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

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.

Phenotypic divergence among threespine stickleback that differ in nuptial coloration

“…Recent population genomic studies have begun to unravel the evolutionary forces that underly phenotypic change following the colonization of new habitats Jones, Grabherr, et al, 2012;Marques, Taylor, et al, 2017;Rosenblum et al, 2004). It would be interesting to know whether the phenotypic divergence that we observe in color, shape, size, and plating between freshwater morphs is associated with genetic divergence among populations and color morphs.…”

Predictable genome-wide sorting of standing genetic variation during parallel adaptation to basic versus acidic environments in stickleback fish

“…The quest for elucidating the genomic basis of adaptive diversification commonly proceeds by comparing populations from two ecologically distinct habitat types at genome-wide markers. Genetic loci important to differential adaptation are then identified by screening the populations for exceptionally strong habitat-related genetic differentiation relative to the genome-wide background level (e.g., Roesti et al 2015;Lamichhaney et al 2016;Reid et al 2016;Yeaman et al 2016;Marques et al 2017). This approach is particularly informative when multiple populations adapted independently to each habitat type are available, as such "parallel" (or convergent; Arendt and Reznick 2008) evolution helps distinguish deterministic selective from stochastic genetic differentiation (Berner and Salzburger 2015).…”

“…; Marques et al. ). This approach is particularly informative when multiple populations adapted independently to each habitat type are available, as such “parallel” (or convergent; Arendt and Reznick ) evolution helps distinguish deterministic selective from stochastic genetic differentiation (Berner and Salzburger ).…”

Opsin expression predicts male nuptial color in threespine stickleback

“…These results were also modulated within lakes by depth, a proxy for optical environment (Bolnick et al 2016;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b). Threespine stickleback males display color polymorphism at multiple geographic scales (Reimchen 1989;Boughman, 2001;Scott, 2001;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b;Marques, Lucek et al, 2017;Marques, Taylor et al, 2017). As these color phenotypes typically covary with features of the optical environment, sensory drive theory is commonly invoked to explain the maintenance of multiple color phenotypes (Reimchen 1989;Boughman, 2001;Scott, 2001;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b;Marques, Lucek et al, 2017;Marques, Taylor et al, 2017).…”

“…Threespine stickleback males display color polymorphism at multiple geographic scales (Reimchen 1989;Boughman, 2001;Scott, 2001;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b;Marques, Lucek et al, 2017;Marques, Taylor et al, 2017). As these color phenotypes typically covary with features of the optical environment, sensory drive theory is commonly invoked to explain the maintenance of multiple color phenotypes (Reimchen 1989;Boughman, 2001;Scott, 2001;Brock et al, 2017a;Brock, Bolnick, & Cummings, 2017b;Marques, Lucek et al, 2017;Marques, Taylor et al, 2017). However, negative frequency-dependent selection via male-male competition could also facilitate the maintenance of color polymorphisms, possibly via interactions with the signaling environment (Bolnick et al 2016;Djikstra & Border, 2018;Tinghitella et al, 2017).…”