Hemipteran insects experience recurrent and synergistic molecular evolution adapting to diet shift

Hemiptera is an insect order with extremely high physiological and behavioral diversity. Feeding traits have switched and reversed multiple times, but the molecular basis governing this phenotypical change remains unclear.

We obtained the high-quality genomes and salivary gland transcriptomes of two essential biocontrol agents, Eocanthecona furcellata and Arma custos (Hemiptera: Heteroptera: Pentatomidae: Asopinae). This subfamily represents a typical insect clade with the reversal of feeding traits from phytophagy to zoophagy. Combined with public data of an additional 38 phylogenetically related insects and salivary gland transcriptomes of representative species, we performed a comprehensive analysis on the molecular evolution of feeding traits. We defined a set of diet-related gene groups and found that these genes were repetitively expanded in zoophagous species and experienced fast evolution and positive selection during diet reversal in the E. furcellata-A. custos clade. Transcriptomic analysis revealed dynamic upregulation of diet-related gene expression in zoophagous species, and further endeavor narrowed down the candidates to several genes, like trypsin and carboxypeptidase, which might be involved in diet reversal.

In conclusion, the evolution of zoophagy in Hemiptera and the reversal of feeding traits might require the synergistic regulations at both genomic and transcriptomic levels. Our study provides a potential connection between genotype and phenotype and advances the understanding of the adaptive evolution of zoophagous insects.