Tracing ModernHuman Origins

THE 13 MAY ISSUE CONTAINED THREE PAPERS(“Single, rapid coastal settlement of Asiarevealed by analysis of complete mito-chondrial genomes,” V. Macaulay et al.,Reports, p. 1034; “Reconstructing the ori-gin of Andaman Islanders,” K. Thangaraj et

al., Brevia, p. 996; “Did early humans gonorth or south?”, P. Forster and S.Matsumura, Perspectives, p. 965) thatimply that a modern human migration outof Africa with replacement of all non-African archaic humans is an establishedfact that needs no further argument, andthat all that remains now is to ascertain thetime(s) and route(s) of the purportedmigration(s). This presents a profoundlymisleading picture about the present stateof debate on modern human origins.

Mitochondrial DNA (mtDNA) studieshave been used to support ideas about mod-ern human origins, but much information isnow known that contradicts the conclusionsof the early mtDNA literature. For example,nuclear loci rarely, if ever, show the low coa-lescence times (~200,000 years) seen inmtDNA, nor do they show strictly Africanroots. Indeed, there is now growing evidenceof strictly non-African polymorphisms thatdate to before the birth of modern humans(1–5). Nuclear loci do not always, or evencommonly, show the strong signals of expan-sions that are so strikingly present in human

mtDNA (6). Why does Macaulay et al.’smtDNA study suggest that a few hundredfemales migrated out of Africa, whereas thenuclear DNA suggests an effective popula-tion of around 10,000 (7)? All these datahave to be explained before a proper estima-tion of the place of mtDNA evidence in theoverall picture can be made.

Exclusive attention to mtDNA data hasled to an extremely one-sided picture ofmodern human origins. No theory that doesnot explain all or, at least, most of the factswill survive. Not until the mtDNA data is

reconciled with nuclear DNA data and thearchaeological and other anthropologicalevidence will we have an enduring solutionto the puzzle of modern human origins.

HENRY HARPENDING1 AND VINAYAK ESWARAN2

1Department of Anthropology, University of Utah,

Stewart Building, Salt Lake City, UT 84112, USA.2Department of Mechanical Engineering, Indian

Institute of Technology, Kanpur 208016, India.

References1. R. M. Harding et al., Am. J. Hum. Genet. 60, 772 (1997).2. Z. Zhao et al., Proc. Natl. Acad. Sci. U.S.A. 97, 11354

(2000).3. N.Yu et al., Mol. Biol. Evol. 18, 214 (2001).4. D. Garrigan et al., Mol. Biol. Evol. 22,189 (2005).5. J. Hardy et al., Biochem. Soc. Trans. 33, 582 (2005).6. H. C . Harpending , S. T. Sherry, A. R. Rogers, M.

Stoneking, Curr. Anthropol. 34, 483 (1993).7. N.Takahata, Mol. Biol. Evol. 10, 2 (1993).

ResponseBOTH MODERN HUMAN MITOCHONDRIALDNA (mtDNA) and the male-specific partof the modern human Y chromosome have arecent origin in Africa and were dispersedthroughout the rest of the world less than100,000 years ago (1, 2). This is not to saythat there was no (limited) interbreeding ofanatomically modern humans with archaichumans, which might be reflected in someautosomal and X-chromosome genes—apossibility that our Report did not address.The current evidence from these loci, how-ever, remains equivocal.

Existing autosomal data do not, in mostcases, provide strong evidence for eitherreplacement or hybridization, despiteclaims to the contrary. The high coales-

cence time of autosomalloci is not relevant, sincein itself this tells usalmost nothing aboutmore recent settlementevents: A small foundergene pool could wellhave either a deep or shal-low ancestry within areplacement perspective.Given the limited amountof variation in non-

recombined stretches of the autosomes,there is typically little power to distinguishdifferent demographic models. This is astrue of the autosomal data used byTempleton (3) as it is of the data in thepapers cited by Harpending and Eswaran.The authors of the most recent of these (4)are entirely open about this, but their(frequency-based) suggestion that the rootof their tree lies in Asia is mistaken; there issimply insufficient branching structure tofix the geographical location of the rootwith any confidence. Moreover, suppos-

edly ancient Asian-specif ic single-nucleotide polymorphisms such as thosecited by Harpending and Eswaran are asso-ciated with age estimates of enormousuncertainty.

