The evolution and genomic basis of beetle diversity

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 symbiontindependent
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.