Sociality in weevils is shaped by sheltering and convergent gene losses
Listed in
This article is not in any list yet, why not save it to one of your lists.Abstract
Eusociality, characterized by overlapping generations, cooperative brood care, and reproductive division of labour, has arisen independently across diverse, phylogenetically distant insect orders, including Hymenoptera (ants, bees, and wasps), Blattodea (termites), and Coleoptera (weevils). While multiple studies have investigated the molecular evolution of sociality from solitary ancestors in Hymenoptera and Blattodea, so far little is known about the evolutionary signatures of social evolution in Coleoptera. Weevils (Curculionidae) provide an ideal system for addressing this question, as they cover the full spectrum of social complexity from parental care, through several origins of facultative eusociality to the only obligately eusocial beetle, Austroplatypus incompertus . We generated genome assemblies for A. incompertus and two facultatively eusocial weevil species, Xylosandrus germanus and Xyleborinus saxesenii , which together with 18 publicly available weevil genomes span two independent evolutionary origins of sociality. Our analyses reveal a genome-wide relaxation of purifying selection with increasing social complexity, which is most pronounced in A. incompertus . We find a significant excess of convergent gene family contractions in lineages where sociality evolved, and no evidence of elevated positive selection. These findings indicate that the molecular mechanisms of social evolution in weevils are primarily characterised by relaxed selection and gene loss, rather than adaptive innovation and gene family expansions. These observations are consistent with sheltering and reduced effective population size playing an important role, a pattern not previously observed in other clades.
Significance statement
Eusociality has evolved independently multiple times across the insect tree of life, yet the genomic mechanisms underlying these transitions remain poorly understood outside of Hymenoptera and termites. By generating genomes for Austroplatypus incompertus , the sole obligately eusocial beetle, and closely related facultatively eusocial weevil species, we construct a comprehensive genomic dataset spanning the full spectrum of social complexity within a single family. Genome-wide relaxation of purifying selection accompanies increasing social complexity in weevils, consistent with patterns documented in other social insects. Interestingly, instead of positive selection and gene family expansions, the main genomic signature is one of convergent gene family contractions. These findings demonstrate that the genomic routes to eusociality are more diverse than previously appreciated.