Bold conclusions of ancient Asianancestry also suffer from limited sampling.Non-African mtDNAs most likely evolvedin the Horn of Africa and dispersed fromthere, but none of the cited papers on auto-somal loci include data from this region.Even if such data were available, identify-ing non-African founder lineages in suchlow-resolution systems is deeply problem-atic because of recent back-migrationacross the Red Sea (5). In cases where auto-

somal loci do have the necessary resolution,they suggest the replacement model (6–8).The discordant population-size estimatesreferred to by Harpending and Eswaran arelikely more apparent than real, since theselong-term values are usually obtained withthe multiregional stipulation of randommating and constant population size. Theanalysis of overly simplistic models withmethods that throw away what little infor-mation there is in most of these loci throwsup straw men, such as the apparent lack of“strong signals of expansion” in some auto-somal loci (9).

VINCENT MACAULAY,1* CATHERINE HILL,2

ALESSANDRO ACHILLI,3 CHIARA RENGO,3

DOUGLAS CLARKE,4 WILLIAM MEEHAN,4

JAMES BLACKBURN,4 ORNELLA SEMINO,3 ROSARIA

SCOZZARI,5 FULVIO CRUCIANI,5 ADI TAHA,6

NORAZILA KASSIM SHAARI,7 JOSEPH MARIPA RAJA,7

PATIMAH ISMAIL,7 ZAFARINA ZAINUDDIN,8

WILLIAM GOODWIN,9 DAVID BULBECK,10

HANS-JÜRGEN BANDELT,11 STEPHEN OPPENHEIMER,12

ANTONIO TORRONI,3 MARTIN RICHARDS2

1Department of Statistics, University of Glasgow,

Glasgow G12 8QQ, UK. 2Institute for Integrative

and Comparative Biology, University of Leeds,

Leeds LS2 9JT, UK. 3Dipartimento di Genetica e

Microbiologia, Università di Pavia, 27100 Pavia,

LETTERS

www.sciencemag.org SCIENCE VOL 309 23 SEPTEMBER 2005 1995

Both modern humanmitochondrial DNA…

and the male-specific partof the modern human Y

chromosome have a recentorigin in Africa and were

dispersed throughout therest of the world less than

100,000 years ago…”

–MACAULAY ET AL.

“

[These papers] imply that a modernhuman migration out of Africa with

replacement of all non-African archaichumans is an established fact that

needs no further argument…”

–HARPENDING AND ESWARAN

“

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Proteomics

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1996

Italy. 4Department of Chemical and Biological

Sciences, University of Huddersfield, Huddersfield

HD1 3DH, UK. 5Dipartimento di Genetica e Biologia

Molecolare, Università “La Sapienza,” 00185 Rome,

Italy. 6National Museum of Kuala Lumpur, 50566

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43400 Serdang, Selangor, Malaysia. 8Department of

Forensic Medicine and Science, University of Glasgow,

Glasgow G12 8QQ, UK. 9Department of Forensic and

Investigative Science,University of Central Lancashire,

Preston PR1 2HE, UK. 10School of Archaeology and

Anthropology, The Australian National University,

Canberra ACT 0200, Australia. 11Department of

Mathematics, University of Hamburg, 20146

Hamburg, Germany. 12Department of Anthropology,

University of Oxford, Oxford OX1 2JD, UK.

*To whom correspondence should be addressed.

E-mail: vincent@stats.gla.ac.uk

References1. M. Ingman, H. Kaessmann, S. Pääbo, U. Gyllensten,

Nature 408, 708 (2000).2. Y. Ke et al., Science 292, 1151 (2001).3. A. R.Templeton, Nature 416, 45 (2002).4. D. Garrigan, Z. Mobasher, T. Sverson, J. A. Wilder, M. F.

Hammer, Mol. Biol. Evol. 22, 189 (2005).5. T. Kivisild et al., Am. J. Hum. Genet. 75, 752 (2004).6. S.A.Tishkoff et al., Science 271, 1380 (1996).7. S. Alonso, J. A. L. Armour, Proc. Natl. Acad. Sci. U.S.A.

98, 864 (2001).8. W. S.Watkins et al., Am. J. Hum. Genet. 68, 738 (2001).9. J. Hey, E. Harris, Mol. Biol. Evol. 16, 1423 (1999).

