House mouse Mus musculus dispersal in East Eurasia inferred from 98 newly determined complete mitochondrial genome sequences

Kuniya Abe,Toshihiko Shiroishi,Naruya Saitou,Naoki Osada,Yue Li,Hiromichi Yonekawa,Toyoyuki Takada,Hitoshi Suzuki,Kazuo Moriwaki,Alexey P. Kryukov,Kazumichi Fujiwara,Yosuke Kawai

doi:10.1038/s41437-020-00364-y

Abstract

The Eurasian house mouse Mus musculus is useful for tracing prehistorical human movement related to the spread of farming. We determined whole mitochondrial DNA (mtDNA) sequences (ca. 16,000 bp) of 98 wild-derived individuals of two subspecies, M. m. musculus (MUS) and M. m. castaneus (CAS). We revealed directional dispersals reaching as far as the Japanese Archipelago from their homelands. Our phylogenetic analysis indicated that the eastward movement of MUS was characterised by five step-wise regional extension events: (1) broad spatial expansion into eastern Europe and the western part of western China, (2) dispersal to the eastern part of western China, (3) dispersal to northern China, (4) dispersal to the Korean Peninsula and (5) colonisation and expansion in the Japanese Archipelago. These events were estimated to have occurred during the last 2000–18,000 years. The dispersal of CAS was characterised by three events: initial divergences (ca. 7000–9000 years ago) of haplogroups in northernmost China and the eastern coast of India, followed by two population expansion events that likely originated from the Yangtze River basin to broad areas of South and Southeast Asia, including Sri Lanka, Bangladesh and Indonesia (ca. 4000–6000 years ago) and to Yunnan, southern China and the Japanese Archipelago (ca. 2000–3500). This study provides a solid framework for the spatiotemporal movement of the human-associated organisms in Holocene Eastern Eurasia using whole mtDNA sequences, reliable evolutionary rates and accurate branching patterns. The information obtained here contributes to the analysis of a variety of animals and plants associated with prehistoric human migration.

Highlights

The early to mid-Holocene is a crucial period in the development of present day human cultural and genetic diversity
A NN network constructed from the mitogenome sequences yielded four distinct lineages, designated CAS, DOM, MUS and NEP, representing the subspecies M. m. castaneus, M. m. domesticus, M. m. musculus and a hitherto unknown lineage (NEP) collected from Nepal, respectively (Supplementary Fig. S2)
The early and middle Holocene is a crucial time period, when the fundamental regional human populations and cultures were established through colonisation and transfer of agricultural systems

Summary

Introduction

The early to mid-Holocene is a crucial period in the development of present day human cultural and genetic diversity. The three subspecies are known to have settled in their present geographic territories due to human activities from the Neolithic onwards, with DOM ranging from the Middle East to western Europe, CAS from Iran to southern China and Indonesia and MUS from the southern coastal region near the Caspian Sea through eastern Europe and northern Eurasia, including western and northern China, the Korean Peninsula and the Japanese Archipelago (e.g., Duplantier et al 2002; Bonhomme et al 2007; Suzuki et al 2013). Five distinct lineages of mitochondrial DNA (mtDNA) exist in M. musculus (Prager et al 1998; Sakuma et al 2016), three of which represent the three major subspecies groups of MUS, DOM and CAS and two of haplotypes from limited geographic areas in Nepal (Terashima et al 2006) and Yemen and Madagascar (Duplantier et al 2002), respectively. The three major subspecies lineages contain substantial levels of divergence within each of them

Methods

Results

Conclusion