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.

Convergent evolution of body color between sympatric freshwater fishes via different visual sensory evolution

“…On the other hand, the coevolution pattern between body color and visual sense in Nomorhamphus might be similar to that reported in lake sticklebacks, in which female perceptual sensitivity to red light increases with decreasing extent of long wavelengths in habitat environments, and the male body redness is tuned to the female perceptual sensitivity (Boughman, 2001; but see Rennison, Owens, Heckman, Schluter, & Veen, 2016). Boughman (2001) argued that this positive covariance could be caused by the male signals evolving to match a pre-existing bias.…”

Regulatory Architecture of Gene Expression Variation in the Threespine Stickleback Gasterosteus aculeatus

“…The species is also distributed throughout semimarine environments with large temperature and salinity gradients, such as estuaries and the brackish water Baltic Sea (McCairns and Bernatchez 2010; Guo et al 2015; Konijnendijk et al 2015). Successful colonization of these diverse habitats necessitates behavioral, morphological, and physiological adaptation to novel environmental conditions including changed temperature, salinity, oxygen, light, parasite and predator regimens, a process that can occur rapidly (Kitano et al 2010; Barrett et al 2011; Terekhanova et al 2014; Lescak et al 2015; Huang et al 2016, Rennison et al 2016). Parallel adaptations between independently founded freshwater populations frequently involve the same regions of the genome and arise from preexisting genetic variation in the marine population (Colosimo et al 2005; Hohenlohe et al 2010; Jones et al 2012; Liu et al 2014; Conte et al 2015, but see DeFaveri et al 2011; Leinonen et al 2012; Ellis et al 2015; Ferchaud and Hansen 2016).…”

Climatic niche evolution is faster in sympatric than allopatric lineages of the butterfly genusPyrgus

“…Over small spatial scales, habitat heterogeneity in the form of climatic variation or differences in community composition may initiate niche shifting in response to competition. Variation in the performance of populations under contrasting environmental conditions may ultimately promote divergence, as shown along a depth gradient in fishes [30].…”