Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments

PLoS Biol. 2017 Apr 11;15(4):e2001627. doi: 10.1371/journal.pbio.2001627. eCollection 2017 Apr.

Abstract

Repeated adaptation to a new environment often leads to convergent phenotypic changes whose underlying genetic mechanisms are rarely known. Here, we study adaptation of color vision in threespine stickleback during the repeated postglacial colonization of clearwater and blackwater lakes in the Haida Gwaii archipelago. We use whole genomes from 16 clearwater and 12 blackwater populations, and a selection experiment, in which stickleback were transplanted from a blackwater lake into an uninhabited clearwater pond and resampled after 19 y to test for selection on cone opsin genes. Patterns of haplotype homozygosity, genetic diversity, site frequency spectra, and allele-frequency change support a selective sweep centered on the adjacent blue- and red-light sensitive opsins SWS2 and LWS. The haplotype under selection carries seven amino acid changes in SWS2, including two changes known to cause a red-shift in light absorption, and is favored in blackwater lakes but disfavored in the clearwater habitat of the transplant population. Remarkably, the same red-shifting amino acid changes occurred after the duplication of SWS2 198 million years ago, in the ancestor of most spiny-rayed fish. Two distantly related fish species, bluefin killifish and black bream, express these old paralogs divergently in black- and clearwater habitats, while sticklebacks lost one paralog. Our study thus shows that convergent adaptation to the same environment can involve the same genetic changes on very different evolutionary time scales by reevolving lost mutations and reusing them repeatedly from standing genetic variation.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptation, Ocular / radiation effects*
  • Alleles
  • Amino Acid Substitution
  • Animals
  • British Columbia
  • Color Vision / radiation effects
  • Cone Opsins / genetics*
  • Cone Opsins / metabolism
  • Evolution, Molecular*
  • Fish Proteins / genetics*
  • Fish Proteins / metabolism
  • Gene Duplication
  • Gene Frequency
  • Gene-Environment Interaction
  • Genetic Variation / radiation effects*
  • Genomics / methods
  • Islands
  • Lakes
  • Pacific Ocean
  • Phylogeny
  • Smegmamorpha / genetics
  • Smegmamorpha / growth & development
  • Smegmamorpha / physiology*
  • Species Specificity
  • Sunlight*

Substances

  • Cone Opsins
  • Fish Proteins