Human paternal and maternal demographic histories: insights from high-resolution Y chromosome and mtDNA sequences.

Sebastian Lippold,Anne Butthof,Mingkun Li,Hongyang Xu,Roland Schröder,Mark Stoneking,Albert Ko,Gabriel Renaud

doi:10.1186/2041-2223-5-13

Abstract

BackgroundComparisons of maternally-inherited mitochondrial DNA (mtDNA) and paternally-inherited non-recombining Y chromosome (NRY) variation have provided important insights into the impact of sex-biased processes (such as migration, residence pattern, and so on) on human genetic variation. However, such comparisons have been limited by the different molecular methods typically used to assay mtDNA and NRY variation (for example, sequencing hypervariable segments of the control region for mtDNA vs. genotyping SNPs and/or STR loci for the NRY). Here, we report a simple capture array method to enrich Illumina sequencing libraries for approximately 500 kb of NRY sequence, which we use to generate NRY sequences from 623 males from 51 populations in the CEPH Human Genome Diversity Panel (HGDP). We also obtained complete mtDNA genome sequences from the same individuals, allowing us to compare maternal and paternal histories free of any ascertainment bias.ResultsWe identified 2,228 SNPs in the NRY sequences and 2,163 SNPs in the mtDNA sequences. Our results confirm the controversial assertion that genetic differences between human populations on a global scale are bigger for the NRY than for mtDNA, although the differences are not as large as previously suggested. More importantly, we find substantial regional variation in patterns of mtDNA versus NRY variation. Model-based simulations indicate very small ancestral effective population sizes (<100) for the out-of-Africa migration as well as for many human populations. We also find that the ratio of female effective population size to male effective population size (Nf/Nm) has been greater than one throughout the history of modern humans, and has recently increased due to faster growth in Nf than Nm.ConclusionsThe NRY and mtDNA sequences provide new insights into the paternal and maternal histories of human populations, and the methods we introduce here should be widely applicable for further such studies.

Highlights

Comparisons of maternally-inherited mitochondrial DNA and paternally-inherited non-recombining Y chromosome (NRY) variation have provided important insights into the impact of sex-biased processes on human genetic variation
The seminal finding that NRY differences are bigger than mitochondrial DNA (mtDNA) differences among global populations of humans, and that this is due to a higher rate of female than male migration due to patrilocality [6], may instead reflect methodological differences in how mtDNA versus NRY variation was assayed in that study [7]
To allow for more accurate comparisons between mtDNA and NRY variation and to permit demographic inferences based on the NRY, we developed a capture-based array to enrich Illumina sequencing libraries for approximately 500 kb of NRY sequence

Summary

Introduction

Comparisons of maternally-inherited mitochondrial DNA (mtDNA) and paternally-inherited non-recombining Y chromosome (NRY) variation have provided important insights into the impact of sex-biased processes (such as migration, residence pattern, and so on) on human genetic variation. MtDNA variation is usually investigated by sequencing hypervariable segments of the control region, (or, increasingly, via complete mtDNA genome sequences), mtDNA differences among global populations of humans, and that this is due to a higher rate of female than male migration due to patrilocality [6], may instead reflect methodological differences in how mtDNA versus NRY variation was assayed in that study [7]. Another fundamental question concerns whether or not male and female effective population sizes have been the same over time. These and other fundamental aspects of human maternal and paternal demographic history remain unanswered

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