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 ~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 To address this, we explored the genomic consequences of beetle-plant trophic interactions by performing comparative gene family analyses across 18 species representing the two most species-rich beetle suborders. We contrasted the gene contents of species from the mostly plant-eating suborder Polyphaga with those of the mainly predatory Adephaga. We found 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 identified families of enzymes putatively involved in beetle-plant interactions that underwent adaptive expansions in Polyphaga. There was especially strong 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 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.
Footnotes
Department of Genetic Medicine and Development, University of Geneva and Swiss Institute of Bioinformatics, Geneva, Switzerland.
Institute of Molecular Biology and Biotechnology, Foundation for Research and Technology - Hellas, Heraklion, Greece.
Department of Environmental Systems Science, ETHZ, Zurich, Switzerland.
Department of Biomedicine, University of Basel, Basel, Switzerland.
mathieu.seppey{at}unige.ch, panagiotis_ioannidis{at}imbb.forth.gr, bemerson{at}ipna.csic.es, camille.pitteloud{at}usys.ethz.ch, marc.robinson-rechavi{at}unil.ch, julien.roux{at}unibas.ch, hermesescalona{at}gmail.com, dmckenna{at}memphis.edu, b.misof{at}zfmk.de, sshin4{at}memphis.edu, xinzhou{at}cau.edu.cn, robert.waterhouse{at}unil.ch, nadir.alvarez{at}ville-ge.ch
List of abbreviations
- ABC
- adenosine triphosphate-binding cassette transporters
- AICc
- Akaike Information Criterion (small-sample-size corrected)
- BM
- Brownian motion
- BUSCO
- Benchmarking Universal Single-Copy Ortholog assessment tool
- CAFE
- Computational Analysis of gene Family Evolution tool
- CE
- carboxylesterase
- CYS
- cysteine protease
- FDR
- false discovery rate
- GH
- glycoside hydrolase
- GST
- glutathione S-transferase
- LSE
- lineage specific expansion
- MAFFT
- Multiple Alignment using Fast Fourier Transform tool
- OG
- orthologous group
- OU
- Ornstein-Uhlenbeck
- P450
- cytochrome P450 monooxygenase
- SER
- serine protease
- UGT
- uridine 5’-diphospho-glycosyltransferase