Beetles’ diversity was driven by coevolution with plants — and a little help from some microbial friends

A green immigrant leaf weevil, Polydrusus sericeus, one of tens of thousands of species in the family Curculionidae (Flickr, Dann Thrombs)

Beetles have long had a special place, if not in the heart of the Creator, in the imaginations of evolutionary biologists. They’re widely considered the most diverse single clade of animals, something upwards of 400,000 species that share a common ancestor — when the explosive diversification of that ancient lineage began, how it proceeded, and what caused it have been the subject of a lot of research. Many of those questions are addressed in a paper published in Proceedings of the National Academy of Sciences last month, which uses an unprecedented genomic dataset to figure out when beetles began their epic diversification, and tests one major hypothesis for the reason behind that diversification.

The going hypothesis for beetles’ diversity has long been that coevolution with flowering plants was responsible. Some of the most diverse beetle clades feed on living plant tissue, and the idea is that the evolutionary arms race between plants’ chemical and physical defenses and the counter-measures of herbivorous beetles — tolerating or breaking down toxins, dodging prickles and rerouting latex – helped push both trophic players into new realms of biodiversity. However, it wasn’t clear that the timing worked out. A reconstruction of the history of weevils, a major clade of plant-feeding beetles, found that they didn’t began their diversification in synchronization with flowering plants, but some time after angiosperms became the dominant group of plants on land.

The new paper, led by Duane McKenna, tackles a much broader sample of beetle diversity with several modern sets of genetic data. First, the authors estimated a new phylogeny of the beetles from data for over 4800 protein-coding genes in 146 species; they then used data from 89 genes in 521 species to reconstruct a time-calibrated phylogeny and identify points at which diversification increased — presumably as new species formed while adapting to novel environments or resources.

That time-calibrated reconstruction puts the origins of the beetles in the Carboniferous, about 327 million years ago, which is rather earlier than the oldest-known beetle fossils. However, it also found major accelerations of diversification for several herbivorous beetle clades in time-frames aligned with the origins and increasing dominance of flowering plants. As a nice counterpoint, this analysis also reconstructs a parallel decrease in diversification rates for beetle lineages associated with non-flowering plants. The authors estimate that a quarter of all the increases in diversification that they find are associated with transitions to herbivory, making it the single factor that contributed most to beetle diversification.

The final data set in the paper examines the diversification of beetle genes, rather than beetles — specifically, a class of genes that code for enzymes which can degrade the complex structural molecules of plant cell walls. Animals have relatively few such enzymes, which is why many herbivorous species rely on gut bacteria or other microbial symbionts to help them get the most out of their diets. Herbivorous beetles possess whole classes of plant cell wall-degrading enzymes seen in no other animal taxa, which they may have picked up from symbiotic fungi and bacteria via horizontal gene transfer.

Targeted sequencing of these genes in the taxa from the first phylogenetic reconstruction found concentrations of diversity in the Buprestoidea and the Phytophaga, two herbivorous beetle lineages that are sufficiently far enough apart in the phylogeny that it is quite unlikely for them to have inherited all these specialized enzymes from a common ancestor. The sequences of beetles’ cell wall-degrading enzyme genes did indeed suggest shared ancestry with equivalent enzymes in bacteria and fungi, and bacterial and fungal taxa that have been found in symbiosis with beetles. However, this shared ancestry predated the common ancestors of all genes within each family of cell wall-degrading enzymes in the beetles. That is to say, beetle lineages likely acquired single members of each enzyme family from microbial symbionts, then elaborated those enzymes as they diversified to exploit a wide array of host plants.

Representation of an array of plant cell wall-degrading enzyme families across the beetle phylogeny, and relationships between genes in each family from beetles and from bacteria or fungi. (McKenna et al 2019, Figure 3)

So this study fills in some substantial details about how there came to be so many beetles, both by lining up the timing of their diversification with the rise of flowering plants, and by tracing the origins of a key innovation — the enzymes that allow many beetles to make a living eating plant matter — that made transitions to herbivory possible and profitable. Attributing beetle diversification to the acquisition of key genes from microbial symbionts would’ve seemed pretty wild a few years ago, but the scenario outlined in this data suggests a relatively conservative version of that hypothesis: mostly via single gene-transfer events within herbivorous lineages, that gave them a starting place for further adaptive diversification.

References

Farrell, B. D. 1998. “Inordinate fondness” explained: Why are there so many beetles? Science 281:555–559. doi: 10.1126/science.281.5376.555

McKenna, D. D., A. S. Sequiera, A. E. Marvaldi, and B. Farrell. 2009. Temporal lags and overlap in the diversification of weevils and flowering plants. PNAS 106:7083–7088. doi: 10.1073/pnas.0810618106

McKenna, D. D., S. Shin, D. Ahrens, M. Balke, C. Beza-Beza, D. J. Clarke, A. Donath, et al. 2019. The evolution and genomic basis of beetle diversity. PNAS 201909655. doi: 10.1073/pnas.1909655116

About Jeremy Yoder

Jeremy Yoder is an Assistant Professor of Biology at California State University, Northridge. He also blogs at Denim and Tweed, and tweets under the handle @jbyoder.
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