The evolution and genomic basis of beetle diversity

TLDR

Beetles are the most diverse animal group, yet their evolutionary history and the role of herbivory in their diversification remain poorly understood. The study proposes that horizontally transferred plant cell wall‑degrading enzymes enabled beetles to digest lignocellulose, driving the evolution of specialized plant‑feeding habits. The authors reconstructed beetle phylogeny with 4,818 genes across 146 species, estimated diversification timing with 89 genes across 521 species, and traced lignocellulose‑digestion genes using 154 genomes or transcriptomes. Phylogenomic analyses dated beetles to the Carboniferous, clarified relationships, and showed that horizontally transferred PCWDEs coincided with herbivory origins and diversification bursts, implying that these genes, along with codiversification with angiosperms and low extinction, drove the rise of nearly half of all beetle species.

Abstract

The order Coleoptera (beetles) is arguably the most speciose group of animals, but the evolutionary history of beetles, including the impacts of plant feeding (herbivory) on beetle diversification, remain poorly understood. We inferred the phylogeny of beetles using 4,818 genes for 146 species, estimated timing and rates of beetle diversification using 89 genes for 521 species representing all major lineages and traced the evolution of beetle genes enabling symbiont-independent digestion of lignocellulose using 154 genomes or transcriptomes. Phylogenomic analyses of these uniquely comprehensive datasets resolved previously controversial beetle relationships, dated the origin of Coleoptera to the Carboniferous, and supported the codiversification of beetles and angiosperms. Moreover, plant cell wall-degrading enzymes (PCWDEs) obtained from bacteria and fungi via horizontal gene transfers may have been key to the Mesozoic diversification of herbivorous beetles—remarkably, both major independent origins of specialized herbivory in beetles coincide with the first appearances of an arsenal of PCWDEs encoded in their genomes. Furthermore, corresponding (Jurassic) diversification rate increases suggest that these novel genes triggered adaptive radiations that resulted in nearly half of all living beetle species. We propose that PCWDEs enabled efficient digestion of plant tissues, including lignocellulose in cell walls, facilitating the evolution of uniquely specialized plant-feeding habits, such as leaf mining and stem and wood boring. Beetle diversity thus appears to have resulted from multiple factors, including low extinction rates over a long evolutionary history, codiversification with angiosperms, and adaptive radiations of specialized herbivorous beetles following convergent horizontal transfers of microbial genes encoding PCWDEs.