Parents exposed to warming produce offspring lower in weight and condition.

The parental environment can alter offspring phenotypes via the transfer of non-genetic information. Parental effects may be viewed as an extension of (within-generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non-genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish (Acanthochromis polyacanthus) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present-day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present-day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within-generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change.

Sex- and time-specific parental effects of warming on reproduction and offspring quality in a coral reef fish.

Global warming can disrupt reproduction or lead to fewer and poorer quality offspring, owing to the thermally sensitive nature of reproductive physiology. However, phenotypic plasticity may enable some animals to adjust the thermal sensitivity of reproduction to maintain performance in warmer conditions. Whether elevated temperature affects reproduction may depend on the timing of exposure to warming and the sex of the parent exposed. We exposed male and female coral reef damselfish (Acanthochromis polyacanthus) during development, reproduction or both life stages to an elevated temperature (+1.5°C) consistent with projected ocean warming and measured reproductive output and newly hatched offspring performance relative to pairs reared in a present-day control temperature. We found female development in elevated temperature increased the probability of breeding, but reproduction ceased if warming continued to the reproductive stage, irrespective of the male's developmental experience. Females that developed in warmer conditions, but reproduced in control conditions, also produced larger eggs and hatchlings with greater yolk reserves. By contrast, male development or pairs reproducing in higher temperature produced fewer and poorer quality offspring. Such changes may be due to alterations in sex hormones or an endocrine stress response. In nature, this could mean female fish developing during a marine heatwave may have enhanced reproduction and produce higher quality offspring compared with females developing in a year of usual thermal conditions. However, male development during a heatwave would likely result in reduced reproductive output. Furthermore, the lack of reproduction from an average increase in temperature could lead to population decline. Our results demonstrate how the timing of exposure differentially influences females and males and how this translates to effects on reproduction and population sustainability in a warming world.

Developmental effects of heatwave conditions on the early life stages of a coral reef fish.

Marine heatwaves, which are increasing in frequency, duration and intensity owing to climate change, are an imminent threat to marine ecosystems. On coral reefs, heatwave conditions often coincide with periods of peak recruitment of juvenile fishes and exposure to elevated temperature may affect their development. However, whether differences in the duration of high temperature exposure have effects on individual performance is unknown. We exposed juvenile spiny damselfish, Acanthochromis polyacanthus, to increasing lengths of time (3, 7, 30 and 108 days post-hatching) of elevated temperature (+2°C). After 108 days, we measured escape performance at present-day control and elevated temperatures, standard length, mass and critical thermal maximum. Using a Bayesian approach, we show that 30 days or more exposure to +2°C leads to improved escape performance, irrespective of performance temperature, possibly owing to developmental effects of high temperature on muscle development and/or anaerobic metabolism. Continued exposure to elevated temperature for 108 days caused a reduction in body size compared with the control, but not in fish exposed to high temperature for 30 days or less. By contrast, exposure to elevated temperatures for any length of time had no effect on critical thermal maximum, which, combined with previous work, suggests a short-term physiological constraint of ∼37°C in this species. Our study shows that extended exposure to increased temperature can affect the development of juvenile fishes, with potential immediate and future consequences for individual performance.