Selection and demography shape genomic variation in a Sky Island species

Abstract

Over time, populations of species can expand, contract, fragment and become isolated, creating subpopulations that must adapt to local conditions. Understanding how species maintain variation after divergence as well as adapt to these changes in the face of gene flow, is of great interest, especially as the current climate crisis has caused range shifts and frequent migrations for many species. Here, we characterize how a mycophageous fly species, Drosophila innubila, came to inhabit and adapt to its current range which includes mountain forests in southwestern USA separated by large expanses of desert. Using population genomic data from more than 300 wild-caught individuals, we examine four populations to determine their population history in these mountain forests, looking for signatures of local adaptation. We find D. innubila spread northwards during the previous glaciation period (30-100 KYA), and has recently expanded even further (0.2-2 KYA). D. innubila shows little evidence of population structure, consistent with a recent establishment and genetic variation maintained since before geographic stratification. We also find some signatures of recent selective sweeps in chorion proteins and population differentiation in antifungal immune genes suggesting differences in the environments to which flies are adapting. However, we find little support for long-term recurrent selection in these genes. In contrast, we find evidence of long-term recurrent positive selection in immune pathways such as the Toll-signaling system and the Toll-regulated antimicrobial peptides.