Five millennia of mitonuclear discordance in Atlantic bluefin tuna identified using ancient DNA

Abstract

Mitonuclear discordance between species is readily documented in marine fishes. Such discordance may either be the result of past natural phenomena or the result of recent introgression from previously seperated species after shifts in their spatial distributions. Using ancient DNA spanning five millennia, we here investigate the long-term presence of Pacific bluefin tuna (Thunnus orientalis) and albacore (Thunnus alalunga) -like mitochondrial (MT) genomes in Atlantic bluefin tuna (Thunnus thynnus), a species with extensive exploitation history and observed shifts in abundance and age structure. Comparing ancient (n = 130) and modern (n = 78) Atlantic bluefin MT genomes from most of its range, we detect no significant spatial or temporal population structure, which implies ongoing gene flow between populations and large effective population sizes over millennia. Moreover, we identify discordant MT haplotypes in ancient specimens up to 5000 years old and find that the frequency of these haplotypes has remained similar through time. We therefore conclude that MT discordance in the Atlantic bluefin tuna is not driven by recent introgression. Our observations provide oldest example of directly observed MT discordance in the marine environment, highlighting the utility of ancient DNA to obtain insights in the long-term persistence of such phenomena.