Opsin Evolution in Damselfish: Convergence, Reversal, and Parallel Evolution Across Tuning Sites

Abstract

The visual system plays a role in nearly every aspect of an organism’s life history, and there is a direct link between visual pigment phenotypes and opsin genotypes. In previous studies of African cichlid fishes, we found evidence for positive selection among some opsins, with sequence variation greatest for opsins producing the shortest and longest wavelength visual pigments. In this study, we examined opsin evolution in the closely related damselfish family (Pomacentridae), a group of reef fishes that are distributed widely and have a documented fossil record of at least 50 million years (MY). We found increased functional variation in the protein sequences of opsins at the short- and long-wavelength ends of the visual spectrum, in agreement with the African cichlids, despite an order of magnitude difference in the ages of the two radiations. We also reconstructed amino acid substitutions across opsin tuning sites. These reconstructions indicated multiple instances of parallel evolution, at least one definitive case of convergent evolution, and one evolutionary reversal. Our findings show that the amino acids at spectral tuning sites are labile evolutionarily, and that the same codons evolve repeatedly. These findings emphasize that the aquatic light environment can shape opsin sequence evolution. They further show that phylogenetic approaches can provide important insights into the mechanisms by which natural selection “tinkers” with phenotypes.

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Acknowledgments

We would like to thank Shaun Collin and the 2007 Marine Neurobiology course attendees as well as the Moreton Bay Research Station for their hospitality. Thanks also to Alan Goldizen for logistical support. This work was supported by the University of Maryland, NSF grant IOS 0841270 (KLC), and the Australian Research Council (NJM). Members of the University of Maryland cichlid group provided valuable suggestions, comments, and support throughout this project

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Correspondence to Christopher M. Hofmann.

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Hofmann, C.M., Marshall, N.J., Abdilleh, K. et al. Opsin Evolution in Damselfish: Convergence, Reversal, and Parallel Evolution Across Tuning Sites. J Mol Evol 75, 79–91 (2012). https://doi.org/10.1007/s00239-012-9525-0

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Keywords

  • Opsin
  • Ancestral state reconstruction
  • Parallel evolution
  • Pomacentridae