Regulation of thermal acclimation varies between generations of the short‐lived mosquitofish that developed in different environmental conditions

Abstract

Summary1. Environmental variability and perturbations can influence population persistence. It is therefore important to understand whether and how animals can compensate for environmental variability and thereby increase resilience of natural populations. Evolutionary theory predicts that in fluctuating environments, selection should favour developmental modifiers that reduce phenotypic expression of genetic variation. The expected result is that phenotypes are buffered from environmental variation across generations. 2. Our aim was to determine whether phenotypes of mosquitofish (Gambusia holbrooki) remain stable across generations in which individuals were born into different thermal environments. We predicted that the spring generation (cool environment) would acclimate by increasing the concentration of regulatory transcription factor mRNA and activities of rate-limiting enzymes (hierarchical regulation) to compensate for the negative thermodynamic effects of lower temperatures on metabolic and locomotor performance. In contrast, the summer-born generation (warm environment) would show less capacity for acclimation and hierarchical regulation. 3. We show that fish from both generations acclimated, but that there were significant differences in the phenotypic consequences of acclimation. The overall result was that burst performance, metabolic scope, and the activities of cytochrome c oxidase and lactate dehydrogenase were buffered from environmental change and did not differ between spring and summer fish at their natural water temperatures of 15°C and 25°C, respectively. However, there were differences between generations in sustained swimming performance and citrate synthase activity. 4. We used metabolic control analysis to show that modes of regulation of metabolic scope and locomotor performance differed between generations. Spring-born fish relied to a greater extent on rate-limiting enzymes and transcriptional regulator (PGC-1a and b) mRNA concentrations than summer-born fish. 5. We suggest that developmental modifiers are favoured in fluctuating environments to maximize phenotypic fitness of each generation. We show that the interaction between developmental and reversible acclimation can increase the resilience of physiological performance in a natural population to climate variation.

The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures inXenopus laevisDaudin

“…Alternatively, there may be a relative increase in the ATP allocated to muscle myosin ATPase or SERCA activity during winter. Hence, if the capacity for metabolic cold acclimation is limited, as it is likely to be (Seebacher et al, 2013), there may be an allocation trade-off (Angilletta et al, 2003). Interestingly, burst speed was higher at the lower 15°C test temperature in our Xenopus acclimated to low temperatures, but this was not paralleled by acclimation in muscle force production, power output or oxygen consumption.…”

Immune-Challenged Fish Up-Regulate Their Metabolic Scope to Support Locomotion

“…Hence, if metabolic maintenance costs increase, the resultant reduction in metabolic scope can create an allocation trade-off [29]. Decreases in the amount of energy available to other activities may, however, be counterbalanced physiologically through an increase in the capacities of mitochondrial metabolic pathways [27, 30, 31]. While such compensatory responses may abolish ATP shortages, trade-offs may still persist if investment in multiple aerobically-challenging activities depletes storages of ingested chemical energy with detrimental consequences for body condition.…”

UV‐B radiation interacts with temperature to determine animal performance

“…Developmental conditions can affect epigenetic regulation and modify DNA and histone molecules, thereby changing gene expression programs and phenotypes later in life (Klose & Bird 2006;Greer & Shi 2012). In addition, developmental conditions can also modulate the capacity for reversible acclimation (Scott & Johnston 2012;Seebacher, Beaman & Little 2014). Summer animals have higher antioxidant enzyme activities, lower damage and therefore better performance when acclimated close to the temperature of their developmental environment.…”