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. Author summary When organisms colonize a new environment in replicate, natural selection often leads to similar phenotypic adaptations. Such “convergent evolution” is known from both distant relatives, e.g., sea cows and whales adapting to an aquatic life, and from multiple populations within a species, but the causing genetic changes are rarely known. Here, we studied how a fish, the threespine stickleback, repeatedly adapted its color vision to living in red light–dominated blackwater lakes. Using multiple natural populations and a 19-y evolution experiment, we found selection on a blue light–sensitive visual pigment gene. One allele of this gene with a red-shifted light sensitivity facilitated repeated blackwater colonization. Surprisingly, two amino acid changes responsible for the red-shift have independently occurred 198 million years earlier, after the gene was duplicated in the ancestor of all spiny-rayed fish and modified into blue- and red-shifted gene copies. While other fish species today use these two gene copies to adapt to clear- and blackwater, stickleback have lost a copy and reevolved these mutations on different alleles of the same gene causing convergent adaptation to these habitats. Thus, we conclude that the same genetic changes can be responsible for convergent evolution on very different time scales.
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