The ecological function of thyroid hormones

Abstract

Thyroid hormones (TH) are central hormonal regulators, orchestrating gene expression and complex biological processes vital for growth and reproduction in variable environments by triggering specific developmental processes in response to external cues. TH serve distinct roles in different species: inducing metamorphosis in amphibians or teleost fishes, governing metabolic processes in mammals, and acting as effectors of seasonality. These multifaceted roles raise questions about the underlying mechanisms of TH action. Recent evidence suggests a shared ecological role of TH across vertebrates, potentially extending to a significant portion of bilaterian species. According to this model, TH ensure that ontogenetic transitions align with environmental conditions, particularly in terms of energy expenditure, helping animals to match their ontogenetic transition with available resources. This alignment spans post-embryonic developmental transitions common to all vertebrates and more subtle adjustments during seasonal changes. The underlying logic of TH function is to synchronize transitions with the environment. This review briefly outlines the fundamental mechanisms of thyroid signalling and shows various ways in which animals use this hormonal system in natural environments. Lastly, we propose a model linking TH signalling, environmental conditions, ontogenetic trajectory and metabolism. This article is part of the theme issue 'Endocrine responses to environmental variation: conceptual approaches and recent developments'.

Keywords: adaptation; ecology; hormone function; thyroid hormones.

Figure 1.

Summary diagram of the hypothalamo pituitary thyroid axis (HPT; light blue), and hypothalamo pituitary adrenal/interrenal axis (HPA/HPI; pink) in vertebrates. Special emphasis is put on the differences between the mode of hypotalamic peptide delivery to the adenohyphysis (green inset, light grey lobe) in mammals (left) versus fishes (right). See text for details. TRH: thyrotropin-releasing hormone; CRH: corticotropin releasing hormone; TSH: thyroid-stimulating hormone; ACTH: adrenocorticotropic hormone; GR: glucocorticoid receptor; TR: thyroid hormone receptor, RXR: retinoid X receptor.

Figure 2.

Tuning of metabolism, energy demands, and environment through the modulation of TH levels: illustration of some of the main case-studies mentioned in the text. Differences in TH levels across species or populations have been found to tune organisms to: differences in food availability across environments (top left, Gasterosteus aculeatus); differences in sea anemone hosts (top right, Amphiprion percula); adaptation to high temperatures (bottom left, Vulpes zerda); and adaptation to cold temperatures (bottom right). Tuned TH levels are here represented by a slider dial (left, low; right, high).

Figure 3.

TH levels coordinate the metamorphosis of marine fishes with their life history and ecological transitions. (a) A peak in TH levels is associated with the metamorphosis of pelagic fish larvae, often as they transition from the open ocean to reefs and coastal environments. While a natural range of TH levels is conducive to proper development and successful metamorphosis, large deviations in either direction lead to developmental defects and larvae/juveniles maladapted to their new environment. (b) Shifts in the maturity of coral reef fish entering the reef habitat and implication for the peak of TH and TR expression with respect to their life history. In the surgeonfish Acanthurus triostegus, the falling limb of the peak in TH and TR expression coincides with the crossing of the reef crest, timing metamorphosis with the imminent ecological change. In other species, different life stages are seen crossing the reef: already metamorphosized juveniles in the case of Rhinecanthus aculeatus, or non-metamorphosed larvae for the carapid Carapus homei. Other species, such as Pterapogon kauderni complete their entire lifecycle within the lagoon, and therefore do not have pelagic stage at all: they are considered as ‘apelagic’ species and may be reminiscent of direct developing frogs.

Figure 4.

A general model for the ecological role of TH. Organisms (here, a developing surgeonfish) can maintain optimal fitness while navigating ontogenetic and ecological changes, with often drastically different physiological demands, by tuning their TH levels. Blue path: optimal progression in TH levels throughout early development (here, metamorphosis). (a) Detuning between the organism and the environment owing to precocious changes in TH levels. (b) Detuning between the organism and the environment owing to a failure in changing the TH levels (e.g. owing to endocrine disruptors in the environment). (c) Local acclimation: the organism fine tunes its TH levels (here, slight increase) to better match its environment and thus improve its fitness. The thick dotted grey line indicates maintenance of suboptimal fitness levels in the absence of TH tuning. (d) Detuning between the organism and the environment owing to a sudden change in environmental conditions (e.g. climate change). The thick dotted grey line indicates maintenance of high fitness at the given TH level in the absence of ecological changes. Events marked with an asterisk are illustrated as happening at the juvenile and adult stages, but may occur at any timepoint throughout the life cycle.