A cosmopolitan inversion drives seasonal adaptation in overwinteringDrosophila

Abstract

Drosophila melanogasterliving in temperate regions evolve as they track seasonal fluctuations. Yet, we lack an understanding of the genetic architecture of seasonal adaptive tracking. By sequencing orchard populations collected across multiple years, we characterized the genomic signal of seasonal demography and identified that the cosmopolitan inversion In(2L)t drives seasonal adaptation. In(2L)t shows footprints of selection that are inconsistent with simple explanations of genetic drift, as well as signatures of partial selective sweeps. A meta-analysis of phenotypic studies shows that seasonal loci within In(2L)t are associated with behavior, life-history, physiology, and morphology traits. Our results identify candidate regions that underlie seasonal adaptive tracking and link them to phenotype. This work supports the general hypothesis that inversions are important drivers of rapid adaptation.

Geographic and seasonal variation of theforgene reveal signatures of local adaptation inDrosophila melanogaster

“…In hopes of mitigating this issue, I filtered out the reads with an effective coverage (N ef f ) lower than 28 in this study. I applied this filter based on a previous work that used some of the samples included in this analysis (Nunez et al, 2022). This study suggested that the use of samples with N ef f < 28 created outliers in a principal component analysis driven by N ef f , but samples with N ef f > 28 no longer generated atypical observations.…”

“…Because the filtering process drastically reduced the number of individuals (pools) in a few populations, I grouped together populations from the nearest neighbor localities to ensure a minimum sample size of 5. I also applied a minimum effective coverage N ef f filter of 28 to avoid the influence of atypical observations driven by samples with low coverage (Nunez et al, 2022). The DEST dataset provides the coordinates of each collection site, enabling one to obtain data about the seasonality of temperature and precipitation.…”

“…To avoid the influence of atypical observations driven by samples with low coverage, I applied a minimum effective coverage N ef f filter of 28 (e.g., Nunez et al, 2022). I also removed pools and SNP loci with more than 20% missing genotypes.…”

Population genetic simulation: Benchmarking frameworks for non‐standard models of natural selection

“…For all simulations, a 1 megabase (Mb) chromosomal region was simulated, with evolutionary and population genetic parameters reflecting those of a wild Drosophila melanogaster population. D. melanogaster was chosen because Drosophilids have been the focal taxon of research into the population genetics of many different types of selection (Sella et al., 2009), including temporally fluctuating selection (Behrman & Schmidt, 2022; Machado et al., 2021; Nunez et al., 2022; Rudman et al., 2022; Wittmann et al., 2017), a form of selection that displays complex dynamics not easily implemented using standard population genetic simulation software. As D. melanogaster has a very large estimated effective population size ( N e ), on the order of 1 million individuals (Sprengelmeyer et al., 2020), population parameters were downscaled in the simulations, and recombination rate ( r ) and mutation rate ( μ ) parameters proportionately upscaled.…”

Complex genomic landscape of inversion polymorphism in Europe’s most destructive forest pest

“…Importantly, polymorphic inversions are a reservoir of genetic variation that can facilitate adaptation to rapidly changing environments. Indeed, several studies have shown that polymorphic inversions support rapid adaptation to changing climatic conditions (Rane et al 2015;Kapun and Flatt 2019;McCulloch and Waters 2023) or adaptive tracking of fluctuating environments (Nunez et al 2023). Spruce bark beetle populations are subject to seasonal weather changes and a rapidly changing environment due to strong anthropogenic pressures (Hofmann et al 2024).…”