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Molecular Evolution of the Odorant and Gustatory Receptor Genes in Lepidopteran Insects: Implications for Their Adaptation and Speciation

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Abstract

Lepidoptera (comprised of butterflies and moths) is one of the largest groups of insects, including more than 160,000 described species. Chemoreception plays important roles in the adaptation of these species to a wide range of niches, e.g., plant hosts, egg-laying sites, and mates. This study investigated the molecular evolution of the lepidopteran odorant (Or) and gustatory receptor (Gr) genes using recently identified genes from Bombyx mori, Danaus plexippus, Heliconius melpomene, Plutella xylostella, Heliothis virescens, Manduca sexta, Cydia pomonella, and Spodoptera littoralis. A limited number of cases of large lineage-specific gene expansion are observed (except in the P. xylostella lineage), possibly due to selection against tandem gene duplication. There has been strong purifying selection during the evolution of both lepidopteran odorant and gustatory genes, as shown by the low ω values estimated through CodeML analysis, ranging from 0.0093 to 0.3926. However, purifying selection has been relaxed on some amino acid sites in these receptors, leading to sequence divergence, which is a precursor of positive selection on these sequences. Signatures of positive selection were detected only in a few loci from the lineage-specific analysis. Estimation of gene gains and losses suggests that the common ancestor of the Lepidoptera had fewer Or genes compared to extant species and an even more reduced number of Gr genes, particularly within the bitter receptor clade. Multiple gene gains and a few gene losses occurred during the evolution of Lepidoptera. Gene family expansion may be associated with the adaptation of lepidopteran species to plant hosts, especially after angiosperm radiation. Phylogenetic analysis of the moth sex pheromone receptor genes suggested that chromosomal translocations have occurred several times. New sex pheromone receptors have arisen through tandem gene duplication. Positive selection was detected at some amino acid sites predicted to be in the extracellular and transmembrane regions of the newly duplicated genes, which might be associated with the evolution of the new pheromone receptors.

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Acknowledgments

We would like to thank Hugh Robertson from the University of Illinois, Urbana Champaign, for the BmGr DNA sequences; Shui Zhan and Stephen Reppert from the University of Massachusetts Medical School, for the DpOR and DpGR protein sequences. Fillipe Vieira and Julio Rozas from the University of Barcelona for suggestion for the use of BadiRate. We thank the editor and the three anonymous reviewers for giving constructive suggestions for the improvement of this paper. This study was financially supported by the Graduate School and the Department of Biology, Faculty of Science, Prince of Songkla University.

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  1. Department of Biology, Faculty of Science, Prince of Songkla University, Songkla, 90112, Thailand

    Patamarerk Engsontia & Chutamas Satasook

  2. The Center for Genomics and Bioinformatics Research, Department of Molecular Biotechnology and Bioinformatics, Faculty of Science, Prince of Songkla University, Songkla, 90112, Thailand

    Unitsa Sangket & Wilaiwan Chotigeat

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Engsontia, P., Sangket, U., Chotigeat, W. et al. Molecular Evolution of the Odorant and Gustatory Receptor Genes in Lepidopteran Insects: Implications for Their Adaptation and Speciation. J Mol Evol 79, 21–39 (2014). https://doi.org/10.1007/s00239-014-9633-0

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  • DOI: https://doi.org/10.1007/s00239-014-9633-0

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