Direct and indirect impacts of positive selection on genomic variation in Drosophila serrata

Abstract

Understanding the extent to which microevolutionary adaptation relies on novel beneficial mutations, as opposed to previously neutral standing genetic variation, is an important goal of evolutionary genetics. Progress towards this goal has been enhanced during the genomic era through the study of selective sweeps. Selective sweeps fall into two categories: hard sweeps via new mutations and soft sweeps via pre-existing mutations. However, data are currently lacking on the relative frequency of these two types of selective sweep. In this study, we examined 110 whole genome sequences from Drosophila serrata sampled from eastern Australia and searched for hard and soft sweeps using a deep learning algorithm (diploS/HIC). Analyses revealed that approximately 15% of the D. serrata genome was directly impacted by soft sweeps, and that 46% of the genome was indirectly influenced via linkage to these soft sweeps. In contrast, hard sweep signatures were very rare, only accounting for 0.1% of the scanned genome. Gene ontology enrichment analysis further supported our confidence in the accuracy of sweep detection as several traits expected to be under frequent selection due to evolutionary arms races (e.g. immunity and sperm competition) were detected. Within soft sweep regions and those flanking them, there was an over-representation of SNPs with predicted deleterious effects, suggesting positive selection drags deleterious variants to higher frequency due to their linkage with beneficial loci. This study provides insight into the direct and indirect contributions of positive selection in shaping genomic variation in natural populations.

Signatures of Adaptation, Constraints, and Potential Redundancy in the Canonical Immune Genes of a Key Pollinator

“…Although we may expect genes involved in intracellular signaling to evolve under purifying selection in order to maintain function, selection acting on genes coding for receptors of the Toll signaling cascade may allow for adaptation to novel or re-emergent threats. Consequently, initiators and ligands of the Toll pathway, such as CLIP serine proteases and spätzle proteins, have been previously reported to have accelerated rates of evolution at the macroevolutionary scale across Apis and Bombus species ( Barribeau et al 2015 ) as well as in Drosophila species ( Jiggins and Kim 2007 ; Levin and Malik 2017 ; Wang et al 2022 ), highlighting the importance of such genes to contribute to the immune response. Our results support previous findings of positive selection acting on initiators and receptors of these pathways suggestive that such genes may help bumblebees cope with pathogens in their natural landscape.…”

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

“…The fact that we did not find signatures of selective sweeps using SFS-based methods in most candidate outlier regions may be another indication of polygenic adaptation, known to be more detectable with pairwise tests for allelic differentiation (Stölting et al 2015;Schneider et al 2021). This result, together with the absence of a significant reduction of genetic diversity in outlier regions, may also suggest that those candidate regions are more likely subject to soft sweeps than hard sweeps (Pritchard et al 2010;Wang et al 2022). The two types of outlier genes (C2_max and C2_mean) may here not reflect different selection regimes but just different variant architectures within outlier genes.…”

Divergence of olfactory receptors associated with the evolution of assortative mating and reproductive isolation in mice

“…The fact that we did not find signatures of selective sweeps using SFS-based methods in most candidate outlier regions may be another indication of polygenic adaptation, known to be more detectable with pairwise tests for allelic differentiation (Stölting et al 2015; Schneider et al 2021). This result may also suggest that those candidate regions are more likely subject to soft sweeps than hard sweeps (Wang et al unpublished data). Since outlier gene regions are not associated with regions of reduced genetic diversity or reduced recombination rate, a general effect of background selection inflating the levels of genetic differentiation in our data seems unlikely.…”

“…The fact that we did not find signatures of selective sweeps using SFS-based methods in most candidate outlier regions may be another indication of polygenic adaptation, known to be more detectable with pairwise tests for allelic differentiation (Stölting et al 2015; Schneider et al 2021). This result, together with the absence of a significant reduction of genetic diversity in outlier regions, may also suggest that those candidate regions are more likely subject to soft sweeps than hard sweeps (Pritchard et al 2010; Wang et al 2022). The two types of outlier genes ( C 2 _max and C 2 _mean ) may here not reflect different selection regimes but just different variant architectures within outlier genes.…”