ResponseHARPENDING AND ESWARAN QUESTION THEconcordance between the phylogenetic sig-nals obtained from mitochondrial versusnuclear DNA markers in relation to modernhuman origins. It is well known that becauseof the fourfold higher effective populationsize (Ne) for diploid autosomal loci, theexpected coalescence times of the treesbased on them can be four times deeper thana tree drawn from a haploid locus such asmtDNA. It is also statistically more probablethan for a locus, with smaller Ne, that theroot of the gene tree of a population is notfound in all of the fractions arising after pop-ulation subdivision. Given the stochasticnature of the coalescence process, even themost precise estimate of the time to the mostrecent common ancestor (MRCA) of allhuman lineages would not necessarily carryany conclusive information about the pat-terns of the spread of the genetic variation inthis locus. Unlike the nuclear studies citedby Harpending and Eswaran, our mtDNAstudy and that of Macaulay et al. and thecommentary on them (“Did early humans gonorth or south?”, P. Forster and S.Matsumura, Perspectives, 13 May, p. 965)are focused on the genetic diversity that hasaccumulated on top (downstream) of thereconstructed ancestral sequences—founder haplogroups M, N, and R—that arecommonly shared among distant non-African populations from West Asia toAustralia. The idea behind such a phylogeo-graphic approach is to define the ancestral

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nodes in the tree that carry descendants indistinct regions of the world and to studytheir geographic distribution and time depththrough the coalescent method. By thisapproach, all non-African mtDNAsequences appear to be derived from hap-logroups M, N, and R, which in turn coa-lesce in haplogroup L3, which has a widedistribution in Africa. It is, again, not theoverall coalescence time in haplogroup L3of all the non-African lineages but the aver-aged coalescence times to founder hap-logroups M, N, and R that are considered asthe estimators of the time back to the “out ofAfrica” migration (the outcome could inprinciple be the same even if the non-African MRCA were equal to the globalMRCA). The task of defining such founderhaplotypes and estimating their time depthat nuclear loci is, however, complicatedbecause of the lower substitution rate andthe reshuffling effect of recombination.

KUMARASAMYTHANGARAJ,1 GYANESHWER

CHAUBEY,1TOOMAS KIVISILD,2ALLA G. REDDY,1

VIJAY K. SINGH,1AVINASHA. RASALKAR,1

LALJI SINGH1

1Centre for Cellular and Molecular Biology,

Hyderabad-500 007, India. 2Estonian Biocenter,

Riia 23,Tartu-51010, Estonia.

Bacteria and

Island Biogeography

IN THEIR BREVIA “LARGER ISLANDS HOUSEmore bacterial taxa” (24 June, p. 1884), T.Bell et al. show that the bacterial diversityin bark-lined water pans (“treeholes”) atthe base of beech trees tends to increasewith water volume. This result isexplained in terms of the theory of islandbiogeography (1).

The result is intriguing, but the interpre-tation offered would seem most unlikely.The theory of island biogeography impliesthat in “islands” such as treeholes, speciesnumbers represent a dynamic balancebetween local extinction of species popula-tions and immigration of species that werenot previously present. Absolute popula-tion sizes increase with increasing islandsize, and larger populations are less likelyto suffer stochastic extinctions. Largerislands also represent larger targets forimmigrating propagules, and so they tendto support more species [although surelythe small (~50-ml) treeholes dry out peri-odically?].

Insofar as there are probably no bacter-ial species that are exclusively confined tobark-lined holes at the base of beech trees,these habitats can hardly be considered asislands; rather, they are rapidly inoculatedby bacteria from the surrounding soil andlitter, from rainwater running along branches

and down tree trunks, and by atmosphericdeposition of ubiquitous bacterial spores.Furthermore, bacterial densities in suchwater bodies are likely to be at least 107 to108 cells ml−1, and although these maycomprise many species, such huge popu-lation sizes would preclude stochasticextinctions. The assumptions underlyingthe theory of island biogeography aretherefore not met.

Bell et al.’s species-area curve does notreally fit the predicted power function verywell; rather, bacterial diversity seems toincrease stepwise at treehole volumesaround 1 liter. It is likely that the largerwater bodies support additional micro-habitats. One possibility is that large tree-holes include an anaerobic layer at the bot-tom that accommodates large populationsof other physiological types of bacteria.

TOM FENCHEL1 AND BLAND J. FINLAY2

1Marine Biological Laboratory, University of

Copenhagen, DK–3000 Helsingør, Denmark.2Centre for Ecology and Hydrology Dorset,

Winfrith Technology Centre, Dorchester, Dorset,

DT2 8ZD, UK.

Reference1. R. MacArthur, E. O. Wilson, The Theor y of Island

Biogeography (Princeton Univ. Press, Princeton, NJ,1967).

THE LONG-LASTING DEBATE ABOUT THEubiquitous distribution of microbes hasrecently received considerable attention. Inthe microbial world, is everything poten-tially everywhere provided that the envi-ronmental conditions are adequate? Or dothe same rules apply as for macroscopicorganisms?

