Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles.
Seppey MDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
Ioannidis PDepartment of Genetic Medicine and Development, University of Geneva, 1211, Geneva, Switzerland.
Emerson BCIsland Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de la Laguna, Santa Cruz de Tenerife, Spain.
Pitteloud CDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
Robinson-Rechavi MDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
Roux JDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
Escalona HECenter for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.
McKenna DDDepartment of Biological Sciences, University of Memphis, Memphis, TN 38111, USA.
Misof BCenter for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.
Shin SDepartment of Biological Sciences, University of Memphis, Memphis, TN 38111, USA.
Zhou XDepartment of Entomology, College of Plant Protection, China Agricultural University, Beijing, China.
Waterhouse RMDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland. robert.waterhouse@unil.ch.
Alvarez NDepartment of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland. nadir.alvarez@ville-ge.ch.
English
BACKGROUND The 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.
RESULTS We 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.
CONCLUSIONS Our 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.