ReviewHuman demographic history: refining the recent African origin model
Introduction
Reconstructing human demography goes far beyond a justified curiosity about our past. It is essential in order to find evidence for adaptation at the molecular level, or to correctly interpret and predict levels of linkage disequilibrium (LD), which measures the strength of the association between nearby loci along a chromosome permitting the fine determination of disease gene positions. At the end of the 1980s, the first studies of human molecular diversity suggested that our species had evolved from a small African population that had subsequently colonised the whole world, supplanting former hominids, ∼120–200 thousand years (KY) ago 1., 2., 3., around the time of the first appearance of anatomically modern humans [4••]. This replacement model, which was later coined as the ‘Out of Africa’, or ‘Recent African Origin’ (RAO) model (Fig. 1a), has since been widely adopted by the human population genetics community. It was, however, disputed by some archaeologists for whom there is evidence of a regional continuity in the Pleistocene fossil record, which cannot be explained by a complete replacement of Homo erectus in Asia or Neanderthals in Europe [5]. They proposed instead a model of multiregional evolution (MRE), where modern humans would have emerged gradually and simultaneously from Homo erectus on different continents, this coherence being made possible by ongoing gene flow between continental groups [6] (Fig. 1b). Further examination of the pattern of mitochondrial DNA (mtDNA) diversity also revealed an excess of rare variants 7., 8•. and unimodal distributions of pairwise differences [9], which are expected after a population expansion or an episode of positive selection, both leading to star-shaped gene trees [10]. Although it is difficult to differentiate selective from demographic factors by looking at a single genetic marker, these results were interpreted as evidence for large Pleistocene demographic expansions [11]. In the past few years, the genetic diversity of sexual and autosomal chromosomes has been further examined, providing more opportunities to check the validity of the models of human evolution and demography previously based on mtDNA. Patterns of nuclear diversity in coding regions were sometimes found to be markedly different from those seen in mtDNA, with much older coalescence times and less evidence for past demographic expansions [12], thus calling into question the validity and the generality of the simple RAO model of human evolution 13., 14•..
Section snippets
Larger and older genetic diversity in Africa
A majority of studies have shown that African populations harbour more genetic diversity than non-African populations for mtDNA sequences 2., 15., Y chromosome microsatellites 16., 17., Y chromosome sequences 18., 19., 20., Y chromosome SNPs (single-nucleotide polymorphisms) 21•., 22., X chromosome sequences 23., 24., 25., 26., autosomal microsatellites 27., 28., autosomal sequences 29., 30., 31••., 32., 33•., 34••., as well as autosomal SNPs [35••]. This basic result is generally interpreted
Lower levels of linkage disequilibrium in African populations
Another important line of evidence in favour of an African origin of modern humans comes from the analysis of patterns of LD within populations. Two recent studies of SNP diversity across the genome 50., 51••. have confirmed previous reports of lower LD levels in African populations (e.g. [44]). The first study, based on 272 ‘high frequency’ polymorphisms in 19 random genome regions, showed that high levels of LD (D’>0.5) were evident only over much shorter distances in a Nigerian population (5
Past expansions rule
Examination of mitochondrial diversity has led many authors to postulate that human populations had gone through one or more episodes of large Pleistocene population expansions 40–200 KY ago, resulting in star-shape gene genealogies 9., 10., 11., and causing rejection of tests of selective neutrality and population equilibrium 7., 54.. However, similar signatures of population expansions have been more difficult to find from nuclear diversity studies. Examination of microsatellite diversity
Demographic expansions due to range expansion
Predictions about the genetic consequences of demographic expansions (e.g. star-like trees) have been formulated for the case of a single unsubdivided population, which is not very realistic. Although demographic expansions can be linked to technological innovations [63•], which raise the carrying capacity of a given population, they can also result from a range expansion increasing the total size of the population by augmenting the number of occupied sites. Range expansions could result from
Demography versus selection
Assuming past expansion of human populations leads one to predict that the expected pattern of molecular diversity at neutral loci — shown by negative Tajima's D statistics and an excess of rare variants — should be similar to that expected under positive selection in stationary populations. Loci that show departures from these expectations would thus be likely candidates for selection. Paradoxically, this would include loci showing no apparent departure from selective neutrality and population
Towards more refined models of human evolution
Both the RAO and MRE models of human evolution are certainly overly simple, as they do not fully account for subdivisions within continents [61••], potential climatic changes affecting migration patterns and census sizes of populations [40], long-range migrations [14•], technical and cultural innovations, potential sex-linked differences in generation-time [20], dispersal abilities, social structure [66••], and mating behaviour. Although it is difficult to account for all these parameters in an
Conclusions
If the MRE model or a non-African origin cannot be ruled out and were favoured for explaining past human demography, the larger genetic diversity found in Africa would nevertheless imply that the effective size of sub-Saharan Africa has been much larger than that of the sum of all other continents for much of recent human evolution 37., 38••.. In that case, most of the genetic diversity of modern humans would still have originated in Africa, resulting in a pattern extremely similar to that
Acknowledgements
Thanks to Grant Hamilton, Carlo Largiadèr, and Montgomery Slatkin for their comments on the manuscript. This work was supported by Swiss NSF grants No 31-54059.98 and 31-56755.99.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Now in press
The work referred to in the text as (N Ray, M Currat, L Excoffier, unpublished data) is now in press.
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