The evolution and genomic basis of beetle diversity

Authors: MCKENNA, DUANE - University Of Memphis; SHIN, SEUNGGWAN - University Of Memphis; AHRENS, DIRK - Zoological Research Museum Alexnder Koenig; BALKE, MICHAEL - Bavarian State Collection For Zoology; BEZA-BEZA, CRISTIAN - University Of Memphis; CLARKE, DAVE - University Of Memphis; DONATH, ALEX - Zoological Research Museum Alexnder Koenig; ESCALONA, HERMES - Commonwealth Scientific And Industrial Research Organisation (CSIRO); FRIEDRICH, FRANK - Universitat Hamburg; LETSCH, HARALD - University Of Vienna; LUI, SHANLIN - China National Genebank; MADDISON, DAVID - Oregon State University; MAYER, CHRISTOPH - Zoological Research Museum Alexnder Koenig; MISOF, BERNHARD - Zoological Research Museum Alexnder Koenig; MURIN, PEYTON - University Of Memphis; NIEHUIS, OLIVER - University Of Freiburg; PETERS, RALPH - Zoological Research Museum Alexnder Koenig; PODSIADLOWSKI, LARS - Zoological Research Museum Alexnder Koenig; POHL, HANS - Friedrick-Schiller University; Scully, Erin; YAN, EVGENY - Russian Academy Of Sciences; ZHOU, XIN - China Agricultural University; SLIPINSKI, ADAM - Commonwealth Scientific And Industrial Research Organisation (CSIRO); BEUTEL, ROLF - Friedrick-Schiller University

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/15/2019
Publication Date: 12/16/2019
Citation: McKenna, D.D., Shin, S., Ahrens, D., Balke, M., Beza-Beza, C., Clarke, D.J., Donath, A., Escalona, H.E., Friedrich, F., Letsch, H., Lui, S., Maddison, D., Mayer, C., Misof, B., Murin, P.J., Niehuis, O., Peters, R., Podsiadlowski, L., Pohl, H., Scully, E.D., Yan, E.V., Zhou, X., Slipinski, A., Beutel, R.G. 2019. The evolution and genomic basis of beetle diversity. Proceedings of the National Academy of Sciences. 116(49):24729-24737. https://doi.org/10.1073/pnas.1909655116.
DOI: https://doi.org/10.1073/pnas.1909655116

Interpretive Summary: Herbivorous beetles represent a diverse and prominent group that exploits various plant tissues as their primary diet. Plant tissues are inherently difficult to digest and require specialized enzymes for efficient nutrient extraction, but several enzymes have been identified in insects that serve these purposes. The prominence of these enzymes in herbivorous beetles and the evolutionary origin of these genes that encode these enzymes have remained largely uncharacterized, but may have contributed to the diversity of herbivorous diets in beetles. Here, we reconstruct the evolutionary history of 521 different species of beetles and reveal that plant cell wall degrading enzymes (PCWDEs) that enable the digestion of plant tissues first appeared in the genomes of herbivorous beetles during the Jurassic period. Furthermore, our analyses reveal two independent evolutionary introductions of the genes that encode PCWDEs into the genomes of herbivorous beetles, one of which originated from fungi and the second of which originated from bacteria. Overall, this study shows that the transfer of genes from fungi and bacteria to beetles can facilitate the colonization of new diets and habitats and that interactions with microbes are an important factor in the evolutionary trajectory of beetles. Results shed light on the evolution and genomic basis of specialized feeding by beetle herbivores.

Technical Abstract: Herbivorous insects are a dominant feature of terrestrial biodiversity but the evolution and genomic basis of plant feeding in insects remains virtually unknown. We reconstructed the phylogeny of beetles (order Coleoptera) and the evolution of beetle genes encoding putative plant cell wall degrading enzymes (PCWDEs) using genomic data from 521 species. Our analyses resolve beetle relationships and reveal the rapid diversification of specialized herbivorous beetles - accounting for nearly 20% of insect species - following independent origins of PCWDEs from Bacteria and Fungi beginning in the Jurassic. The origin and subsequent adaptive evolution of beetle genes enabling efficient metabolism of woody plant biomass thus appears to have been key to the Mesozoic adaptive radiation of beetles on plants.