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

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.

Data and Resources

Additional Info

Field Value
Source
Version
Authors
Maintainer
Maintainer Email
Article Host Type publisher
Article Is Open Access true
Article License Type cc-by
Article Version Type publishedVersion
Citation Report https://scite.ai/reports/10.1371/journal.pbio.2001627
DOI 10.1371/journal.pbio.2001627
Date Last Updated 2019-05-14T04:31:20.803775
Evidence open (via page says license)
Funder code(s)
Journal Is Open Access true
Open Access Status gold
PDF URL https://journals.plos.org/plosbiology/article/file?id=10.1371/journal.pbio.2001627&type=printable
Publisher URL https://doi.org/10.1371/journal.pbio.2001627