The history of ancient Japanese dogs revealed by mitogenomes

Abstract

Archaeological evidence indicates that dogs appeared in Japan at least 9300 years ago, during the Jomon period. The Jomon period dogs (Jomon dogs) retained the morphological characteristics of ancient domestic dogs throughout the Jomon period, possibly due to their geographical isolation from continental dogs. Therefore, we expect them to retain the genetic characteristics of ancient domestic dogs. To explore this possibility, we determined the mitochondrial genomes of five Jomon dogs, including one of the oldest dogs in Japan (7400-7200 cal BP), and seven late-8th-century Japanese dogs (Suwada dogs). We analyzed these sequences with 719 mitochondrial genomes of ancient and modern canids. The dog mitochondrial DNA (mtDNA) sequences have been grouped into six clades (haplogroups A-F), and clade A comprises six sub-clades (sub-haplogroups A1-A6). Classification of the Jomon dogs' mtDNA haplotypes revealed that these dogs belong to a nested A2/A3 sub-haplogroup not shared by other modern or ancient samples. The mtDNA sequences of Jomon dogs form a monophyletic clade which is sister to the A3 sub-clade in the phylogenetic trees. Network analysis showed that the Jomon dogs' mtDNA sub-clade diverged close to the base of the A2 and A3 haplotype network, which was centered by an ancient dog from South China. The Jomon dog mtDNAs diverged from A3 (~11500 years ago) soon after the A2 and A3 divergence (~12800 years ago), indicating early divergence of the Jomon dogs' sub-clade. These results suggest that the Jomon dogs were possibly introduced into the Japanese archipelago 11500-9300 years ago. The mtDNAs of late-8th-century dogs were more diverse and were different haplogroups than that of Jomon dogs, suggesting that other haplogroups likely replaced the haplogroup of Jomon dogs through the introduction of dogs that accompanied the migration of people into Japan in later periods.