Developmental plasticity can match offspring phenotypes to environmental conditions experienced by parents. Such epigenetic modifications are advantageous when parental conditions anticipate offspring environments. Here we show firstly, that developmental plasticity manifests differently in males and females. Secondly, that under stable conditions, phenotypic responses (metabolism and locomotion) accumulate across several generations. Metabolic scope in males was greater at warmer test temperatures (26–36 °C) in offspring bred at warm temperatures (29–30 °C) compared to those bred at cooler temperatures (22–23 °C), lending support to the predictive adaptive hypothesis. However, this transgenerational matching was not established until the second (F2) generation. For other responses, e.g. swimming performance in females, phenotypes of offspring bred in different thermal environments were different in the first (F1) generation, but became more similar across three generations, implying canalization. Thirdly, when environments changed across generations, the grandparental environment affected offspring phenotypes. In females, the mode of the swimming thermal performance curve shifted to coincide with the grandparental rather than the parental or offspring developmental environments, and this lag in response may represent a cost of plasticity. These findings show that the effects of developmental plasticity differ between traits, and may be modulated by the different life histories of males and females.

Evolutionary theory predicts that intergenerational environmental fluctuations lead to transgenerational effects where offspring phenotypes are matched to conditions experienced by previous generations. However, in fluctuating environments, transgenerational effects can be detrimental by causing mismatches between ancestral and offspring environments. Acclimation in offspring could alleviate these negative effects. We determined whether the interaction between transgenerational effects and acclimation affects locomotor performance and dispersal in guppies (Poecilia reticulata). In a fully factorial experiment, we tested the interaction between ancestral (22 or 30°C for six to eight generations), acclimation (22 or 30°C for 4 weeks) and acute test temperatures (two to five temperatures across 18–34°C). We predicted that matching ancestral and acclimation temperatures to acute environmental temperature maximises physiological capacities (swimming performance [Ucrit] and metabolic enzyme activities), and dispersal in an artificial stream. Alternatively, when ancestral and acute temperatures were mismatched, we predicted that thermal acclimation compensates for this mismatch by shifting performance curves. Finally, we hypothesised that physiological capacities are positively related to dispersal. We measured dispersal as a combination of traits characterising the departure and transient phases of dispersal (time taken to leave the introductory pool, voluntary speed against the current, number of dispersal decisions taken) in an 8‐m artificial stream. As hypothesised, Ucrit was greatest when ancestral, acclimation and acute temperatures matched. Cold acclimation reduced the decrement in Ucrit resulting from a mismatch between ancestral and acute test temperatures. In both sexes, the interaction between ancestral and acclimation temperatures determined Ucrit, but not metabolic enzyme activities, and it affected the number of dispersal decisions in males only. Contrary to our hypothesis, physiological capacities did not constrain dispersal. Males were more likely to initiate dispersal when the acute temperatures mismatched their ancestral temperature. After initiating dispersal, males moved at a greater voluntary speed and made more dispersal decisions in environments matching their ancestral environment. Our findings imply that although the interaction between transgenerational effects and acclimation modulates locomotor capacities, these relationships do not necessarily translate to all ecologically relevant locomotor tasks. Instead, sex‐specific life‐history traits such as life span are more likely to influence dispersal, and males in particular may initiate dispersal to escape suboptimal conditions. A http://onlinelibrary.wiley.com/doi/10.1111/1365-2435.13105/suppinfo is available for this article.

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Animals integrate information from different environmental cues to maintain performance across environmental gradients. Increasing average temperature and variability induced by climate change can lead to mismatches between seasonal cues. We used mosquitofish (Gambusia holbrooki) to test the hypotheses that mismatches between seasonal temperature and light regimes (short days and warm temperature and vice versa) decrease swimming performance, metabolic rates and mitochondrial efficiency and that the responses to light and temperature are mediated by thyroid hormone. We show that day length influenced thermal acclimation of swimming performance through thyroid-dependent mechanisms. Oxygen consumption rates were influenced by acclimation temperature and thyroid hormone. Mitochondrial substrate oxidation rates (state three rates) were modified by the interaction between temperature and day length, and mitochondrial efficiency (P/O ratios) increased with warm acclimation. Using P/O ratios to calibrate metabolic (oxygen consumption) scope showed that oxygen consumption did not predict adenosine triphosphate (ATP) production. Unlike oxygen consumption, ATP production was influenced by day length in a thyroid-dependent manner. Our data indicate that oxygen consumption alone should not be used as a predictor of ATP production. Overall, the effects of thyroid hormone on locomotion and energetics were reversed by mismatches such as warm temperatures on short days. We predict that mid to high latitudes in North America and Asia will be particularly affected by mismatches as a result of high seasonality and predicted warming over the next 50 years.

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