Evolution and genetic basis of the plant-penetrating ovipositor, a key adaptation in the transition to herbivory within the Drosophilidae
AbstractHerbivorous insects are extraordinarily diverse, yet are found in only one-third of insect orders. This skew may be driven by barriers to plant colonization coupled with phylogenetic constraint on plant-colonizing adaptations. Physical barriers can be surmounted by key innovations like the plant-penetrating ovipositor. Within Drosophilidae, ovipositor margins densely adorned with hard bristles used to cut into plants evolved repeatedly, but their evolutionary, developmental and genomic basis has only been explored in Drosophila suzukii. Here, we addressed this gap using Scaptomyza, an herbivorous radiation nested in a detritivorous clade. First, we found that ovipositor bristle number increased markedly as herbivory evolved in Scaptomyza. We then dissected the genomic architecture of variation in ovipositor bristle number within S. flava using a pooled genome wide association study (pool-GWAS). Variation in ovipositor bristle number in S. flava was heritable and associated with single nucleotide polymorphisms (SNPs) within non-coding regions involved in neural development. Genotyping of individual flies replicated the association at a candidate SNP upstream of Gai, a neural development gene, and estimated that it contributes to an average gain of ∼0.58 bristles/ovipositor in S. flava. Neural developmental genes thus underlie variation in this key morphological adaptation, possibly facilitating the evolution of this trait and the colonization of tough tissue of living plants.