Insular environment-dependent introgression from an arid-grassland orchid to a wetland orchid on an oceanic island

Abstract

Abstract Adaptive introgression plays a vital role in allowing recipient species to adapt and colonize new environments. However, our understanding of such environment-dependent introgressions is primarily limited to specific plant taxa in particular settings. In Japan, two related orchid species, the autonomously self-pollinating Pogonia minor and the outcrossing Pogonia japonica, typically inhabit dry grasslands and wetlands, respectively. Intriguingly, an island ecotype of P. japonica exists in arid, wind-swept, open sites on volcanic mountain slopes on Kozu Island, in the oceanic Izu Islands. To investigate potential introgression and its implications between P. japonica and P. minor on Kozu Island, we applied a comprehensive approach that included examining morphological traits, genome-wide SNP data, and plastid DNA sequences. We also examined the breeding systems of these species on Kozu Island through artificial pollination experiments to determine if introgression from P. minor has endowed the P. japonica ecotype with selfing capabilities. Extensive sampling on Kozu Island revealed that all P. japonica specimens exhibit signs of introgression from P. minor, suggesting the absence of pure P. japonica populations on the island. Furthermore, the chloroplast haplotypes of the insular P. japonica ecotype consistently match those of P. minor, indicating a predominantly asymmetrical initial hybridization with P. minor acting mainly as the maternal parent in the formation of F1 hybrids. Despite the advantages of self-fertilization in isolated environments, the insular P. japonica does not exhibit autogamy. Consequently, the scarcity of moist habitats, rather than selection pressure for selfing, likely contributes to the observed widespread introgression. Our study strongly suggests that the arid-environment-adapted P. minor has introgressed into the insular ecotype of P. japonica, enabling its successful colonization of arid volcanic mountain slopes of the oceanic island.