Evolutionary dynamics of plant cell wall-degrading enzymes reflects feeding ecology in weevils.

Abstract

Many herbivorous beetles depend on plant cell wall-degrading enzymes (PCWDEs) to access the nutritious plant cell content. However, the evolution of PCWDEs in weevils, the most diverse lineage of herbivores, remains poorly understood. Using transcriptomic and genomic analyses of 45 weevil species spanning the majority of existing subfamilies, we identified a total of 13 different PCWDE families, revealing high variability between species. Interestingly, the PCWDE repertoires tracked dietary specialization, with convergent reductions in fungivorous taxa. Furthermore, PCWDE gene family dynamics were driven by both larval and adult specialized herbivory on different plant organs. Despite this complex evolutionary history, phylogenetic analyses place core PCWDE functionalities at the base of the Phytophaga (weevils, leaf beetles, and longhorn beetles) and reveal subsequent horizontal gene transfer (HGT) events from various donors during early Phytophaga diversification. These findings demonstrate that HGTs, gene duplications, and losses shaped PCWDE diversity and facilitated the ecological success of weevils.