Fit and fatty freshwater fish: contrasting polyunsaturated fatty acid phenotypes between hybridizing stickleback lineages

Abstract

Long‐chain polyunsaturated fatty acids are biologically important lipids that are unevenly distributed between and throughout environments. This heterogeneity can affect the evolution of metabolic processes, as populations adapt to the resource landscape that they encounter. Here, we compare fatty acid phenotypes of stickleback over two time scales of evolutionary divergence: between two lineages with different metabolic capacities for fatty acid synthesis (i.e. different copy number of the fatty acid desaturase gene; FADS2) that independently colonized European freshwaters during the Pleistocene and Holocene; and between two ecotypes within each lineage that have diverged more recently (~150 years) in different habitats (i.e. lake and stream). We measured fatty acid profiles of wild‐caught and lab‐reared fish for each lineage and ecotype combination after rearing lab fish on a diet deficient in omega‐3 long‐chain polyunsaturated fatty acids. Since these lineages hybridize in nature, we also measured profiles of lab‐reared hybrids and backcrosses raised on the same deficient diet. Wild fish showed strong compositional differences in fatty acids between habitats, lineages and sexes. Common garden fish had generally lower polyunsaturated fatty acid levels than wild fish, and females had lower omega‐6:omega‐3 than males. Fish from the lineage with fewer FADS2 copies also had lower levels of docosahexaenoic acid. Overall, we document divergence in fatty acid phenotypes between stickleback lineages with different histories of freshwater colonization, and between ecotypes in the early stages of adaptive population divergence.

Special issue: Questioning the roles of resources nutritional quality in ecology

“…Last, two articles of the Special issue lie at the interface of the dominant cluster (i.e. aquatic ecosystem/stoichiometry‐lipids/trophodynamics‐fitness) and the cluster including evolutionary–reproduction purposes (Hudson et al 2022, Leal et al 2022).…”

“…It is also interesting to note that less than 20% of all published studies, explicitly refer to evolutionary issues, while many interactions between species and the quality of their resources have been shaped on an evolutionary time scale. In this special issue, Hudson et al (2022) tackle such question through the analysis of different fish lineages and their metabolic capacities of PUFA synthesis, showing how divergences between lineages depend on the history of freshwater colonization of the studied species. Finally, since some elements/molecules used for defining resources quality can be typical from some ecosystems or resource types, such resources quality parameters can be consequently used as ecosystem tracers (Majdi et al 2018).…”

“…The articles published in this special issue are well representative of these trends since one third of the published articles question resources quality through the consideration of resources elemental content (Chouvelon et al 2022, Lowman et al 2022, Sentis et al 2022), while a second third focuses on resources macro‐nutrient contents, alone (Le Gall et al 2022, Zaguri et al 2022) or in association with fatty acids (van Deurs et al 2022). Finally, three articles specifically focus on fatty acids/lipids (Hudson et al 2022, Leal et al 2022, Mathieu‐Resuge et al 2022).…”

“…‐ As generally observed in ecosystem ecology, evolutionary questions are still too rarely explicitly tested in trophic ecology investigations. Despite a large array of studies have observed and discussed the evolutionary tenets at play behind the selection of consumers nutritional requirements (see for example Hudson et al 2022 in this issue), the inclusion of such research questions in the general understanding of ecosystem functioning remains limited.‐ Finally, Lowman et al (2022) illustrate that the potential nutritional quality of basal producers can be significantly altered by global warming. In the context or the current global changes and considering the multiple stressors organisms are exposed to, understanding the causes and the consequences of changes in basal resource quality in a multistressor context (concomitant changes in temperature, nutrient and water availability, presence of pollutants …) is an urgent need, as much in terms of prediction of future ecosystem trajectories as in terms of goods and services provision by nature for humanity.…”

“…-As generally observed in ecosystem ecology, evolutionary questions are still too rarely explicitly tested in trophic ecology investigations. Despite a large array of studies have observed and discussed the evolutionary tenets at play behind the selection of consumers nutritional requirements (see for example Hudson et al 2022 in this issue), the inclusion of such research questions in the general understanding of ecosystem functioning remains limited. -Finally, Lowman et al (2022) illustrate that the potential nutritional quality of basal producers can be significantly altered by global warming.…”