Drosophila innubila has recently expanded its geographic range and shows high levels of gene flow between geographically isolated populations
To characterize how D. innubila came to inhabit its current range, we collected flies from four Sky island locations across Arizona: Chiricahuas (CH, 81 flies), Huachucas (HU, 48 flies), Prescott (PR, 84 flies) and Santa Ritas (SR, 67 flies) (Figure 1). Interestingly, previous surveys mostly failed to collect D. innubila north of the Madrean archipelago in Prescott (Dyer and Jaenike 2005). We easily sampled from that location, suggesting a possible recent invasion (though we were also unable to collect D. innubila in the exact locations previously sampled) (Dyer and Jaenike 2005). If this was a recent colonization event, it could be associated with the changing climate of the area leading to conditions more accommodating toD. innubila , despite over 300 kilometers of geographic isolation (Figure 1).
To determine when D. innubila established each population and rates of migration between locations, we isolated and sequenced the DNA from our sampled D. innubila populations and characterized genomic variation. We then examined the population structure and changes in demographic history of D. innubila using silent polymorphism in Structure (Falush et al. 2003) and StairwayPlot (Liu and Fu 2015). We find all sampled populations have a current estimated effective population size (Ne) of ~1,000,000 individuals and an ancestral Ne of ~4,000,000 individuals, though all experience a bottleneck about 100,000 years ago to an Neof 10,000-20,000 (Figure 1, Supplementary Figure 1A & B). This bottleneck coincides with a known glaciation period occurring in Arizona (Survey 2005). Each surveyed population then appears to go through separate population expansions between one and thirty thousand years ago, with populations settling from south to north (Figure 1A, Supplementary Figure 1A & B). Specifically, while the HU population appears to have settled first (10-30 thousand years ago), the PR population was settled much more recently (200-2000 years ago). This, in combination of the absence of D. innubila in PR until ~2016 sampling suggests recent northern expansion ofD. innubila (Figure 1). Also note that StairwayPlot (Liu and Fu 2015) has estimated large error windows for PR, meaning the invasion could be more recent or ancient than the 200-2000 year estimate.
Given the geographic isolation between populations, we expected to find a corresponding signature of population differentiation among the populations. Using Structure (Falush et al. 2003), we find surprisingly little population differentiation between locations for the nuclear genome (Supplementary Figure 1C) but some structure by location for the mitochondrial genome (Supplementary Figure 1D), consistent with previous findings (Dyer 2004; Dyer and Jaenike 2005). Together these suggest that there is still consistent gene flow between populations potentially via males.
Figure 1: A. Schematic of the range expansion of D. innubila and DiNV based on StairwayPlot results across the four sample locations in Arizona (AZ), Chiracahua’s (CH), Huachucas (HU), Prescott (PR) and Santa Ritas (SR). B and C. Summary of Structure/Fst results for B. autosomal polymorphism andC. mitochondrial polymorphism. Thickness of arrows inB and C indicates the median of FSTfor genes in each category, with 1 indicating completely isolated populations and 0 indicating complete gene flow. Light grey lines show the Arizona border.