Phylogenomics reveals an island as a genetic reservoir of a continental population

Abstract

AimIslands can become sources of continental biodiversity through reverse colonization. This is contradicted by the classic view of islands as sinks, because microevolution predicts difficulties in continental colonization by small island populations that are genetically depauperate. We fill this gap by examining historical demography that contributed to genetic variation of a continental population after reverse colonization. We exploit a rail species that likely evolved through reverse colonization, challenging the expectation that rails are the representatives of “end-of-colonization” on islands.LocationContinental East Asia (Russian Far East), Japanese ArchipelagoTaxaSwinhoe’s Rail (Coturnicops exquisitus)MethodsTo confirm reverse colonization, therein a continental population is derived from an island lineage, we reconstruct a complex phylogenetic relationship considering gene flow and introgression. We apply multiple methods using both high-throughput sequencing and mitochondrial datasets. We reconstruct a comprehensive demographic history of the species based on historical trajectory inference by Stairway Plot 2, fastsimcoal2 demographic modeling, and species distribution modeling. We assess genetic variation of the continental population and the key demographic process underlying them.ResultsThe continental population is inferred as a derived group within an island lineage, supporting reverse colonization. Demographic reconstruction suggests a significant population size decline through reverse colonization, with intraspecific gene flow from the island population. Introgression from an American sister species into the continental population is supported, which may be responsible for the unexpectedly high genetic variation observed.Main conclusionsUsing phylogenomics, we reconstruct reverse colonization associated with a complex history of population size changes and gene flow. Introgression, particularly, plays a pivotal role in rapidly restoring advantageous genetic variation for persistence and expansion on the continent post-reverse colonization. In theory, introgression assists adaptive radiation and diversification. Thus, our findings facilitate an understanding of the processes that islands contribute to global biodiversity, thereby bridging a gap between micro- and macroevolution.