A Whole-Genome Scan for Association with Invasion Success in the Fruit Fly Drosophila suzukii Using Contrasts of Allele Frequencies Corrected for Population Structure

Abstract

Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here, we characterized the genome response of the spotted wing drosophila Drosophila suzukii during the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we called C2, that contrasts allele frequencies corrected for population structure. We evaluated this new statistical framework using simulated data sets and implemented it in an upgraded version of the program BayPass. We identified a relatively small set of single-nucleotide polymorphisms that show a highly significant association with the invasive status of D. suzukii populations. In particular, two genes, RhoGEF64C and cpo, contained single-nucleotide polymorphisms significantly associated with the invasive status in the two separate main invasion routes of D. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by nonequilibrium demographic conditions for which binary covariables of interest can be defined at the population level.

The worldwide invasion ofDrosophila suzukiiis accompanied by a large increase of transposable element load and a small number of putatively adaptive insertions

“…insertions. This may be due to overall large effective population sizes as suggested in (Olazcuaga et al 2020), but also to the fact that Tajima's D is unlikely to detect soft selective sweep, i.e. adaptation from standing variation or multiple successive beneficial mutations (Pennings and Hermisson 2006) it is probably the insertion itself rather than the absence that might be adaptive.…”

“…To evaluate the effect of genetic variation on TE abundance we performed a genome-wide scan for association using methods controlling for population structure. To that end we relied on the 13,530,656 bi-allelic variants (mostly SNPs) previously described on the same data set (Olazcuaga et al 2020)…”

“…We investigated the presence of putatively adaptive insertions using a genome scan combining three methods controlling for population structure implemented in BayPass (Olazcuaga et al 2020). First, we assessed overall differentiation (based on the XtX statistics).…”

“…Third, it may be due to differences in the methodology used for the two species. Our analysis relies essentially on the research of overly differentiated TEs across populations with a correction for population structure (Gautier 2015;Olazcuaga et al 2020), whereas in the analysis used for D.…”

Near-chromosome level genome assembly of the fruit pest Drosophila suzukii using long-read sequencing

“…The raw paired-end sequences (2 × 150) were made available from the SRA repository under the SRR10260310 accession. Finally, for the US-Wat, the US-Haw and the CN-Nin populations, we relied on the Pool-seq data recently produced by 68 from samples of 50 individuals (including 4, 25 and 36 females, respectively) and available from the SRA under the SRR10260026, SRR10260031 and SRR10260027 accessions respectively. The three data sets consisted of 2 × 125 bp PE sequences obtained from a HiSeq 2500 sequencer.…”