With their Brevia “Larger islands housemore bacterial taxa” (24 June, p. 1884), astudy on bacterial diversity in water-filledtreeholes, T. Bell et al. brought an interest-ing contribution to this debate by showingthat, as for larger organisms, a steep micro-bial taxa-area relationship (i.e., the value ofslope z of the regression between diversityand sampling area) is possible. This findingbrings support to the proponents of the pos-sible local distribution of microorganismsby contradicting one of the supposed fun-damental differences between microbesand larger organisms (1).

Although these new results are poten-tially important, I believe that they areundermined by a methodological limitationof the study. Because Bell et al. homoge-nized the water extracted from the treeholesbefore analyzing the community composi-tion, they could not provide a measure ofwithin-habitat heterogeneity, an importantpotential source of overall bacterial diver-sity in the water-filled treehole. Indeed, theobserved increase in bacteria diversity mayat least partly be due to one or more of thefollowing confounding factors that may be

www.sciencemag.org SCIENCE VOL 309 23 SEPTEMBER 2005

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L E T T E R S

associated with a larger body of water: (i)increased potential ecosystem stability(e.g., lower probability of drying out duringextended warm and dry periods, lowersolute concentration fluctuation resultingfrom partial evaporation and rain events,and lower temperature fluctuations); (ii)micro-niche diversity (e.g., stratificationwithin the water body and the organic sedi-ments) (2); and (iii) food-web complexity(e.g., diversity of metazoa inducing top-down effect) (3, 4).

An estimate of possible treehole hetero-geneity would allow reassessment of thefull value of their results. The lack of thisinformation unfortunately does not allow usto establish if their results indeed are in con-tradiction with the “everything is every-where” postulate.

EDWARD A. D. MITCHELL

WSL, Antenne Romande and EPFL-ENAC-ISTE-

ECOS, Lausanne 1015, Switzerland.

References1. B. J. Finlay, G. F. Esteban, T. Fenchel, Protist 155, 15

(2004).2. M. C. Horner-Devine, K. M. Carney, B. J. M. Bohannan,

Proc. R. Soc. London Ser. B Biol. Sci. 271, 113 (2004).3. L. Jiang, P. J. Morin, Am. Nat. 165, 350 (2005).4. E. Zollner, B. Santer, M. Boersma, H. G. Hoppe, K.

Jurgens, Freshwater Biol. 48, 2174 (2003).

Response FENCHEL AND FINLAY HAVE ARGUED THAT

microbes have a cosmopolitan distributionand that the relationship between speciesand area is flat (1). In the sense that ittakes but one black swan to prove that allswans are not white, we have clearlyshown that all microbial taxa-area rela-tionships are not flat.

Fenchel and Finlay claim that (i) becauseno bacterial species are exclusively con-fined to treeholes, they cannot be consid-ered “islands”; (ii) local extinction andcolonization dynamics are unlikely toexplain species richness; and (iii) becauseof their great abundance, bacteria areunlikely to suffer from “stochastic extinc-tion.” However, treeholes clearly do followthe standard ecological def inition of anisland: “a self-contained region whosespecies originate entirely by immigrationfrom outside the region” (2). “Stochasticextinction” refers to individual species; quot-ing abundances of the whole bacterial com-munity is irrelevant. We do not know thelocal colonization or extinction rates, sowhether species richness within a treeholeresults in part from a balance of these tworates is a hypothesis that remains to be tested.

Despite Fenchel and Finlay’s claims, thefit between the data and a power function isexcellent (R2 = 0.91), and the z value (0.26)is within the range of those observed forlarger taxa in island habitats (0.2 to 0.35)(2), a conclusion that is now supported byother recent studies (3, 4). These facts are at

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variance with the “everything is every-where” postulate.

Fenchel and Finlay say that we explainour result in terms of the theory of islandbiogeography (5). In fact our conclusion isthat “[t]he result implies that analogousprocesses structure both microbial commu-nities and communities of larger organ-isms.” This includes many factors beyondthose of colonization and extinction, cen-tral to MacArthur and Wilson’s theory. Thechallenge is to assay these and their relativeimportance.

Mitchell’s principal criticism is that ourresults are “undermined by a methodologi-cal limitation of the study” because thewater was homogenized before describingthe communities. To the contrary, it is pre-cisely this technique that makes the resultscomparable to studies of larger organisms.Nearly every survey of the species-arearelationship on islands, including the clas-sic studies that are most often cited (2), alsohomogenized the habitats from each island.

