Targeted re‐sequencing confirms the importance of chemosensory genes in aphid host race differentiation

Abstract

Host-associated races of phytophagous insects provide a model for understanding how adaptation to a new environment can lead to reproductive isolation and speciation, ultimately enabling us to connect barriers to gene flow to adaptive causes of divergence. The pea aphid (Acyrthosiphon pisum) comprises host races specializing on legume species and provides a unique system for examining the early stages of diversification along a gradient of genetic and associated adaptive divergence. As host choice produces assortative mating, understanding the underlying mechanisms of choice will contribute directly to understanding of speciation. As host choice in the pea aphid is likely mediated by smell and taste, we use capture sequencing and SNP genotyping to test for the role of chemosensory genes in the divergence between eight host plant species across the continuum of differentiation and sampled at multiple locations across western Europe. We show high differentiation of chemosensory loci relative to control loci in a broad set of pea aphid races and localities, using a modelfree approach based on principal component analysis. Olfactory and gustatory receptors form the majority of highly differentiated genes and include loci that were already identified as outliers in a previous study focusing on the three most closely related host races. Consistent indications that chemosensory genes may be good candidates for local adaptation and barriers to gene flow in the pea aphid open the way to further investigations aiming to understand their impact on gene flow and to determine their precise functions in response to host plant metabolites.

Intrinsic incompatibilities evolving as a by‐product of divergent ecological selection: Considering them in empirical studies on divergence with gene flow

“…There are also specific examples of highly pleiotropic or connected genes involved in divergence. For example, in contrast to the expectations of strong purifying selection and conservation, the highly pleiotropic gene Vitellogenin has been shown to experience bouts of recent selection between different honey bee races (Kent, Issa, Bunting, & Zayed, ), and chemosensory genes, which bind a wide range of chemicals, have been suggested to play a role in local adaptation to different host plants in pea aphids (Eyres et al., ; Smadja et al., ).…”

Identifying genomic hotspots of differentiation and candidate genes involved in the adaptive divergence of pea aphid host races

“…Because we restricted our analysis to three host races, we could not properly identify repeated or parallel cases of adaptation within the pea aphid complex. Some targets of selection may be shared between biotypes as reported in earlier studies (Eyres et al., ; Nouhaud et al., ; Smadja et al., ), but it is still unclear to what extent adaptation to different host plants would rely on the same loci, through the parallel reuse of standing variation (Ravinet et al., ). Moreover, the pea aphid radiation is recent (Peccoud, Simon et al., ) and host races considered in this study still experience gene flow, making it possible for a variant under selection to invade all of them, resulting in a global selective sweep (Bierne, ).…”

Molecular mechanisms of adaptation and speciation: why do we need an integrative approach?

“…() performed F ST and π a /π s tests on a set of 153 candidate genes potentially underlying pea aphid speciation and found 19 genes showing increased divergence across three populations; a larger set of genes and aphid populations has confirmed and expanded on this work (Eyres et al . in this issue). Functionally testing each individual gene is costly and time‐consuming, yet it is only by assessing the function of the most promising individual genes that we can make firm conclusions about their contribution to adaptation and the physical properties that favoured specific variants (Harms & Thornton ).…”