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

David A Marques,David M Kingsley,John S Taylor,Thomas E Reimchen,Felicity C Jones,Federica Di Palma,Nick Barton

doi:10.1371/journal.pbio.2001627

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.

Highlights

Successful colonization of a new habitat requires adaptation to a multitude of different selection pressures
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

Summary

Introduction

Successful colonization of a new habitat requires adaptation to a multitude of different selection pressures. When similar habitats are colonized in replicate by different populations or species, phenotypic adaptation is often convergent [1], and this is most striking in adaptive radiations in multiple lakes or on several islands [2]. An adaptive radiation with replicate habitat colonization is found among threespine stickleback (Gasterosteus aculeatus) inhabiting the Haida Gwaii archipelago, British Columbia, Canada. One major predictor of natural selection in the Haida Gwaii stickleback radiation is the spectrum of visible light [16]. Most Haida Gwaii lakes are either oligotrophic clearwater lakes featuring full-spectrum light to blue-shifted light with increasing depth, or they are dystrophic blackwater lakes, stained by dissolved tannins leading to a red-shifted light spectrum [16,17,18]. Blackwater lakes are extreme, almost “nocturnal” visual environments, as both downwelling shortwavelength light and almost all up- or sidewelling light is absorbed, leaving only downwelling red light in a small cone above the focal animal

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