Phylogenomics reveals a gene flow history of reverse colonization

A microevolutionary theory assumes that small island populations are genetically depauperate and have difficulties in back-colonizing continents, becoming evolutionary dead-ends. This conventional view of islands as biodiversity sinks is, however, currently challenged by “reverse colonization,” a macroevolutionary phenomenon where a continental lineage originates and sometimes diversifies from island ancestors. It, therefore, remains elusive about the microevolutionary processes by which island populations become sources of continental biodiversity. We filled this gap by examining historical demography that contributed to the genetic variation of a continental population post-reverse colonization. We took advantage of the Swinhoe’s Rail that likely evolved through reverse colonization from the Japanese Archipelago to the Eurasian continent, challenging the expectation that insular rails are the representatives of “end-of-colonization” (e.g. flightlessness evolution). We reconstructed a dynamic demographic history of the Swinhoe’s Rail, including intraspecific gene flow, introgression, demographic trajectory, and historical distribution, by integrative phylogenomics using high-throughput sequencing and species distribution modeling. We revealed that a stable Japanese ancestral population, which was once established through colonization from Alaska, colonized the Eurasian continent, thereby confirming reverse colonization. Reverse colonization was characterized by repeated founding events along the archipelago that drastically decreased population size. However, the continental population retained unexpectedly high genetic variation. We unveiled a complex history of both intraspecific gene flow and introgression underlying reverse colonization. Particularly, we suggested that introgression from an American species to the continental population may have played a pivotal role in restoring genetic variation post-reverse colonization, potentially facilitating population persistence and expansion. In theory, increased genetic variation via introgression can lead to adaptive radiation and diversification by generating new combinations of alleles. Therefore, our findings encourage reinterpreting islands as “evolutionary turning points,” which facilitates an understanding of the processes that islands contribute to global biodiversity, thereby bridging a gap between micro-and macroevolution. Lay Summary Islands have long been viewed as biodiversity sinks based on a microevolutionary assumption that island populations are small and genetically depauperate, having difficulties in re-colonizing continents. This conventional view is, however, currently challenged by “reverse colonization,” a macroevolutionary phenomenon where a continental lineage originates from islands. This contradiction, therefore, raises an important question about how and what demographic histories of island populations heighten genetic variation and thereby allow successful reverse colonization. Here we address this question by focusing on a rail species that likely experienced reverse colonization from Japan to the Eurasian continent, despite the expectation that many island rails have small population sizes and experience island-specific evolution, leading to “evolutionary dead-ends. ” Our integrative phylogenomics supported the continental population originating from an island lineage, confirming reverse colonization. We unveiled a complex history of both intraspecific gene flow and introgression associated with reverse colonization. Particularly, we suggested that introgression may have played a pivotal role in restoring genetic variation and continental population expansion post-reverse colonization. In theory, introgression assists adaptive radiation and diversification by rapidly introducing novel genetic variation. Thus, our findings shed light on how islands contribute to global biodiversity, thereby bridging a gap between micro-and macroevolution.