Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles

Genome Biology

Seunggwan Shin¹  Duane D. McKenna¹  Camille Pitteloud²  Mathieu Seppey³  Marc Robinson-Rechavi⁴  Robert M. Waterhouse⁴  Julien Roux⁵  Nadir Alvarez⁶  Bernhard Misof⁷  Hermes E. Escalona⁷  Panagiotis Ioannidis⁸  Xin Zhou⁹  Brent C. Emerson^1,10 

[1] 0000 0000 9560 654X, grid.56061.34, Department of Biological Sciences, University of Memphis, Memphis, TN 38111, USA;0000 0001 2165 4204, grid.9851.5, Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland;0000 0001 2156 2780, grid.5801.c, Present address: Department of Environmental Systems Science, ETHZ, 8092, Zurich, Switzerland;0000 0001 2165 4204, grid.9851.5, Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland;0000 0001 2223 3006, grid.419765.8, Present address: Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, 1211, Geneva, Switzerland;0000 0001 2165 4204, grid.9851.5, Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland;0000 0001 2223 3006, grid.419765.8, Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland;0000 0001 2165 4204, grid.9851.5, Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland;0000 0001 2223 3006, grid.419765.8, Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland;0000 0004 1937 0642, grid.6612.3, Present address: Department of Biomedicine, University of Basel, 4031, Basel, Switzerland;0000 0001 2165 4204, grid.9851.5, Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland;Geneva Natural History Museum, 1208, Geneva, Switzerland;0000 0001 2216 5875, grid.452935.c, Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany;0000 0001 2322 4988, grid.8591.5, Department of Genetic Medicine and Development, University of Geneva, 1211, Geneva, Switzerland;0000 0001 2223 3006, grid.419765.8, Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland;0000 0004 0635 685X, grid.4834.b, Present address: Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology–Hellas, Heraklion, Greece;0000 0004 0530 8290, grid.22935.3f, Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China;0000 0004 1804 5442, grid.466812.f, Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de la Laguna, Santa Cruz de Tenerife, Spain;

关键词: Gene family evolution;    Beetle-plant trophic interactions;    Beetle diversification;    Detoxification enzymes;   

DOI  :  10.1186/s13059-019-1704-5

来源: publisher

【 摘 要 】

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.

【 授权许可】

CC BY