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Mismatched light and temperature cues disrupt locomotion and energetics via thyroid-dependent mechanisms.

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.

SUBMITTER: Le Roy A

PROVIDER: S-EPMC7287392 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Mismatched light and temperature cues disrupt locomotion and energetics via thyroid-dependent mechanisms.

Le Roy Amélie A Seebacher Frank F

Conservation physiology 20200611 1

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 (<i>Gambusia holbrooki</i>) 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 a ...[more]

PMID: 32547766

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Project description:BackgroundMaternal lifestyle factors, including smoking and increased body weight, increase risks of adult diseases such as metabolic syndrome and infertility. The fetal thyroid gland is essential for the control of fetal metabolic rate, cardiac output, and brain development. Altered fetal thyroid function may contribute to increased disease onset later in life. Here, we investigated the impact of maternal smoking and high maternal weight on human fetal thyroid function during the second trimester.MethodsThyroid glands and plasma were collected from fetuses electively terminated in the second trimester (normally progressing pregnancies). Plasma total triiodothyronine (T3) and total thyroxine (T4) were measured by solid-phase extraction-liquid chromatography-tandem mass spectrometry. Fetal plasma thyroid-stimulating hormone (TSH) levels were measured using a multiplex assay for human pituitary hormones. Histology and immunolocalization of thyroid developmental markers were examined in thyroid sections. Transcript levels of developmental, functional, apoptotic, and detoxification markers were measured by real-time PCR. Statistical analyses were performed using multivariate linear regression models with fetal age, sex, and maternal smoking or maternal body mass index (BMI) as covariates.ResultsMaternal smoking was associated with significant changes in fetal plasma T4 and TSH levels during the second trimester. Smoke-exposed thyroids had reduced thyroid GATA6 and NKX2-1 transcript levels and altered developmental trajectories for ESR2 and AHR transcript levels. Maternal BMI > 25 was associated with increased fetal thyroid weight, increased plasma TSH levels, and abnormal thyroid histology in female fetuses. Normal developmental changes in AHR and ESR1 transcript expression were also abolished in fetal thyroids from mothers with BMI > 25.ConclusionsFor the first time, we show that maternal smoking and high maternal BMI are associated with disturbed fetal thyroid gland development and endocrine function in a sex-specific manner during the second trimester. These findings suggest that predisposition to post-natal disease is mediated, in part, by altered fetal thyroid gland development.

Dataset Information

Mismatched light and temperature cues disrupt locomotion and energetics via thyroid-dependent mechanisms.

Publications

Mismatched light and temperature cues disrupt locomotion and energetics via thyroid-dependent mechanisms.

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