Origins of modern humans still look recent.

Hey and Harris take exception to some of the points that I raised about their recent work in my review of new findings in human origins research [1xHuman evolution: origins of modern humans still look recent. Disotell, T. Curr Biol. 1999; 9: R647–R650Abstract | Full Text | Full Text PDF | PubMed | Scopus (15)See all References[1]. Their first point regards the debate between the “recent replacement” model and the “multiregional model”. I defined the “recent replacement” model as one in which “a single population, most likely of African origin, expanded and replaced archaic populations throughout the world, beginning around 200,000 years ago.” The model in general is supported by numerous researchers (reviewed in [1xHuman evolution: origins of modern humans still look recent. Disotell, T. Curr Biol. 1999; 9: R647–R650Abstract | Full Text | Full Text PDF | PubMed | Scopus (15)See all References, 3xThe evolution of modern humans: a comparison of the African and non-African evidence. Brauer, G. : 123–154See all References, 9xSex-specific contributions to genome variation. Disotell, T.R. Curr Biol. 1999; 9: R29–R31Abstract | Full Text | Full Text PDF | PubMed | Scopus (13)See all References]), and this statement in particular does not imply that this population consisted of anatomically modern humans. It might very well have been, and probably was, an African archaic population, given that no anatomically modern fossils approach this date. Furthermore, although some of the oldest anatomically modern fossil humans are known from the Israeli sites of Skhul and Jebel Qafzeh, this area at the time could be considered an extension of Africa on the basis of the numerous “Ethiopian” mammal species present [2xThe Human Career: Human Biological and Cultural Origins. Klein, R.G. See all References[2]. Although this population might have been “out of Africa” by our contemporary standards, these people surely had close affinities with slightly older south, east, and north African populations. I cannot argue with their contention that population subdivision probably existed within Africa before populations left in a new wave of migrations most probably between 50,000 and 100,000 years ago, after the initial dispersals out of Africa more than a million years ago. My main point was that populations living in Asia and Europe at that time were replaced by these new immigrants as the vast majority of genetic systems studied to date suggest (reviewed in [1xHuman evolution: origins of modern humans still look recent. Disotell, T. Curr Biol. 1999; 9: R647–R650Abstract | Full Text | Full Text PDF | PubMed | Scopus (15)See all References, 3xThe evolution of modern humans: a comparison of the African and non-African evidence. Brauer, G. : 123–154See all References, 9xSex-specific contributions to genome variation. Disotell, T.R. Curr Biol. 1999; 9: R29–R31Abstract | Full Text | Full Text PDF | PubMed | Scopus (13)See all References]), which stands in opposition to the multiregional model that posits in situ evolution in these regions from indigenous archaic populations. I did make an error by implying that they only sequenced eight African individuals in their study of the PDHA1 locus [7xX chromosome evidence for ancient human histories. Harris, E.E. and Hey, J. Proc Natl Acad Sci USA. 1999; 96: 3320–3324Crossref | PubMed | Scopus (174)See all References[7], when in fact they found eight haplotypes out of the sixteen African individuals actually sequenced. Given the enormous diversity found within Africa for almost all of the genetic systems examined to date (which is supported by Harris and Hey’s study), I would still contend, as Seielstadt et al. [10xA view of modern human origins from Y chromosome microsatellite variation. Seielstad, M., Bekele, E., Ibrahim, M., Tour, A., and Traor, M. Genome Res. 1999; 9: 558–567PubMedSee all References[10] do, that additional sampling is merited to verify that alleles shared between Africans and non-Africans have not been missed. A good example of this problem has recently been reported by Kivisild et al. [11xDeep common ancestry of Indian and western Eurasian mtDNA lineages. Kivisild, T., Bamshad, M.J., Kaldma, K., Metspalu, M., Metspalu, E., Reidla, M., Laos, S., Parik, J., Watkins, W.S., Dixon, M.E. et al. Curr Biol. 1999; 9: 1331–1334Abstract | Full Text PDF | PubMedSee all References[11] in which the mitochondrial haplogroup U, which was considered to be western Eurasian-specific and had never been reported in India or further east, turns out to be the second most common haplogroup in the subcontinent after they typed 550 Indian mtDNA (mitochondrial DNA) samples. Hey and Harris and I also disagree over the significance of potential unequal rates of evolution in the PDHA1 locus among primates. I presented a