Adaptation, ancestral variation and gene flow in a ‘Sky Island’Drosophilaspecies

Abstract

1Over time, populations of species can expand, contract, and become isolated, creating subpopulations that 2 can adapt to local conditions. Understanding how species adapt following these changes is of great interest, 3 especially as the current climate crisis has caused range shifts for many species. Here, we characterize how 4 Drosophila innubila came to inhabit and adapt to its current range: mountain forests in southwestern USA 5 separated by large expanses of desert. Using population genomic data from more than 300 wild-caught 6 individuals, we examine four distinct populations to determine their population history in these mountain-7 forests, looking for signatures of local adaptation to establish a genomic model for this spatially-distributed 8 system with a well understood ecology. We find D. innubila spread northwards during the previous 9 glaciation period (30-100 KYA), and has recently expanded even further (0.2-2 KYA). Surprisingly, D. 10 innubila shows little evidence of population structure, though consistent with a recent migration, we find 11 signatures of a population contraction following this migration, and signatures of recent local adaptation 12 and selective sweeps in cuticle development and antifungal immunity. However, we find little support for 13 recurrent selection in these genes suggesting recent local adaptation. In contrast, we find evidence of 14 recurrent positive selection in the Toll-signaling system and the Toll-regulated antimicrobial peptides. 15 65 evolutionary change and this is particularly interesting regarding the coevolution with pathogens (DYER 66 AND JAENIKE 2005; UNCKLESS 2011a). We also wanted to understand how D. innubila adapt to their local 67

Rapid evolution and horizontal gene transfer in the genome of a male-killingWolbachia

“…The w Inn samples are highly structured based on both the total and synonymous variation (Figure 4). Using a principle component analysis, we find three clear clusters, separating the Chiricahua and Prescott populations, and grouping the Santa Rita and the Huachuca populations together (Figure 4), as seen with the mitochondrial genome and consistent with previous findings (J aenike et al 2003; D yer and J aenike 2005; J aenike and D yer 2008; H ill and U nckless 2020a). This suggests that females are not moving between locations or at least not reproducing after moving, creating structure in the populations of this maternally inherited endosymbiont (J aenike et al 2003).…”

“…To that end, we examined the genome and population genomic variation in w Inn. In a previous survey we collected wild D. innubila from four geographically isolated mountain locations and tested strains for Wolbachia using PCR to amplify wsp primers and found 48 lines infected with Wolbachia (Supplementary Table 1, 13 from the Chiricahua mountains, 27 from Prescott, 2 from the Huachucas, and 6 from the Santa Ritas) (H ill and U nckless 2020b; H ill and U nckless 2020a).…”

“…We collected wild Drosophila at four mountainous locations across Arizona between the 22nd of August and the 11th of September 2017 (H ill and U nckless 2020b; H ill and U nckless 2020a). Specifically, we collected at the Southwest research station in the Chiricahua mountains (31.871 latitude, −109.237 longitude), Prescott National Forest (34.540 latitude, −112.469 longitude), Madera Canyon in the Santa Rita mountains (31.729 latitude, −110.881 longitude) and Miller Peak in the Huachuca mountains (31.632 latitude, −110.340 longitude).…”

“…We further analyzed the 343 putative D. innubila flies which we homogenized and extracted DNA from using the Qiagen Gentra Puregene Tissue kit (USA Qiagen Inc., Germantown, MD, USA) (H ill and U nckless 2020b; H ill and U nckless 2020a). We tested these samples for infection using Wolbachia primers specific to the Wolbachia surface protein ( wsp ) gene alongside a positive and negative control (Z hou et al 1998).…”

“…For the 48 Wolbachia -infected lines we previously extracted DNA and sequenced the host and Wolbachia genomes on two runs of an Illumina HiSeq 4000 (150 bp paired-end (H ill and U nckless 2020a; H ill and U nckless 2020b), Illumina, San Diego, CA), producing an average of 20,618,752 reads per sample, of which an average of 436,527 mapped to Wolbachia per sample, as summarized in Supplementary Table 1.…”