Human genetic differentiation across the Strait of Gibraltar

Abstract

Background: The Strait of Gibraltar is a crucial area in the settlement history of modern humans because it represents a possible connection between Africa and Europe. So far, genetic data were inconclusive about the fact that this strait constitutes a barrier to gene flow, as previous results were highly variable depending on the genetic locus studied. The present study evaluates the impact of the Gibraltar region in reducing gene flow between populations from North-Western Africa and South-Western Europe, by comparing formally various genetic loci. First, we compute several statistics of population differentiation. Then, we use an original simulation approach in order to infer the most probable evolutionary scenario for the settlement of the area, taking into account the effects of both demography and natural selection at some loci.

Results: We show that the genetic patterns observed today in the region of the Strait of Gibraltar may reflect an ancient population genetic structure which has not been completely erased by more recent events such as Neolithic migrations. Moreover, the differences observed among the loci (i.e. a strong genetic boundary revealed by the Y-chromosome polymorphism and, at the other extreme, no genetic differentiation revealed by HLA-DRB1 variation) across the strait suggest specific evolutionary histories like sex-mediated migration and natural selection. By considering a model of balancing selection for HLA-DRB1, we here estimate a coefficient of selection of 2.2% for this locus (although weaker in Europe than in Africa), which is in line with what was estimated from synonymous versus non-synonymous substitution rates. Selection at this marker thus appears strong enough to leave a signature not only at the DNA level, but also at the population level where drift and migration processes were certainly relevant.

Conclusions: Our multi-loci approach using both descriptive analyses and Bayesian inferences lead to better characterize the role of the Strait of Gibraltar in the evolution of modern humans. We show that gene flow across the Strait of Gibraltar occurred at relatively high rates since pre-Neolithic times and that natural selection and sex-bias migrations distorted the demographic signal at some specific loci of our genome.

Figure 1

Proportion of genetic variance (average value) due to differences between the two continental groups of populations South-Western Europe (SWE) and North-Western Africa (NWA) (A) and within both groups (B).

Figure 2

Proportion of the best 0.25% simulations among 400,000 for each of 4 alternative scenarios and RH, GM, Y-chromosome and mtDNA loci. P stands for Palaeolithic scenario, N for Neolithic, PN for Palaeolithic and Neolithic and PNI for Palaeolithic, Neolithic and Islamic expansion (see text for details).

Figure 3

Curves representing the prior (dotted line) and posterior distributions (plain lines) obtained for the Nm_intra and Nm_inter parameters of scenario P and 4 genetic loci: RH, GM, mtDNA and Y chromosome ("Y-STR" and "Y-SNP") as well as the estimation for the 4 loci taken together ("All loci"). The mode of the distribution is given in brackets.

Figure 4

Curves representing the prior (dotted black line) and posterior distributions (plain line) obtained for the selection coefficient s with scenarios P at HLA-DRB1 as well as MNSs and ABO loci. The modes and the 90% CI of the posterior distributions are given. For HLA-DRB1, s has also been estimated independently in North-Western Africa (in dashed grey) and South-Western Europe (in dashed blue), see text for details.

Figure 5

Schematic representation of the two grids of demes representing South-Western Europe (SWE) and North-Western Africa (NWA). The whole simulated area is subdivided into 256 demes. The two crosses represent the demes where the settlement of the areas starts from a common genetic pool t generations ago. There are two different migration rates: m_intra is the migration rate between demes within a continent (either SWE or NWA) and m_inter is the migration rate between demes among continents. Continents are connected by 8 demes on each side.