Evolutionary dynamics of plant cell wall-degrading enzymes in weevils: A comparative study across Curculionoidea

Weevils of the superfamily Curculionoidea arguably represent the most diverse group of herbivorous beetles. Most of the 62,000 described species feed on live plants, some on rotten wood, and others on wood-decaying fungi. They include economically important pests like bark beetles (Scolytinae), grain weevils (Sitophilus spp.), and the boll weevil (Anthonomus grandis). Previous research suggests that enzymes breaking down plant cell wall polysaccharides may have influenced weevil diversification. However, our understanding of the distribution of plant cell wall-degrading enzymes (PCWDEs) and their evolution in Curculionoidea is limited to a few species, primarily within Curculionidae. Herein, using transcriptome and genome data, we analyzed PCWDE-encoding genes in 45 weevil species representative of the majority of families within Curculionoidea. Our investigation revealed the presence of 13 families of PCWDEs, including the description of putative endo-α-1,5-L-arabinanases from subfamily 6 of glycoside hydrolase family 43 (GH43_6) in animals for the first time. Different weevil species possessed varying numbers of PCWDE families, ranging from one to nine. Notably, species associated with wood-decaying fungi, including ambrosia beetles (Scolytinae), exhibited a reduced set of PCWDEs compared to closely related species that primarily feed on plants. Our study provides valuable insights into the distribution and diversity of PCWDEs within Curculionoidea, reinforcing the role played by horizontal gene transfer, gene duplication and gene loss in the evolution of these enzyme families.