Genomic Insights into the Evolution of Parental Care in Weevils

Abstract

Parental care, a key step in the evolution of sociality, has evolved multiple times in insects, yet the molecular mechanisms underlying its emergence remain poorly understood. Weevils (Curculionidae) exhibit diverse parental care behaviours, from nest building to egg and larval attendance, making them an ideal system to investigate genomic changes associated with subsociality. We analysed 13 high-quality weevil genomes, encompassing independent origins of egg and larval attendance, to test two predictions: (1) the sheltering hypothesis, where parental care relaxes selection on traits critical for independent larval survival, and (2) the regulatory hypothesis, where behavioural shifts are driven by changes in transcriptional regulation. Gene family evolution analyses revealed significantly more convergent contractions, particularly in genes linked to transcriptional regulation and enzymatic activity, on branches where larval attendance evolved, consistent with functional gene loss under relaxed selection. Selection analyses identified over 400 genes under relaxed selection, especially those associated with transcriptional regulation and neural plasticity, further supporting hypothesis 1. In contrast, positive selection and intensified selection were rare but enriched for genes regulating gene expression, consistent with hypothesis 2. Together, these results suggest that parental care in weevils drives both simplification of larval traits through relaxed selection and convergent gene loss, and innovation in caregiving behaviours via adaptive changes in gene regulation. Significance statementParental care is a pivotal evolutionary innovation, yet its genetic basis in insects remains underexplored. By comparing genomes from weevil species with and without care behaviours, we reveal two key processes shaping the emergence of subsociality: relaxation of selection on genes linked to larval independence and adaptive evolution in genes regulating gene expression. This combination likely reflects reduced demands on protected larvae alongside fine-tuning of parental behaviours. Our findings highlight how simple social systems can evolve through both loss and innovation, offering a comparative framework for understanding social evolution across insects.