Metabolic programming mediated by an essential fatty acid alters body composition and survival skills of a marine fish

Abstract

ResearchCite this article: Fuiman LA, Perez KO. 2015 Metabolic programming mediated by an essential fatty acid alters body composition and survival skills of a marine fish. Proc. R. Soc. Metabolic programming occurs when variations in nutrition during a specific developmental window result in long-term metabolic effects. It has been studied almost exclusively in humans and other mammals but never in an ecological context. Here, we report metabolic programming and its functional consequences in a marine fish, red drum. We demonstrate that maternal provisioning of eggs with an essential fatty acid, docosahexaenoic acid (DHA), varies with DHA content of the maternal diet. When offspring are reared on a DHA-replete diet, whole-body DHA content of offspring depends upon the amount of DHA that was in the egg. We further demonstrate that whole-body DHA content is correlated with traits related to offspring fitness (escape responses, routine swimming, growth, and survival). DHA content of red drum eggs produced in nature is in the range where the effects of metabolic programming are most pronounced. Our findings indicate that during a brief developmental window, DHA plays a role in establishing the metabolic capacity for its own uptake or storage, with protracted and possibly permanent effects on ecologically important survival skills of individuals and important implications for dynamics of populations and food webs.

Fatty acids differentiate consumers despite variation within prey fatty acid profiles

“…Maternal influences on the lipid composition of eggs have been documented to reflect dietary shifts to a relatively large degree (Bell, Farndale, Bruce, Navas, & Carillo, 1997;Cahu, Cuzon, & Quazuguel, 1995;Fernández-Palacios et al, 1995). Differences in maternal dietary fatty acid profiles have elicited differential fatty acid metabolism, survival, and antipredator responses in offspring (Czesny & Dabrowski, 1998;Fuiman & Ojanguren, 2011;Fuiman & Perez, 2015). This would indicate that for steelhead trout, maternal diets and provisions to embryos could alter progeny survival through changes in fatty acid allocations.…”

Fatty acids in an iteroparous fish: variable complexity, identity, and phenotypic correlates

“…However, the vast majority of studies have focused on the influence of diet on fatty acid identity and have not considered the importance of fatty acid complexity (Czesny and Dabrowski 1998;Moles et al 2008;Fuiman and Perez 2015). This study is one of the first to move beyond the identity of fatty acids to consider the importance of fatty acid complexity to indicators of egg quality in a freshwater fish.…”

“…Few studies, however, have progressed beyond examining the role D r a f t of one or a few specific fatty acids to assess how fatty acid complexity may correspond to individual performance. Most iteroparous species allocate fatty acids to reproduction by mobilizing compounds from somatic stores well before spawning occurs (Henderson 2000), and this allocation may be preferential for specific fatty acids (Jeong et al 2002) with implications for larval performance long after hatching (Fuiman and Perez 2015). Environmental effects, including temperature, may alter this allocation process in both somatic and gonadal tissues (Knipprath and Mead 1968;Alhazzaa et al 2013;Feiner et al 2016a), thereby influencing the composition and complexity of eggs and potentially their quality.…”

“…For example, docosahexaenoic acid (22:6n-3; DHA) concentrations in eggs have been positively linked to egg survival, hatching success, and larval mobility (Czesny and Dabrowski 1998;Tocher 2003;Fuiman and Ojanguren 2011;Fuiman and Perez 2015) and are generally important to neurological development in fishes (Tocher 2010). High levels of eicosapentaenoic acid (20:5n-3; EPA) or increased ratios of EPA to DHA or arachidonic acid (20:4n-6; AA) are related to regulation of inflammatory responses in animals (Calder 2001) and may depress larval function in fish (Henrotte et al 2010).…”

Egg Boon Fatty Acids Reveal Effects of a Climatic Event on a Marine Food Web

“…Such imbalances, especially in DHA, EPA, and ARA, can also affect future ecological Dashed arrows represent an example timeline beginning with normal rainfall (SPI-3) for January (lower left panel), resulting bay salinity in May, and abundance of brown shrimp in offshore trawls 12 months later, PC3 score for the egg boon 5 months later, and corresponding PDSI 20 months before the middle of the spawning season. performance of larvae, even when the larval diet is adequate (metabolic programming; Ojanguren 2011, Fuiman andPerez 2015). For example, the duration of escape responses of red drum larvae (larval total length = 9-10 mm) averaged 44% longer for larvae that came from eggs containing 15% DHA compared with larvae from eggs containing 10% DHA, and variations in the amounts of ARA and other fatty acids were similarly associated with other escape performance traits (Fuiman and Ojanguren 2011).…”