Nutritional adaptation in the marine to freshwater establishment process – how do diet and genotype shape phenotype?

Nutrients, including vital organic compounds, vary in availability across ecosystems, with the potential to act as a strong source of selection for traits that increase nutrient acquisition and biosynthesis. Compared with freshwater ecosystems, marine ecosystems are much richer in the omega-3 long-chain polyunsaturated fatty acid docosahexaenoic acid (DHA) and thus marine animals establishing new freshwater populations are faced with the challenge of acquiring DHA. However, the relative roles of DHA synthesis capacity and diet in the freshwater establishment process remain unresolved. We used common garden experiments to explore phenotypic responses to dietary nutrient content in threespine sticklebacks (Gasterosteus aculeatus) that varied in their genetic capacity for DHA synthesis. We found that diet as well as presumed metabolic adaptation to freshwater nutritional environments (population identity) had strong effects on stickleback phenotype and performance. Sticklebacks enriched with marine-derived fatty acids including DHA grew more and were in better condition compared with controls. Those fed diets with more DHA also accumulated more DHA in muscle tissue. Freshwater sticklebacks accumulated more DHA compared with those from a marine population. However, populations with greater fads2 copy number did not consistently have higher performance or DHA accumulation. Together, these results suggest that DHA availability during development can strongly influence phenotype and performance, with the potential to act as a source of selection. Our findings also suggest that mechanisms beyond the accumulation of fads2 copies, such as plasticity in expression or variation in other DHA synthesis pathway genes, could be important adaptations to the nutritional constraints of freshwater.