Rapid adaptive evolution of colour vision in the threespine stickleback radiation

Abstract

Vision is a sensory modality of fundamental importance for many animals, aiding in foraging, detection of predators and mate choice. Adaptation to local ambient light conditions is thought to be commonplace, and a match between spectral sensitivity and light spectrum is predicted. We use opsin gene expression to test for local adaptation and matching of spectral sensitivity in multiple independent lake populations of threespine stickleback populations derived since the last ice age from an ancestral marine form. We show that sensitivity across the visual spectrum is shifted repeatedly towards longer wavelengths in freshwater compared with the ancestral marine form. Laboratory rearing suggests that this shift is largely genetically based. Using a new metric, we found that the magnitude of shift in spectral sensitivity in each population corresponds strongly to the transition in the availability of different wavelengths of light between the marine and lake environments. We also found evidence of local adaptation by sympatric benthic and limnetic ecotypes to different light environments within lakes. Our findings indicate rapid parallel evolution of the visual system to altered light conditions. The changes have not, however, yielded a close matching of spectrum-wide sensitivity to wavelength availability, for reasons we discuss.

Keywords: Gasterosteus aculeatus; evolution; gene expression; local adaptation; opsin; visual ecology.

Figure 1.

Normalized cone opsin gene expression of marine and freshwater populations. Marine populations are indicated in black and freshwater populations in grey. Horizontal lines indicate the mean of all populations; circles indicate individual fish. O, Oyster Lagoon; LC, Little Campbell River; Pr, Priest Lake; Pa, Paxton Lake; LQ, Little Quarry Lake; T, Trout Lake; K, Kirk Lake; C, Cranby Lake.

Figure 2.

Estimated spectral sensitivity of marine and freshwater populations assuming both use only the A₁ chromophore. Marine populations are indicated in black and freshwater in grey. The thin lines are the fitted values of spectral sensitivity from the mixed-effects model. The shaded regions are 1 s.d. above and below the fitted values, with standard errors also derived from the mixed-effects model.

Figure 3.

Normalized cone opsin gene expression of benthic and limnetic populations. The benthic populations are in black and limnetic populations in grey. Horizontal lines indicate the mean of all populations; triangles indicate individual fish. Location names abbreviated as: Pr, Priest Lake; Pa, Paxton Lake; LQ, Little Quarry Lake.

Figure 4.

Opsin expression in wild and laboratory-reared fish from a marine (O, Oyster Lagoon) and freshwater location (Pr, Priest Lake). Wild fish are indicated in black, laboratory-reared fish in grey. Horizontal lines indicate the mean of the population, and points indicate individual fish.

Figure 5.

(a) Correlations between shifts in spectral sensitivity of individuals from freshwater populations and differences in local light transmission relative to the reference marine population, Oyster Bay. (b) As in (a) but using irradiance to measure light environment shift. (c) Correlations between shifts in spectral sensitivity between sympatric benthic and limnetic stickleback species and differences in local light transmission. (d) As in (c) but using irradiance to compare light environments.