Opsins have evolved under the permanent heterozygote model: insights from phylotranscriptomics of Odonata

Anton Suvorov, Nicholas O. Jensen, Camilla R. Sharkey, M. Stanley Fujimoto, Paul Bodily, Haley M.Cahill Wightman, T. Heath Ogden, Mark J. Clement, Seth M. Bybee

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

Gene duplication plays a central role in adaptation to novel environments by providing new genetic material for functional divergence and evolution of biological complexity. Several evolutionary models have been proposed for gene duplication to explain how new gene copies are preserved by natural selection, but these models have rarely been tested using empirical data. Opsin proteins, when combined with a chromophore, form a photopigment that is responsible for the absorption of light, the first step in the phototransduction cascade. Adaptive gene duplications have occurred many times within the animal opsins’ gene family, leading to novel wavelength sensitivities. Consequently, opsins are an attractive choice for the study of gene duplication evolutionary models. Odonata (dragonflies and damselflies) have the largest opsin repertoire of any insect currently known. Additionally, there is tremendous variation in opsin copy number between species, particularly in the long-wavelength-sensitive (LWS) class. Using comprehensive phylotranscriptomic and statistical approaches, we tested various evolutionary models of gene duplication. Our results suggest that both the blue-sensitive (BS) and LWS opsin classes were subjected to strong positive selection that greatly weakens after multiple duplication events, a pattern that is consistent with the permanent heterozygote model. Due to the immense interspecific variation and duplicability potential of opsin genes among odonates, they represent a unique model system to test hypotheses regarding opsin gene duplication and diversification at the molecular level.

Original languageEnglish (US)
Pages (from-to)1306-1322
Number of pages17
JournalMolecular ecology
Volume26
Issue number5
DOIs
StatePublished - Mar 1 2017
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2016 John Wiley & Sons Ltd

Copyright:
Copyright 2017 Elsevier B.V., All rights reserved.

Keywords

  • Bayesian model
  • gene duplications
  • insect vision
  • positive selection

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