Y-chromosome descent clusters and male differential reproductive success: young lineage expansions dominate Asian pastoral nomadic populations.

Patricia Balaresque,Lluis Quintana-Murci,Sylvain Cussat-Blanc,Patrice Gerard,Mark A Jobling,Nicolas Poulet,Evelyne Heyer

doi:10.1038/ejhg.2014.285

Abstract

High-frequency microsatellite haplotypes of the male-specific Y-chromosome can signal past episodes of high reproductive success of particular men and their patrilineal descendants. Previously, two examples of such successful Y-lineages have been described in Asia, both associated with Altaic-speaking pastoral nomadic societies, and putatively linked to dynasties descending, respectively, from Genghis Khan and Giocangga. Here we surveyed a total of 5321 Y-chromosomes from 127 Asian populations, including novel Y-SNP and microsatellite data on 461 Central Asian males, to ask whether additional lineage expansions could be identified. Based on the most frequent eight-microsatellite haplotypes, we objectively defined 11 descent clusters (DCs), each within a specific haplogroup, that represent likely past instances of high male reproductive success, including the two previously identified cases. Analysis of the geographical patterns and ages of these DCs and their associated cultural characteristics showed that the most successful lineages are found both among sedentary agriculturalists and pastoral nomads, and expanded between 2100 BCE and 1100 CE. However, those with recent origins in the historical period are almost exclusively found in Altaic-speaking pastoral nomadic populations, which may reflect a shift in political organisation in pastoralist economies and a greater ease of transmission of Y-chromosomes through time and space facilitated by the use of horses.

Highlights

Reproductive success, widely used as a measure of fitness, is described as the genetic contribution of an individual to future generations.1Human behavioural ecologists use various fertility-specific measures to directly estimate reproductive success in extant populations; indirect estimates of past reproductive success can be obtained through evolutionary population genetic approaches, which demonstrate that its cultural transmission can be extremely effective.3,4High variance of male reproductive success is detectable from genetic data because it leads to many Y-chromosomal lineages becoming extinct through drift and others expanding markedly
Of which were unique, and 15 haplotypes (0.6%) were each present times, indicating probable examples of successful transmissions (Figure 2). We focused on these 15 haplotypes and studied their spatial distributions and ages to illuminate the history of high reproductive success of their respective common ancestors
Frequent haplotypes are expected to be accompanied by neighbouring haplotypes within the same Y-SNP haplogroup that arise from them via mutation, thereby forming descent clusters (DCs)

Summary

Introduction

Reproductive success, widely used as a measure of fitness, is described as the genetic contribution of an individual to future generations.1Human behavioural ecologists use various fertility-specific measures to directly estimate reproductive success in extant populations (eg, Strassmann and Gillespie2); indirect estimates of past reproductive success can be obtained through evolutionary population genetic approaches, which demonstrate that its cultural transmission can be extremely effective.3,4High variance of male reproductive success is detectable from genetic data because it leads to many Y-chromosomal lineages becoming extinct through drift and others expanding markedly. Reproductive success, widely used as a measure of fitness, is described as the genetic contribution of an individual to future generations.. Human behavioural ecologists use various fertility-specific measures to directly estimate reproductive success in extant populations (eg, Strassmann and Gillespie2); indirect estimates of past reproductive success can be obtained through evolutionary population genetic approaches, which demonstrate that its cultural transmission can be extremely effective.. High variance of male reproductive success is detectable from genetic data because it leads to many Y-chromosomal lineages becoming extinct through drift and others expanding markedly. For any increase to lead to a high population frequency, two factors are needed: biological, with a need for men to be fertile, and cultural, with a continued transmission of reproductive success over generations. The best-known instance is the finding that ~ 0.5% of the world’s Y-chromosomes belongs to a single Asian patrilineage, descending from a common ancestor in historical times, and suggested to be due to the imperial dynasty founded by Genghis Khan

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