Population resequencing of European mitochondrial genomes highlights sex-bias in Bronze Age demographic expansions

Chiara Batini,Daniel Zadik,Horolma Pamjav,Mark A Jobling,Jon H Wetton,Pille Hallast,Åshild J Vågene,Antti Sajantila,Heidi A Eriksen

doi:10.1038/s41598-017-11307-9

Abstract

Interpretations of genetic data concerning the prehistory of Europe have long been a subject of great debate, but increasing amounts of ancient and modern DNA data are now providing new and more informative evidence. Y-chromosome resequencing studies in Europe have highlighted the prevalence of recent expansions of male lineages, and focused interest on the Bronze Age as a period of cultural and demographic change. These findings contrast with phylogeographic studies based on mitochondrial DNA (mtDNA), which have been interpreted as supporting expansions from glacial refugia. Here we have undertaken a population-based resequencing of complete mitochondrial genomes in Europe and the Middle East, in 340 samples from 17 populations for which Y-chromosome sequence data are also available. Demographic reconstructions show no signal of Bronze Age expansion, but evidence of Paleolithic expansions in all populations except the Saami, and with an absence of detectable geographical pattern. In agreement with previous inference from modern and ancient DNA data, the unbiased comparison between the mtDNA and Y-chromosome population datasets emphasizes the sex-biased nature of recent demographic transitions in Europe.

Highlights

Our understanding of European prehistory has been revolutionized by the availability of new DNA sequencing technologies[1], which have allowed the unbiased characterization of sequence variation in modern and ancient human genomes
To allow a comparison between female and male histories, we resequenced the mitochondrial genomes of 340 European and Middle Eastern individuals belonging to 17 populations (Table S1) that were previously analyzed for MSY12
We constructed a maximum parsimony (MP) tree (Fig. 1a; see median-joining network in Figure S1) based on the mitochondrial DNA (mtDNA) coding region only, which is best suited for reliable phylogenetic inference due to its relatively low content of recurrently mutating sites (Figure S2 presents a median-joining network based on the entire sequence)

Summary

Introduction

Our understanding of European prehistory has been revolutionized by the availability of new DNA sequencing technologies[1], which have allowed the unbiased characterization of sequence variation in modern and ancient human genomes. Patterns of diversity suggested low Paleolithic population sizes, with regional differences among Western and Scandinavian groups[6] This picture has been further refined by the study of the DNA of ancient Yamnaya herders from the region of the Pontic-Caspian steppe, the apparent source of Bronze Age migrations into Europe and Asia[7,8,9], and a debated region of origin for Indo-European languages[10]. Analyses of aDNA show that today’s most frequent Y-chromosome haplogroup (R1b-M269) is very rare in Europe until 4.5 KYA5 (see summary elsewhere12), while it is present in all the Yamnaya samples[8,9] This had initially suggested a major introgression of males from the Pontic-Caspian steppe; the R1b sublineage (R1b-L11) common in Europe has not so far been found among Yamnaya sequences[13]. The pattern observed in mtDNA is strikingly different from that in MSY, compatible with expansion after the Last Glacial Maximum, and emphasizing the male-specific nature of the Bronze Age expansion in Europe

Methods

Results

Conclusion