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Transcriptional mechanisms underlying life-history responses to climate change in the three-spined stickleback.

ABSTRACT: Phenotypic plasticity, the ability of an organism to express different phenotypes depending on the environment, provides an important mechanism by which an animal population can persist under rapid climate change. We experimentally tested both life-history and transcriptional responses of an ecological model species, the three-spined stickleback, to warm acclimation at the southern edge of its European range. We explored cross-environment genetic correlations of key life-history traits in male sticklebacks exposed to long-term temperature changes to examine whether the plasticity pattern was variable among genotypes by using a character-state approach. We also studied gene expression plasticity by analysing both whole-transcriptome and candidate gene expression in brain and liver. Male sticklebacks that developed under warmer conditions during winter were smaller in size and invested less in nuptial coloration at the beginning of the breeding season, showing similar responses across different genotypes. The lack of genetic variation in life-history responses may limit any future evolution of the thermal reaction norm in the study population. After long-term exposure to increased winter temperatures, genes responsible for several metabolic and oxidation-reduction processes were upregulated, and some hormone genes involved in growth and reproduction were downregulated in the brain. In the liver, there was no significantly represented gene ontology by the differentially expressed genes. Since a higher temperature leads to a higher resting metabolic rate, living in warmer environments may incur higher energetic costs for ectotherms to maintain cellular homoeostasis, resulting in negative consequences for life-history traits. The expression of genes related to metabolism, cellular homoeostasis and regulatory signalling may underlie temperature-induced changes in life history.

SUBMITTER: Kim SY

PROVIDER: S-EPMC5511362 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Transcriptional mechanisms underlying life-history responses to climate change in the three-spined stickleback.

Kim Sin-Yeon SY Costa Maria M MM Esteve-Codina Anna A Velando Alberto A

Evolutionary applications 20170515 7

Phenotypic plasticity, the ability of an organism to express different phenotypes depending on the environment, provides an important mechanism by which an animal population can persist under rapid climate change. We experimentally tested both life-history and transcriptional responses of an ecological model species, the three-spined stickleback, to warm acclimation at the southern edge of its European range. We explored cross-environment genetic correlations of key life-history traits in male s ...[more]

PMID: 28717391

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Project description:BackgroundConditions experienced by a female during early life may affect her reproductive strategies and maternal investment later in life. This effect of early environmental conditions is a potentially important mechanism by which animals can compensate for the negative impacts of climate change. In this study, we experimentally tested whether three-spined sticklebacks (Gasterosteus aculeatus) change their maternal strategy according to environmental temperatures experienced earlier in life. We studied maternal investment from a life-history perspective because females are expected to adjust their reproductive strategy in relation to their current and future reproductive returns as well as offspring fitness.ResultsF1 families were reared in control and elevated winter temperatures and their reproductive trajectories were studied when returned to common conditions. Females that had experienced the warm winter treatment (n = 141) had a lower fecundity and reduced breeding and total lifespan compared to the control individuals (n = 159). Whereas the control females tended to produce their heaviest and largest clutches in their first reproductive attempt, the warm-acclimated females invested less in their first clutch, but then produced increasingly heavy clutches over the course of the breeding season. Egg mass increased with clutch number at a similar rate in the two groups. The warm-acclimated females increased the investment of carotenoids in the first and last clutches of the season. Thus, any transgenerational effects of the maternal thermal environment on offspring phenotype may be mediated by the allocation of antioxidants into eggs but not by egg size.ConclusionsOur results indicate that conditions experienced by females during juvenile life have a profound effect on life-time maternal reproductive strategies. The temperature-induced changes in maternal strategy may be due to constraints imposed by the higher energetic costs of a warm environment, but it is possible that they allow the offspring to compensate for higher energetic costs and damage when they face the same thermal stress as did their mothers.

Project description:ContextAn increasing concern in the face of human expansion throughout natural habitats is whether animal populations can respond adaptively when confronted with challenges like environmental change and novelty. Behavioural flexibility is an important factor in estimating the adaptive potential of both individuals and populations, and predicting the degree to which they can cope with change.Study designThis study on the three-spined stickleback (Gasterosteus aculeatus) is an empiric illustration of the degree of behavioural variation that can emerge between semi-natural systems within only a single generation. Wild-caught adult sticklebacks (P, N = 400) were randomly distributed in equal densities over 20 standardized semi-natural environments (ponds), and one year later offspring (F1, N = 652) were presented with repeated behavioural assays. Individuals were challenged to reach a food source through a novel transparent obstacle, during which exploration, activity, foraging, sociability and wall-biting behaviours were recorded through video observation. We found that coping responses of individuals from the first generation to this unfamiliar foraging challenge were related to even relatively small, naturally diversified variation in developmental environment. All measured behaviours were correlated with each other. Especially exploration, sociability and wall-biting were found to differ significantly between ponds. These differences could not be explained by stickleback density or the turbidity of the water.FindingsOur findings show that a) differences in early-life environment appear to affect stickleback feeding behaviour later in life; b) this is the case even when the environmental differences are only small, within natural parameters and diversified gradually; and c) effects are present despite semi-natural conditions that fluctuate during the year. Therefore, in behaviourally plastic animals like the stickleback, the adaptive response to human-induced habitat disturbance may occur rapidly (within one generation) and vary strongly based on the system's (starting) conditions. This has important implications for the variability in animal behaviour, which may be much larger than expected from studying laboratory systems, as well as for the validity of predictions of population responses to change.

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Transcriptional mechanisms underlying life-history responses to climate change in the three-spined stickleback.

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Transcriptional mechanisms underlying life-history responses to climate change in the three-spined stickleback.

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