Just a few days after the IPBES’ global biodiversity assessment was presented in Paris, SIB Scientists at the University of Lausanne published a paper explaining the origin of the biodiversity observed among beetles, arguably the largest species richness in the animal kingdom. The international study, published in Genome Biology, employed SIB bioinformatics resources to contrast the gene repertoires of plant-eating beetle species with predatory ones. The results support the view that coevolution with the plants they feed on, and in particular the evolutionary adaptations to neutralise toxic plant compounds, are key drivers of their diversification.

On the importance of early data access

The multi-species analyses were made possible by the availability of insect genomic data from initiatives such as the i5k (Sequencing Five Thousand Arthropod Genomes) and 1KITE (One Thousand Insect Transcriptome Evolution) projects, often as part of pre-publication datasets. Mathieu Seppey remarks, “In order to use genomics to explore the diversity of beetles – elegantly described by J. B. S. Haldane as ‘God’s inordinate fondness for beetles’ – I needed data from several species. I am thus grateful for the contribution of our collaborators who shared their pre-publication data to allow me to expand my set of species and pursue my own research questions. For me, this highlights the importance of early data access, which, in the end, maximises their value.”

Plant–insect interactions: an evolutionary arms race

Beetle species’ richness encompasses more than 380,000 described species, making them one of the largest and most diverse groups of animals. Several explanations have been put forward as to the underlying reasons for this striking species radiation, with the predominant hypothesis focusing on plant–beetle feeding interactions. “This hypothesis is logically appealing because plants offer an abundant and varied food source but they also defend themselves against plant-eating insects, which in turn must continuously find the means to counteract these defences, in an endless arms race. However, evidence to date of genomic changes in insects driven by these interactions has remained largely anecdotal and without explicit hypothesis testing,” explains lead investigator Robert Waterhouse, SIB Group Leader at the Department of Ecology and Evolution, University of Lausanne, Switzerland.

Indeed, to switch from a diet of detritus or fungi to feeding on plants, beetles needed to innovate and develop a remarkable arsenal of weapons. Among these, a key adaptation of plant-eating (phytophagous) beetles, “...is their ability to neutralise or minimise the effects of plant secondary compounds, in a process known as detoxification,” explains co-lead investigator, Nadir Alvarez from the Geneva Natural History Museum. Other tactical strategies include quickly excreting the toxic compounds ingested – and sometimes sequestering them for their own defence – as well as developing specialised mouthparts to overcome a plant’s physical barriers. “Our study focused on genes involved in digestion and detoxification as the processes most clearly directly involved in insect–plant feeding interactions,” explains first author SIB’s Mathieu Seppey, who initiated the research as part of his Molecular Life Sciences Master’s thesis project at the University of Lausanne.

Gene family evolution is much more dynamic in herbivorous than carnivorous beetles

The study explored the possible genomic consequences of plant–beetle interactions by contrasting gene repertoires of nine species each from the mostly plant-eating Polyphaga with those of the mainly predatory (animal-eating) Adephaga. The first step involved assessing the completeness of the genome and transcriptome datasets using Benchmarking Universal Single-Copy Orthologues (BUSCOs) and then delineating families of orthologous genes among species (i.e. equivalent genes in different species encoding proteins with similar functions) using OrthoDB, both of which are SIB resources.

The results show that species feeding on plants present a more dynamic gene repertoire evolution than those feeding on animals, including expansions of gene families such as glutathione S-transferases and carboxylesterases. These enzymes are implicated in dealing with plant defences, and the larger numbers of genes encoding these enzymes in plant-feeding beetles represents a signature of adaptive expansion. This supports the theory that coevolution with the plants they feed on is a significant driver of beetle diversity. “Importantly, our novel approach shows the power of comparing many species with rigorous statistics and explicit modelling of evolutionary processes, to find evidence for adaptive selection,” highlights co-author Marc Robinson-Rechavi, SIB Group Leader at the Department of Ecology and Evolution, University of Lausanne.

Colorado potato beetle
The Colorado potato beetle, Leptinotarsa decemlineata, is one of the nine plant-feeding species that were compared to nine predaceous species in this study. Photo by Scott Bauer, USDA.

Reference:
Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles. Seppey et al., 2019, Genome Biology. DOI: 10.1186/s13059-019-1704-5