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Genome Biol. 2019 May 17;20(1):98. doi: 10.1186/s13059-019-1704-5.

Genomic signatures accompanying the dietary shift to phytophagy in polyphagan beetles.

Author information

1
Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland.
2
Present address: Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, 1211, Geneva, Switzerland.
3
Department of Genetic Medicine and Development, University of Geneva, 1211, Geneva, Switzerland.
4
Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland.
5
Present address: Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology-Hellas, Heraklion, Greece.
6
Island Ecology and Evolution Research Group, Instituto de Productos Naturales y Agrobiología (IPNA-CSIC), San Cristóbal de la Laguna, Santa Cruz de Tenerife, Spain.
7
Present address: Department of Environmental Systems Science, ETHZ, 8092, Zurich, Switzerland.
8
Present address: Department of Biomedicine, University of Basel, 4031, Basel, Switzerland.
9
Center for Molecular Biodiversity Research (ZMB), Zoological Research Museum Alexander Koenig, 53113, Bonn, Germany.
10
Department of Biological Sciences, University of Memphis, Memphis, TN 38111, USA.
11
Department of Entomology, College of Plant Protection, China Agricultural University, Beijing, China.
12
Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland. robert.waterhouse@unil.ch.
13
Swiss Institute of Bioinformatics, 1015, Lausanne, Switzerland. robert.waterhouse@unil.ch.
14
Department of Ecology and Evolution, University of Lausanne, 1015, Lausanne, Switzerland. nadir.alvarez@ville-ge.ch.
15
Geneva Natural History Museum, 1208, Geneva, Switzerland. nadir.alvarez@ville-ge.ch.

Abstract

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.

KEYWORDS:

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

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