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, esti...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2019-12, Vol.116 (49), p.24729-24737
Main Authors: McKenna, Duane D., Shin, Seunggwan, Ahrens, Dirk, Balke, Michael, Beza-Beza, Cristian, Clarke, Dave J., Donath, Alexander, Escalona, Hermes E., Friedrich, Frank, Letsch, Harald, Liu, Shanlin, Maddison, David, Mayer, Christoph, Misof, Bernhard, Murin, Peyton J., Niehuis, Oliver, Peters, Ralph S., Podsiadlowski, Lars, Pohl, Hans, Scully, Erin D., Yan, Evgeny V., Zhou, Xin, Ślipiński, Adam, Beutel, Rolf G.
Format: Article
Language:English
Subjects:
Angiosperms
Animals
Bacteria - enzymology
Bacteria - genetics
Bacterial Proteins - genetics
Bacterial Proteins - metabolism
Beetles
Biodiversity
Biological Evolution
Biological Sciences
Carboniferous
Cell Wall - chemistry
Cell Wall - metabolism
Cell walls
Cellulases - genetics
Cellulases - metabolism
Coleoptera
Coleoptera - enzymology
Coleoptera - genetics
Coleoptera - microbiology
Digestion
Evolution
Evolutionary genetics
Feeding
Fungal Proteins - genetics
Fungal Proteins - metabolism
Fungi
Fungi - enzymology
Fungi - genetics
Gene Transfer, Horizontal
Genes
Genome, Insect
Genomes
Herbivory
Herbivory - genetics
Insect Proteins - genetics
Insect Proteins - metabolism
Jurassic
Lignin - chemistry
Lignin - metabolism
Lignocellulose
Mesozoic
Microorganisms
Phylogeny
Plant tissues
Plants - chemistry
PNAS Plus
Polysaccharide-Lyases - genetics
Polysaccharide-Lyases - metabolism
Polysaccharides - chemistry
Polysaccharides - metabolism
Species
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Summary: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.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.1909655116