Phylogenomics reveals a gene flow history of reverse colonization

AimIslands have recently been recognized as potential sources of biodiversity, challenging the traditional view that their small population sizes and low genetic diversity limit such roles. This raises the question of how insular genetic variation becomes incorporated into continental populations, contrary to expectations of unidirectional colonization. Here, we investigate whether and how island-derived genetic variation has influenced a continental population through population establishment and gene flow in a bird species where frequent trans-ocean dispersal is expected. LocationContinental East Asia (Russian Far East), Japanese Archipelago TaxonSwinhoes Rail (Coturnicops exquisitus) Materials and MethodsWe apply integrative phylogenomics to reconstruct the spatiotemporal history of the species. Colonization sequences and gene flow are inferred by comparing four different phylogenetic reconstruction methods, using mitochondrial sequences obtained by Sanger sequencing and genome-wide data obtained by genotyping by sequencing (MIG-seq). We assess a history of colonization and gene flow based on summary statistics, demographic trajectory inference by Stairway Plot2, demographic modeling by fastsimcoal2, and species distribution modeling. ResultsAnalyses collectively supported asymmetric gene flow from the island to the continental population, following divergence around the Middle Pleistocene. Post-divergence, the island maintained a large and stable population, while the continental population underwent a severe bottleneck, suggesting a significant evolutionary role of the island for the continental population. Additionally, evidence of recent re-establishment of the island by continental individuals indicates dynamic exchange and persistence within a continent-island metapopulation. Main conclusionsThe maintenance of insular genetic variation within a dynamic continent-island metapopulation may have enabled the island to act as a genetic and demographic reservoir for the continental population. Thus, continent-island metapopulation dynamics may be a key evolutionary pathway through which island populations contribute to continental genetic diversity.