Adaptation, ancestral variation and gene flow in a 'Sky Island' Drosophila species

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 south-western 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. In this first extensive study, establishing D. innubila as a key genomic Sky Island model, we find D. innubila spread northwards during the previous glaciation period (30-100 KYA) and have 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 signalling system and the Toll-regulated antimicrobial peptides.

Automated summary

The study characterizes how a mycophageous fly species, Drosophila innubila, adapts to its current range in mountain forests in the south-western USA, using population genomic data from over 300 wild-caught individuals. The research reveals evidence of migration, recent expansion, and genetic variation in D. innubila, as well as different adaptation strategies in chorion proteins and immune genes. Additionally, the study shows long-term recurrent positive selection in immune pathways such as the Toll signaling system and antimicrobial peptides.