Prickly postglacial pioneers: freshwater plankton community composition influences fatty acid desaturase (FADS2) copy number in Southern Greenland threespine sticklebacks

The adaptation of marine fish to freshwater environments includes
prodigious examples of rapid evolution. Given the scarcity of ω-3
long-chain polyunsaturated fatty acids (LC-PUFA) in freshwater, we expect
selection to be strong on fish transitioning to freshwater habitats and
yet the underlying ecological causes of genomic and phenotypic
differentiation are poorly understood for traits associated with lipid
content and composition. Threespine stickleback (Gasterosteus aculeatus)
have repeatedly colonized, and adapted to, freshwater habitats across the
northern hemisphere. These freshwater populations often show elevated copy
number of the fatty acid desaturase 2 gene (FADS2), which increases the
biosynthetic capacity of LC-PUFA. The starkly lower content of LC-PUFA in
freshwater compared to marine prey, especially docosahexaenoic acid (DHA),
likely imposes strong positive selection on freshwater fish for either
increased biosynthesis or greater dietary acquisition of LC-PUFA. The
recently colonized and relatively undisturbed threespine stickleback
populations in postglacial coastal lakes of Southern Greenland offer an
exceptional opportunity to study how variation in the copy number of FADS2
is related to abiotic and biotic conditions of lakes and their
morphometry. As expected, given its position on the stickleback X
chromosome, we found strong sexual dimorphism in FADS2 copy number in all
populations (19 freshwater, 1 marine, and 1 brackish), and an increased
dimorphism in some freshwater populations. We also found that FADS2 copy
number was negatively correlated, for both males and females, with the
abundance of copepods, which are a DHA-rich food source in the zooplankton
community. Overall, our results suggest that the prey community context of
lakes might influence the process of metabolic adaptation of marine fish
colonizing freshwater ecosystems.

海水鱼类适应淡水环境的过程，蕴含着大量快速演化的典型案例。
鉴于淡水环境中ω-3长链多不饱和脂肪酸（LC-PUFA）稀缺，我们推测向淡水生境过渡的鱼类会面临较强的选择压力，但目前学界对与脂质含量及组成相关性状的基因组和表型分化的潜在生态成因仍知之甚少。
三刺棘鱼（Gasterosteus aculeatus）已在北半球多地反复拓殖并适应了淡水生境。
这类淡水种群通常表现出脂肪酸去饱和酶2基因（FADS2）的拷贝数升高，该基因可提升LC-PUFA的生物合成能力。
与海洋猎物相比，淡水环境中的LC-PUFA含量显著更低，尤其是二十二碳六烯酸（DHA），这可能会对淡水鱼类施加强烈的正向选择压力，促使其要么提升LC-PUFA的生物合成能力，要么通过饮食更高效地获取这类物质。
格陵兰南部冰后沿海湖泊中近期拓殖且相对未受干扰的三刺棘鱼种群，为研究FADS2拷贝数变异与湖泊非生物、生物条件及其形态测量特征之间的关联提供了绝佳契机。
正如预期，鉴于该基因位于棘鱼的X染色体上，我们在所有种群（19个淡水种群、1个海洋种群及1个半咸水种群）中均发现FADS2拷贝数存在显著的雌雄二态性，且部分淡水种群的这种二态性有所增强。
我们还发现，无论雄性还是雌性，FADS2拷贝数均与桡足类的丰度呈负相关——桡足类是浮游动物群落中富含DHA的食物来源。
总体而言，本研究结果表明，湖泊的猎物群落背景可能会影响海水鱼类拓殖淡水生态系统后的代谢适应过程。