &Bartlett, pp. 75–94.

Stringer CB (1995) The evolution and distribution oflater Pleistocene human populations. In ES Vrba andGH Denton (eds.): Paleoclimate and Evolution: WithEmphasis on Human Origins. New Haven: Yale Uni-versity Press, pp. 524–531.

Stringer CB (1996a) The Boxgrove tibia: Britain’s oldesthominid and its place in the Middle Pleistocenerecord. In C Gamble and AJ Lawson (eds.): TheEnglish Palaeolithic Reviewed. Trust for Wessex Ar-chaeology Ltd, pp. 52–56.

Stringer CB (1996b) Current issues in modern humanorigins. In WE Meikle, FC Howell, and NG Jablonski(eds.): Contemporary Issues in Human Evolution.California Academy of Science, pp. 115–134.

Stringer CB, and Andrews P (1988) Genetic and fossilevidence for the origin of modern humans. Science239:1263–1268.

Stringer CB, and Gamble C (1993) In Search of theNeanderthals. London: Thames & Hudson.

Stringer CB, Hublin JJ, and Vandermeersch B (1984)The origin of anatomically modern humans in West-ern Europe. In FH Smith and F Spencer (eds.): TheOrigin of Modern Humans: A World Survey of theFossil Evidence. New York: Alan R. Liss, pp. 51–135.

Stringer CB, Grun R, Schwarcz HP, and Goldberg P(1989) ESR dates for the hominid burial site of Skhulin Israel. Nature 338:756–758.

Stringer CB, Humphrey LT, and Compton T (1997)Cladistic analysis of dental traits in recent humansusing a fossil outgroup. J. Hum. Evol. 32:389–402.

Takahata N (1993) Allelic genealogy and human evolu-tion. Mol. Biol. Evol. 10:2–22.

Takahata N, Satta Y, and Klein J (1995) Divergencetime and population size in the lineage leading tomodern humans. Theor. Popul. Biol. 48:198–221.

Tamura K, and Nei M (1993) Estimation of the numberof nucleotide substitutions in the control region ofmitochondrial DNA in humans and chimpanzees. Mol.Biol. Evol. 10:512–526.

Tchernov E (1992a) The Afro-Arabian component in theLevantine mammalian fauna—a short biogeographi-cal review. Israel Journal of Zoology 38:155–192.

Tchernov E (1992b) Biochronology, paleoecology anddispersal events of hominids in the southern Levant.In T Akazawa, K Aoki, and T Kimura (eds.): TheEvolution and Dispersal of Modern Humans in Asia.Tokyo: Hokusen-sha, pp. 149–188.

Tchernov E (1992c) Eurasian-African biotic exchangesthrough the Levantine corridor during the Neogeneand Quaternary. Courier Forsch.-Inst. Senckenberg153:103–123.

Tchernov E (1994) New comments on the biostratigra-phy of the Middle and Upper Pleistocene of theLevant. In O Bar-Yosef and RS Kra (eds.): LateQuaternary chronology and paleoclimates of the East-ern Mediterranean. Tucson: Radiocarbon, pp. 333–350.

Templeton AR (1993) The ‘‘Eve Hypothesis’’: A geneticcritique and reanalysis. American Anthropologist 95:51–72.

Templeton AR (1997) Testing the out of Africa replace-ment hypothesis with mitochondrial DNA data. In GAClark and CM Willermet (eds.): Conceptual Issues inModern Human Origins Research. New York: Aldinede Gruyter, pp. 329–360.

Tishkoff SA, Dietzsch E, Speed W, Pakstis AJ, Kidd JR,Cheung K, Bonne-Tamir B, Santachiara-BenerecettiAS, Moral P, Krings M, Paabo S, Watson E, Risch N,Jenkins T, and Kidd KK (1996) Global patterns oflinkage disequilibrium at the CD4 locus and modernhuman origins. Science 271:1380–1387.

Tishkoff SA, Clark AG, Dietzsch E, Goldman A, SoodyallH, Kidd JR, Jenkins T, and Kidd KK (1997) Demo-graphic history of modern humans inferred fromnuclear genetic haplotype data. In: Abstracts of Pa-pers Presented at the Cold Spring Harbor Laboratory,New York, October 1997. p. 6.

Trinkaus E (1987) The Neandertal face: Evolutionaryand functional perspectives on a recent hominid face.J. Hum. Evol. 16:429–443.

Trinkaus E, and Howells WW (1979) The Neanderthals.Sci. Am. 241:118–133.

Turbon D, Perez-Perez A, and Stringer CB (1997) Amultivariate analysis of Pleistocene hominids: testinghypotheses of European origins. J. Hum. Evo. 32:149–168.

Turner A (1984) Hominids and fellow travellers: Humanmigration into high latitudes as part of a large mam-mal community. In RA Foley (ed.): Hominid Evolutionand Community Ecology. London: Academic Press, pp.193–217.


Valladas H, Joron JL, Valladas G, Arensburg B, Bar-Yosef O, Belfer-Cohen A, Goldberg P, Laville H, Mei-gnen L, Rak Y, Tchernov E, Tillier A-M, and Vander-meersch B (1987) Thermoluminescence dates for theNeanderthal burial site at Kebara in Israel. Nature330:159–160.

