Evolution of five environmentally responsive gene families in a pine-feeding sawfly, Neodiprion lecontei (Hymenoptera: Diprionidae)

A central goal in evolutionary biology is to determine the predictability of adaptive genetic changes. Despite many documented cases of convergent evolution at individual loci, little is known about the repeatability of gene family expansions and contractions. To address this void, we examined gene family evolution in the redheaded pine sawfly Neodiprion lecontei, a noneusocial hymenopteran and exemplar of a pine-specialized lineage evolved from angiosperm-feeding ancestors. After assembling and annotating a draft genome, we manually annotated multiple gene families with chemosensory, detoxification, or immunity functions before characterizing their genomic distributions and molecular evolution. We find evidence of recent expansions of bitter gustatory receptor, clan 3 cytochrome P450, olfactory receptor, and antimicrobial peptide subfamilies, with strong evidence of positive selection among paralogs in a clade of gustatory receptors possibly involved in the detection of bitter compounds. In contrast, these gene families had little evidence of recent contraction via pseudogenization. Overall, our results are consistent with the hypothesis that in response to novel selection pressures, gene families that mediate ecological interactions may expand and contract predictably. Testing this hypothesis will require the comparative analysis of high-quality annotation data from phylogenetically and ecologically diverse insect species and functionally diverse gene families. To this end, increasing sampling in under-sampled hymenopteran lineages and environmentally responsive gene families and standardizing manual annotation methods should be prioritized.

Automated summary

This study investigates the evolution of gene families in the redheaded pine sawfly and finds evidence that gene families may expand and contract predictably in response to new selection pressures. These findings are important for understanding the predictability of gene family evolution in ecological adaptations.