Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish ( Danio rerio)

Abstract

Background

Thyroid hormone (TH) is best known for its role in development in animals, and for its control of metabolic heat production (thermogenesis) during cold acclimation in mammals. It is unknown whether the regulatory role of TH in thermogenesis is derived in mammals, or whether TH also mediates thermal responses in earlier vertebrates. Ectothermic vertebrates show complex responses to temperature variation, but the mechanisms mediating these are poorly understood. The molecular mechanisms underpinning TH action are very similar across vertebrates, suggesting that TH may also regulate thermal responses in ectotherms. We therefore aimed to determine whether TH regulates thermal acclimation in the zebrafish ( Danio rerio). We induced hypothyroidism, followed by supplementation with 3,5-diiodothyronine (T ₂) or 3,5,3 ^′-triiodothyronine (T ₃) in zebrafish exposed to different chronic temperatures. We measured whole-animal responses (swimming performance and metabolic rates), tissue-specific regulatory enzyme activities, gene expression, and free levels of T ₂ and T ₃.

Results

We found that both T ₃ and the lesser-known T ₂, regulate thermal acclimation in an ectotherm. To our knowledge, this is the first such study to show this. Hypothyroid treatment impaired performance measures in cold-acclimated but not warm-acclimated individuals, whereas supplementation with both TH metabolites restored performance. TH could either induce or repress responses, depending on the actual temperature and thermal history of the animal.

Conclusions

The low sensitivity to TH at warm temperatures could mean that increasing temperatures (that is, global warming) will reduce the capacity of animals to regulate their physiologies to match demands. We suggest that the properties that underlie the role of TH in thermal acclimation (temperature sensitivity and metabolic control) may have predisposed this hormone for a regulatory role in the evolution of endothermy.