Valladas H, Reyss JL, Joron JL, Valladas G, Bar-YosefO, and Vandermeersch B (1988) Thermoluminescencedating of Mousterian ‘‘proto Cro-Magnon’’ remainsfrom Israel and the origin of modern man. Nature331:614–616.

Vandermeersch B (1982) The first Homo sapiens sapiensin the Near East. In A Ronen (ed.): The Transitionfrom the Lower to the Middle Palaeolithic and theOrigin of Modern Man. International Series 151.Oxford: BAR, pp. 297–300.

van Vark GN, and Bilsborough A (1991) Shaking thefamily tree. Science 253:834.

van Vark GN, Bilsborough A, and Henke W (1992)Affinities of European Upper Palaeolithic Homo sapi-ens and later human evolution. J. Hum. Evol. 23:401–417.

Vigilant L, Stoneking M, Harpending HC, Hawkes K,and Wilson AC (1991) African populations and theevolution of human mitochondrial DNA. Science 253:1503–1507.

Vignard AE (1923) Une nouvelle industrie lithique, leSebilian. Bul. Inst. Fr. Arch/ Orient. 22. Paris: InstitutFrancaise d’Archaeologie Orientale.

Waddle DM (1994) Matrix correlation tests support asingle origin for modern humans. Nature 368:452–454.

Wallace DC, Brown MD, Schurr TG, Chen Y-S, Lell JT,Sukernik RI, Strakvskaya YB, and Olckers A (1997)Mitochondrial DNA (mtDNA) and Y chromosomevariation in human evolution and disease. In: Ab-stracts of Papers Presented at the Cold Spring HarborLaboratory, New York, October 1997. p. 42.

Watson E, Forster P, Richards M, and Bandelt H-J(1997) Mitochondrial footprints of human expansionsin Africa. Am. J. Hum. Genet. 61:691–704.

Weidenreich F (1943) The Skull of Sinanthropus pekin-ensis: A Comparative Study of a Primitive HominidSkull. Palaeontologia Sinica, 10. Beijing: GeologicalSurvey of China.

Wendorf F, and Schilde R (1974) A Middle Stone AgeSequence From the Central Rift Valley, Ethiopia.Warsaw: Polska Akademia Nauk Instytut HistoriiKultury Materialnej.

Wendorf F, Close AE, Schild R, Gautier A, Schwarcz HP,Miller GH, Kowalski K, Krolik H, Bluszcz A, RobinsD, and Grun R (1990) Le dernier interglaciaire dans leSahara oriental. L’Anthropologie 94:361–391.

Wendorf F, Close A, Schild R, Gautier A, Schwarcz HP,Miller GH, Kowalski K, Krolik H, Bluszcz A, RobinsonD, Grun R, and McKinney C (1991) Chronology andstratigraphy of the Middle Palaeolithic at Bir Tarfawi,Egypt. In JD Clark (ed.): Cultural Beginnings: Ap-proaches at Understanding Early Hominid Life-Waysin the East African Savanna Mosaic. Bonn: RudolfHabelt, pp. 197–208.

Wendorf F, Schild R, and Close AE (1993) MiddlePalaeolithic occupations at Bir Tarfawi and Bir Sa-hara East, Western Desert of Egypt. In L Krzyzaniak,M Kobusiewicz and J Alexander (eds.): Environmen-tal Change and Human Culture in the Nile Basin andNorthern Africa Until the Second Millennium B.C.Poznan: Museum Archeologiczne W Poznaniu, pp.103–112.

Wills C (1990) Population size bottleneck. Nature 348:398.

Wilson AC, Cann RL, and Carr SM (1985) MitochondrialDNA and two perspectives on evolutionary genetics.Biol. J. Linnean Soc. 26:375–400.

Wolpoff MH (1986) Describing anatomically modernHomo sapiens: A distribution without a definabledifference. Anthropos (Brno) 23:41–53.

Wolpoff MH (1989) Multiregional evolution: The fossilalternative to Eden. In P Mellars and CB Stringer(eds.): The Human Revolution. Edinburgh: EdinburghUniversity Press, pp. 62–108.

Wolpoff MH, and Caspari R (1997) Race and HumanEvolution. New York: Simon & Schuster.

Wolpoff MH, Wu XZ, and Thorne AG (1984) ModernHomo sapiens origins: A general theory of hominidevolution involving the fossil evidence from East Asia.In FH Smith and F Spencer (eds.): The Origin ofModern Humans: A World Survey of the Fossil Evi-dence. New York: Alan R. Liss, pp. 411–483.

Wolpoff MH, Thorne AG, Jelınek J, and Zhang Y (1994)The case for sinking Homo erectus: 100 years ofPithecanthropus is enough! Cour. Forschungsinst.Senckenb. 171:783–790.

Wright S (1931) Evolution in Mendelian populations.Genetics 16:97–159.

Yellen JE, Brooks AS, Cornelissen E, Mehlman MJ, andStewart K (1995) A Middle Stone Age worked boneindustry from Katanda, Upper Semliki Valley, Zaire.Science 268:553–556.

Zimmerman HB, Shackleton NJ, Backman J, BaldaufJG, Kaltenbach AJ, and Morton AC (1984) History ofPlio-Pleistocene climate in the northeastern Atlantic,Deep Sea Drilling Project Hole 552A. Initial Reportsof the Deep Sea Drilling Project 81:861–875.


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Towards a theory of modern human origins: Geography, demography, and diversity in recent human evolution