Habitat heterogeneity, ecosystem stabil-ity, and food-web complexity are not con-founding factors; rather, they are mecha-nisms that might explain the pattern that weobserved. Some form of stratified samplingmight have allowed us to assess the degree ofcorrelation between treehole volume andhabitat heterogeneity. However, the onlyappropriate way to establish the mechanismsthat underlie the observed pattern is by con-ducting randomized experiments in whichwe manipulate the treeholes to directly testthese hypotheses. As recent studies havedemonstrated (6), inferring process frompattern is fraught with difficulty.

We sought to determine if a relationshipexists between treehole volume and bacter-ial genetic diversity. We did not set out toestablish the cause of this pattern, nor didwe set out to resolve the long-standingdebate on the ubiquity of bacterial species.Our conclusion that, as for larger organ-isms, comparatively steep microbialspecies-area relationships are possible, isnot altered by knowledge of the causalmechanism(s). We agree that the logicalnext step for research is to uncover themechanism, but doing so will take morethan a stratified sampling procedure.

THOMAS BELL,1,2 JONATHAN A. NEWMAN,3 IAN P.

THOMPSON,1 ANDREW K. LILLEY,1 CHRISTOPHER J.

VAN DER GAST1*1Natural Environment Research Council (NERC)

Centre for Ecology and Hydrology, Mansfield Road,

Oxford OX1 3SR, UK. 2Department of Zoology,

University of Oxford, South Parks Road, Oxford

OX1 3PS, UK. 3Department of Environmental

Biology, University of Guelph, Guelph, ON N1G

2W1, Canada.

*To whom correspondence should be addressed.

E-mail: cjvdg@ceh.ac.uk

References 1. T. Fenchel, B. J. Finlay, Bioscience 54, 777 (2004).2. M. L. Rosenzweig, Species Diversity in Space and Time

(Cambridge Univ. Press, Cambridge, 1995).3. C.J. van der Gast et al., Environ. Microbiol. 7, 1220

(2005).4. I. Reche et al., Ecology 86, 1715 (2005).5. R. H. MacArthur, E. O. Wilson, The Theory of Island

Biogeography (Princeton Univ. Press, Princeton, NJ,1967).

6. G. Bell, Science 293, 2413 (2001).

CORRECTIONS AND CLARIFICATIONS

News Focus: “Sky-high experiments” by E. Pennisi(26 Aug., p. 1314). On page 1315, in the first para-graph of the second column, the sentence “Overall,the carbon in the soil increased by 44%” shouldhave read “Overall, the carbon dioxide in the soilincreased by 44%.”

TECHNICAL COMMENT ABSTRACTS

COMMENT ON “Status and Trends ofAmphibian Declines andExtinctions Worldwide”

Bruno V. S. Pimenta, Célio F. B. Haddad,Luciana B. Nascimento, Carlos AlbertoGonçalves Cruz, José P. Pombal Jr.

Stuart et al. (Reports, 3 Dec . 2004, p. 1783)reported that 1856 amphibian species are threat-ened worldwide according to the IUCN Red List cri-teria. However, a methodic analysis of their results,using Brazilian species as a case study, shows thatthis number is an overestimate resulting from mis-use of the IUCN Criteria and insufficient data.Full text atwww.sciencemag.org/cgi/content/full/309/5743/1999b

RESPONSE TO COMMENT ON “Statusand Trends of Amphibian Declinesand Extinctions Worldwide”

Simon N. Stuart, Janice S. Chanson, Neil A.Cox, Bruce E.Young,Ana S. L. Rodrigues,Debra L. Fischman, Robert W.Waller

Using information on Brazilian species, Pimenta etal. assert that we overestimated the number ofthreatened amphibians. However, this claim, basedon a misunderstanding of the IUCN Red List crite-ria and a strongly evidentiary attitude to listingspecies, almost certainly seriously underestimatesthe number of threatened amphibians in Brazil.Full text atwww.sciencemag.org/cgi/content/full/309/5743/1999c

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www.sciencemag.org SCIENCE VOL 309 23 SEPTEMBER 2005

Letters to the EditorLetters (~300 words) discuss material publishedin Science in the previous 6 months or issues ofgeneral interest. They can be submittedthrough the Web (www.submit2science.org) orby regular mail (1200 New York Ave., NW,Washington, DC 20005, USA). Letters are notacknowledged upon receipt, nor are authorsgenerally consulted before publication.Whether published in full or in part, letters aresubject to editing for clarity and space.

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