Abstract
BackgroundThe diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. Indeed, the largest beetle suborder, Polyphaga, mostly includes plant eaters among its approximately 315,000 species. In particular, plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. However, evidence of changes in beetle gene repertoires driven by such interactions remains largely anecdotal and without explicit hypothesis testing.ResultsWe explore the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representative of the two most species-rich beetle suborders. We contrast the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We find gene repertoire evolution to be more dynamic, with significantly more adaptive lineage-specific expansions, in the more speciose Polyphaga. Testing the specific hypothesis of adaptation to plant feeding, we identify families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There is notable support for the selection hypothesis on large gene families for glutathione S-transferase and carboxylesterase detoxification enzymes.ConclusionsOur explicit modeling of the evolution of gene repertoires across 18 species identifies putative adaptive lineage-specific gene family expansions that accompany the dietary shift towards plants in beetles. These genomic signatures support the popular hypothesis of a key role for interactions with plant chemical defenses, and for plant feeding in general, in driving beetle diversification.
Highlights
The diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed
Using genomic and transcriptomic data from 18 beetle species, we estimate ancestral gene family content, taking into account gene gains and losses across the species phylogeny, to identify significant lineage-specific expansion (LSE) of gene families related to phytophagy and signatures of adaptive expansions in these families. As their evolution might be driven by agents other than those related strictly to trophic niche [30], and morphological genes, as their inferred association with diet is less robust, we focus on genes coding for enzymes, for which adaptive LSE specific to Polyphaga would suggest a role for detoxification and digestive pathways in driving adaptation and speciation
Our modeling of gene repertoire evolution across 18 beetle species identifies putative adaptive lineage-specific gene family expansions that accompany a dietary shift towards plant feeding
Summary
The diversity and evolutionary success of beetles (Coleoptera) are proposed to be related to the diversity of plants on which they feed. The largest beetle suborder, Polyphaga, mostly includes plant eaters among its approximately 315,000 species. Plants defend themselves with a diversity of specialized toxic chemicals. These may impose selective pressures that drive genomic diversification and speciation in phytophagous beetles. Beetles (Coleoptera) encompass approximately 380,000 described species, representing ca. The remarkable evolutionary success of beetles may have been driven by the interplay between their trophic niche and their genomic content and architecture. This is based on the premise that environmental and ecological. Plants have evolved diverse strategies to protect themselves, which in turn impose selective pressures on the animals that feed on them
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