Nutrient availability differs among habitats and can promote evolutionary divergence in metabolic traits among populations. Populations in chronic resource-limited environments are often expected to favor genotypes that promote efficient energy absorption and retention. However, a crucial evolutionary question remains: Does adaptation to nutrient-poor environments lead to a global shift in metabolic processing, or are these changes restricted to specific storage depots while essential functions remain conserved?
To address this question, we used the three-spined stickleback (Gasterosteus aculeatus) as a model. Sticklebacks rapidly and repeatedly adapt to new freshwater habitats on many different continents, making them a good model to study ecological evolution. Marine ecotypes occupy nutrient-rich environments abundant in long-chain polyunsaturated fatty acids (LC-PUFAs) like docosahexaenoic acid (DHA), whereas stream ecotypes have adapted to freshwater habitats that are often less productive and deficient in these essential fatty acids. We reared marine and stream ecotypes under two dietary regimes: a "poor" diet (low-calorie, DHA-deficient) and a "rich" diet (high-calorie, DHA-enriched). We then measured growth, visceral fat deposition level, and blood cholesterol levels, alongside a comprehensive whole-body lipidome analysis.
First, both ecotypes exhibited consistent responses to dietary quality regarding growth and core lipid composition; the rich diet promoted increased body size and triacylglycerol levels. Also, both populations maintained a preserved capacity to efficiently incorporate DHA into cellular membranes and phospholipid classes. Second, several parameters remained invariant regardless of ecotype or diet, with blood cholesterol and sphingolipid levels showing no significant differences. Third, a significant Gene × Environment interaction was observed in visceral fat deposition. Under the rich diet, the stream ecotype exhibited a pronounced and consistent increase in visceral fat accumulation, whereas the marine ecotype showed a more variable storage response.
These findings suggest that metabolic adaptation to nutritional scarcity is modular rather than systemic. Our study demonstrates that ecotypes have diverged in their physiological capacity for visceral lipid accumulation. However, the biochemical mechanisms governing essential lipid utilization remain evolutionarily conserved across populations. These results imply that shifts in energy storage can be decoupled from the evolutionary change in core metabolic functions.