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Metabolic and behavioral solutions to the nutritional challenges of life in freshwater

Periodic Reporting for period 1 - FADSEVOL (Metabolic and behavioral solutions to the nutritional challenges of life in freshwater)

Okres sprawozdawczy: 2021-07-01 do 2023-06-30

All animals require a diverse suite of elemental nutrients and organic compounds in order to survive and reproduce, but nutrients vary widely in their availability both among and within ecosystems. Theory predicts an inverse relationship between availabilitv of organic
animal's diet and its abilitv to make or svnthesize. these nutrients from simpler compounds. Across the tree of lite. organisms feeding on nutritionallv-poor foods tvpicallv have a greater capacitv for synthesis than those feeding on nutritionallv-rich foods. However, the question of how this ability evolves evolves remains unresolved. When species encounter new landscapes with new foods, tor example during range expansion, they may be confronted with lower quality foods as well as competition for these resources with other species. To establish in such environments species: can evolve the capacity to synthesize a greater diversity of important organic compounds internally, and/or change their diet by evolving new traits that enable them to use either new foods that help them meet their nutritional needs.
The omega-3 long-chain polyunsaturated fatty acids (n-3 LCPUFAs) are a particularly important group of organic nutrients that animals need for both early life and reproduction. The availability of these fats can be an important determinant of a consumer's fitness, and affect the evolution of both dietarv and metabolic traits. Organisms in oceans are rich in the n-3 LCPUFAs docosahexaenoic acid (DHA; 22:6n-3) and eicosapentaenoic acid (EPA; 20:5n03), as well as alpha linolenic acid (ALA; 18:3n-3) their n-3 precursor. In contrast,
freshwater primarv producers and consumer typically contain only PA and ALA. This stark nutritional contrast between ecosystems present a significant challenge tor animals expanding their range into treshwater ecosystems, presenting an opportunity tor adaptation. Animals can adapt to a novel nutritional distribution of resource: through different combinations or metabolic traits and behavioral traits.

This project examined how fish from DHA-rich oceans have changed their diet and/ or metabolic synthesis capacity when establishing in freshwaters. In freshwater habitats, we might expected fish to have better ability to store and/or synthesize n-3 LCPUrAs. Functional fatty acid desaturase gene 2 (FADS2) is a key gene in involved in the synthesis of ALA to both EPA and DHA. FADS2 gene duplication is associated with an increased rates of LCPUFA synthesis. Behavioral dietary traits (i.e. eating prey richer in n-3 LCPUFA) associated with the acquisition of n-3 LCPUFA might also evolve in nutritionally-poor freshwaters.

We studied how populations from multiple populations of threespine stickleback (Gasterosteus aculeatus) throughout Europe from multiple geneticallv- and ecologicallv-differentiated populations have evolved the ability to survive in freshwaters. Our obiectives were to understand: 1) Is there evidence of population-specific diet variation in the wild? 2) Is there evidence of population-specific variation in FADS2 copy numbers in the wild and DHA synthesis ability in captivity on controlled diets? 3) Does population-specific diet and/or metabolic variation lead to variation in performance in terms of growth, condition, and survival?
During the project, the ER successfully established how behavioral and metabolic traits allow stickleback to regulate their n-3 LCPUFA and maintain performance in the face of variable nutritional quality. The ER assessed FADS copy numbers and diet in multiple treshwater populations of Threespine sticklebacks in the wild in fall 2021 and then bred multiple populations of sticklebacks in spring 2022, and raised them under experimental conditions on diets varying in n-3 LCPUFA content through spring 2023. Overall, 1) we found wide variation in Fads2 copy numbers and diet in wild freshwater sampled across Europe, but little variation in n-3 LCPUFA phenotypes in the wild. Copy numbers were generally related to time of freshwater establishment, whereby populations that established earlier in freshwater typically had higher copy numbers compared more recently-established populations. 2) We also found evidence of population-specific metabolic variation under common-garden conditions of contrasting food quality. When raised under common-garden conditions on diets with or without n-3 LCPUFA supplementation, populations that varied in copy number also varied in their n-3 LCPUFA synthesis and retention abilitv. Populations that established earlier in freshwaters and had higher cop numbers had higher n-3 LCPUFA content in both dietarv treatments relative to more recentlv established freshwater populations with lower FADS2 copy numbers. 3) We found that all populations grew more and were in better condition when supplemented with n-3 LCPUFA and that differences in condition between control and supplemented treatments tended to be greater in those with lower copy numbers and (more recent) marine ancestry. Mortality was also higher in populations of marine or more recent marine ancestry, especially in control treatments without n-3 LCPUFA supplementation. These results will be disseminated in publications that currently in preparation
These results demonstrate that the relationship between diet, FADS2 copy numbers, and n-3 LCPUFA content in wild sticklebacks are complex in that all wild fish were able to maintain similar n-3 LCPUFA content (during the non-breeding season) despite having variable diets and variable FADS2 copy numbers. However, we did find that copy numbers have increased in European stickleback populations that have been established in freshwaters for longer periods of time. Our experimental results reveal that when diet and environment are controlled, FADS2 copy numbers and dietary n-3 LPCUFA content both have strong effects on survival, growth, condition, and n-3 LCPUFA content of sticklebacks.
A stickleback clutch being artificially created
Stickleback stomach contents, including mayflies
Stickleback female pregnant with eggs
Field sampling in Chriesbach, Zurich, Switzerland
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