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

Trait regression and loss have occurred repeatedly in numerous lineages in response to environmental changes. In parasitoid wasps, a megadiverse group of hymenopteran insects, yolk protein reduction or loss has been observed in many species, likely linked to the transition 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 gene vitellogenin (Vg) underwent five independent loss events in four families, involving 23 of the analyzed endoparasitoid species. Whole-genome alignment suggested that Vg loss occurred during genome rearrangement events. Analysis of Vg receptor gene (VgR) loss, selection, and structural variation in lineages lacking Vg demonstrated functional biases in the patterns of gene loss. The ectoparasitism to endoparasitism transition did not appear to be the primary driver of Vg loss or the subsequent VgR evolution. Together, these findings reveal the genomic changes underlying a unique trait loss in parasitoid wasps. More broadly, this study enhances our understanding of yolk protein loss evolution outside the class Mammalia, highlighting a potential evolutionary trend arising from the availability of an alternative nutrient source for embryonic development.