X-Linked MTMR8 Diversity and Evolutionary History of Sub-Saharan Populations

Damian Labuda,Jean-François Lefebvre,Claudia Moreau,Vania Yotova,Gerd Utermann,Scott M Williams,Francesc Calafell

doi:10.1371/journal.pone.0080710

Abstract

The genetic diversity within an 11 kb segment of the MTMR8 gene in a sample of 111 sub-Saharan and 49 non-African X chromosomes was investigated to assess the early evolutionary history of sub-Saharan Africans and the out-of-Africa expansion. The analyses revealed a complex genetic structure of the Africans that contributed to the emergence of modern humans. We observed partitioning of two thirds of old lineages among southern, west/central and east African populations indicating ancient population stratification predating the out of Africa migration. Age estimates of these lineages, older than coalescence times of uniparentally inherited markers, raise the question whether contemporary humans originated from a single population or as an amalgamation of different populations separated by years of independent evolution, thus suggesting a greater antiquity of our species than generally assumed. While the oldest sub-Saharan lineages, ∼500 thousand years, are found among Khoe-San from southern-Africa, a distinct haplotype found among Biaka is likely due to admixture from an even older population. An East African population that gave rise to non-Africans underwent a selective sweep affecting the subcentromeric region where MTMR8 is located. This and similar sweeps in four other regions of the X chromosome, documented in the literature, effectively reduced genetic diversity of non-African chromosomes and therefore may have exacerbated the effect of the demographic bottleneck usually ascribed to the out of Africa migration. Our data is suggestive, however, that a bottleneck, occurred in Africa before range expansion.

Highlights

In light of recent data, human evolutionary history looks much more complex than what geneticists postulated only a decade ago [1]
The greatest genetic diversity among human populations is observed in sub-Saharan Africa, which leads to revisiting the old question [11,12]: Is greater genetic diversity in Africa due only to older and larger ancestral African population sizes as compared to those outside of Africa, or does it reflect the impact primarily of the out of Africa population bottleneck(s) in reducing the genetic diversity outside Africa? If at the time of out-of-Africa migration Africans and migrant populations did not differ in their genetic structure, but African populations stayed larger than non-Africans, greater African diversity would be expected to result from an accumulation of new low frequency local variants
Extensive gene flow shaped the diversity of sub-Saharan Africans over various periods [19,20,21,22], traces of the ancestral subdivisions can still be recognized in the genetic record [6,20,23,24,25,26]; the homogenizing effect of gene flow that in general will partially conceal the record of the ancestral population structure, is expected to be less obvious in areas of low recombination and strong linkage disequilibrium [27]

Summary

Introduction

In light of recent data, human evolutionary history looks much more complex than what geneticists postulated only a decade ago [1]. Extensive gene flow shaped the diversity of sub-Saharan Africans over various periods [19,20,21,22], traces of the ancestral subdivisions can still be recognized in the genetic record [6,20,23,24,25,26]; the homogenizing effect of gene flow that in general will partially conceal the record of the ancestral population structure, is expected to be less obvious in areas of low recombination and strong linkage disequilibrium [27] Studying loci with such characteristics is of great significance in terms of unravelling human population histories. Single locus oriented studies, can reveal particular and sometimes unusually important historical events, such as that of archaic admixture within Africa, and/or that of Neandertal admixture outside Africa, as documented in our earlier studies focusing on specific DNA segments [4,6,10,28,29]

Methods

Results

Discussion

Conclusion