The genetics of host plant acceptance in pea aphids

The evolution of host-associated sympatric populations in phytophagous insects (so called “host races”) connects adaptive divergence to barriers to gene flow. Pea aphid (Acyrthosiphon pisum) host races specialise on legume species, and because host plant choice leads to assortative mating, the genetic basis of host plant acceptance is key to understanding speciation. Aphids use smell and taste in their host plant selection. While chemosensory genes frequently emerge as “outliers” in genome scans, their link to plant acceptance behaviour remains unclear. We examined the genetic basis of host-associated phenotypes using an F2 cross between two pea aphid host-associated races (specialised on alfalfa—Medicago sativa- and pea—Pisum sativum), assaying behaviour on both host plants and conducting QTL and regional heritability analyses based on a high-resolution linkage map. We identified five regions of moderate effect associated with acceptance of alfalfa, two with pea acceptance and two with survival on alfalfa. Two QTLs, one for alfalfa and one for pea acceptance, are located within a large rearranged region on chromosome 1, while other QTLs linked to alfalfa acceptance and survival are in the same region on chromosome 3—linking host plant choice to fitness. These findings highlight the polygenic basis of acceptance behaviour and the role of gene clustering and chromosomal rearrangements in promoting coupling among barrier loci. We identified 60 chemosensory genes within regions connected to acceptance, 24 of which were divergent among pea aphid races in previous genome scan or gene expression analyses. Evidence linking these genes to acceptance phenotypes supports their role in determining host plant specificity and as barrier loci contributing to pea aphid speciation.