phylogenetic analysis in which I suggested that unequal rates were present and were evidence of potential selection, which would call into question rate and dating estimates. I performed this analysis because, as Harding [12xMore on the X files. Harding, R.M. Proc Natl Acad Sci USA. 1999; 96: 2582–2584Crossref | PubMed | Scopus (8)See all References[12] did in a commentary on their work, I questioned a comparison to β globin as a test of the presence of selection. Given the known function of PDHA1, I along with Harding [12xMore on the X files. Harding, R.M. Proc Natl Acad Sci USA. 1999; 96: 2582–2584Crossref | PubMed | Scopus (8)See all References[12] and Brown et al. [13xTransfection screening for primary defects in the pyruvate dehydrogenase E1a subunit gene. Brown, R.M., Otero, L.J., and Brown, G.K. Human Mol Genet. 1997; 6: 1361–1367Crossref | PubMed | Scopus (19)See all References[13] suspect that selection might be acting on this locus. I also suspect that additional sampling of more chimpanzees will lead to review of numerous other substitutions, perhaps resulting in the reinterpretation of several of the within-human differences. My surprise was not that differences were found between the chimpanzees but that so few were found given that chimpanzees are several-fold more genetically diverse than humans [1xHuman evolution: origins of modern humans still look recent. Disotell, T. Curr Biol. 1999; 9: R647–R650Abstract | Full Text | Full Text PDF | PubMed | Scopus (15)See all References, 8xEvolution of a HOXB6 intergenic region within the great apes and humans. Deinard, A. and Kidd, K. J Hum Evol. 1999; 36: 687–703Crossref | PubMed | Scopus (47)See all References].Relative-rate tests [14xEvidence for higher rates of nucleotide substitution in rodents than in man. Wu, C.I. and Li, W.H. Proc Natl Acad Sci USA. 1985; 82: 1741–1745Crossref | PubMedSee all References[14] do not find statistically significant deviations from equivalent amounts of change along the human and chimpanzee lineages since their common ancestry (Hey, personal communication). This is probably because of the lack of power of this test when so few substitutions are present. The point of this exercise was, however, to again call into question the estimated rates of change and therefore divergence dates estimated from a locus known to have significant physiological effects [12xMore on the X files. Harding, R.M. Proc Natl Acad Sci USA. 1999; 96: 2582–2584Crossref | PubMed | Scopus (8)See all References, 13xTransfection screening for primary defects in the pyruvate dehydrogenase E1a subunit gene. Brown, R.M., Otero, L.J., and Brown, G.K. Human Mol Genet. 1997; 6: 1361–1367Crossref | PubMed | Scopus (19)See all References].To be compatible with the coalescent date of approximately 200,000 years ago for the haploid mtDNA and Y chromosome, X-linked loci such as PDHA1 should yield estimates three times as great, in the range of 600,000 years ago, not the 1.86 million year date inferred by Harris and Hey [7xX chromosome evidence for ancient human histories. Harris, E.E. and Hey, J. Proc Natl Acad Sci USA. 1999; 96: 3320–3324Crossref | PubMed | Scopus (174)See all References[7]. Nachman et al. [15xDNA variability and recombination rates at X-linked loci in humans. Nachman, M.W., Bauer, V.L., Crowell, S.L., and Aquadro, C.F. Genetics. 1998; 150: 1133–1141PubMedSee all References[15], in a study comprising seven X-linked loci, including Hey’s earlier study of PDHA1 [16xMitochondrial and nuclear genes present conflicting portraits of human origins. Hey, J. Mol Biol Evol. 1997; 14: 166–172Crossref | PubMedSee all References[16], estimate mean and mode values of 743,000 and 655,000 years ago, respectively, for the human coalescent date, which is broadly compatible with the mtDNA and Y chromosome results [9xSex-specific contributions to genome variation. Disotell, T.R. Curr Biol. 1999; 9: R29–R31Abstract | Full Text | Full Text PDF | PubMed | Scopus (13)See all References[9]. Interestingly, both PDHA1 and dystrophin produce the two oldest estimates in the study of Nachman et al. [15xDNA variability and recombination rates at X-linked loci in humans. Nachman, M.W., Bauer, V.L., Crowell, S.L., and Aquadro, C.F. Genetics. 1998; 150: 1133–1141PubMedSee all References[15]. Given the numerous genetic studies supporting the “recent replacement” model, my intent in reviewing Harris and Hey’s results was to amplify Harding’s [12xMore on the X files. Harding, R.M. Proc Natl Acad Sci USA. 1999; 96: 2582–2584Crossref | PubMed | Scopus (8)See all References[12] view that “…against the expectations suggested by most other polymorphism data, it is clear that something odd has happened — and perhaps is happening — at the PDHA1 locus.”Department of Anthropology, New York University, New York, NY 10003, USA. E-mail: todd.disotell@nyu.edu