Genomic signatures associated with the evolutionary loss of egg yolk in parasitoid wasps

Abstract

AbstractTrait regression and loss have occurred repeatedly in numerous lineages throughout evolutionary history in response to changing environments. In parasitoid wasps, a mega-diverse group of hymenopteran insects, loss or reduction of yolk in the egg has been reported in many species. This phenotypic change likely evolved as a response to the shift from ectoparasitism to endoparasitism. However, the genetic basis of this trait and the impact of its loss on genome evolution remain poorly understood. Here, we performed a comparative genomic analysis of 64 hymenopteran insects. The conserved insect yolk protein genevitellogenin(Vg) underwent five independent loss events in four families, involving 23 of the analyzed endoparasitoid species. Whole-genome alignment suggested thatVgloss occurred during genome rearrangement events. Analysis ofVgreceptor gene (VgR) loss, selection, and structural variation in lineages lackingVgdemonstrated functional biases in the patterns of gene loss. The ectoparasitism to endoparasitism transition did not appear to be the primary driver ofVgloss or the subsequentVgRevolution. A number of parallel and convergent genomic changes were observed betweenVg-loss lineages, including gene family evolution and selection of genes related to transport, development, and metabolism. These changes may have facilitated embryonic development without the yolk in these lineages. Together, these findings reveal the genomic basis underlying a unique trait loss in parasitoid wasps. More broadly, this study enhances our understanding of yolk loss evolution outside the class Mammalia, highlighting a potential evolutionary trend arising from the availability of an alternative nutrient source for embryonic development.