Abstract
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.
Highlights
Combining information from several cues simultaneously is likely to give a more reliable prediction of the upcoming conditions compared to responses to a single cue only (Bradshaw and Holzapfel, 2008)
We have shown that exposure to mismatching seasonal light and temperature cues can alter whole-animal performance and energetics and that the effects of light and temperature were at least partly mediated by thyroid hormone
Long days at cool temperatures, which can result from light at night—for example (Gaston, 2018), had a pronounced effect on thyroid hormone signalling, and can thereby influence locomotor performance and adenosine triphosphate (ATP) production scope
Summary
Combining information from several cues simultaneously is likely to give a more reliable prediction of the upcoming conditions compared to responses to a single cue only (Bradshaw and Holzapfel, 2008). In particular, is important in temperature acclimation of muscle function and metabolism Bacher, 2013) and in regulation of responses to photoperiod (Nakane and Yoshimura, 2019). It regulates mitochondrial bioenergetics (Harper and Seifert, 2008), and it can alter mitochondrial leak (State 4) respiration and efficiency via genomic and non-genomic mechanisms (Harper and Brand, 1993; Lanni et al, 2016). Thyroid hormone is a likely candidate that synchronizes responses to temperature and light
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