The Multi-Level Regulation of Clownfish Metamorphosis Through Thyroid Hormones

Roux, Natacha; Miura, Saori; Dussenne, Mélanie; Tara, Yuki; Lee, Shu-Hua; Bernard, Simon; Reynaud, Mathieu; Salis, Pauline; Barua, Agneesh; Boulahtouf, Abdelhay; Balaguer, Patrick; Gauthier, Karine; Lecchini, David; Gibert, Yann; Laudet, Vincent

doi:10.2139/ssrn.4137691

Cited by 6 publications

(23 citation statements)

References 3 publications

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“…There is some variation in this canonical pathway, and during metamorphosis in amphibians and fish, for example, the stress-induced corticotropin-releasing hormone controls thyroid-stimulating hormone, and metamorphosis is closely linked to environmental factors such as tadpole density [51]. During development in anemone fish ( Amphiprion ocellaris ), thyroid hormones orchestrate metabolism, morphological changes and behaviour to match juveniles to their ecological context [52]. Beyond metamorphosis, thyroid hormone more generally regulates development, at least in chordates [53].…”

Section: Actions and Interactions Between Thyroid Hormone And Dnmt3mentioning

confidence: 99%

Thyroid hormone links environmental signals to DNA methylation

Seebacher,

Little

2024

Phil. Trans. R. Soc. B

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Environmental conditions experienced within and across generations can impact individual phenotypes via so-called ‘epigenetic' processes. Here we suggest that endocrine signalling acts as a ‘sensor' linking environmental inputs to epigenetic modifications. We focus on thyroid hormone signalling and DNA methylation, but other mechanisms are likely to act in a similar manner. DNA methylation is one of the most important epigenetic mechanisms, which alters gene expression patterns by methylating cytosine bases via DNA methyltransferase enzymes. Thyroid hormone is mechanistically linked to DNA methylation, at least partly by regulating the activity of DNA methyltransferase 3a, which is the principal enzyme that mediates epigenetic responses to environmental change. Thyroid signalling is sensitive to natural and anthropogenic environmental impacts (e.g. light, temperature, endocrine-disrupting pollution), and here we propose that thyroid hormone acts as an environmental sensor to mediate epigenetic modifications. The nexus between thyroid hormone signalling and DNA methylation can integrate multiple environmental signals to modify phenotypes, and coordinate phenotypic plasticity at different time scales, such as within and across generations. These dynamics can have wide-ranging effects on health and fitness of animals, because they influence the time course of phenotypic adjustments and potentially the range of environmental stimuli that can elicit epigenetic responses. This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.

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Section: Actions and Interactions Between Thyroid Hormone And Dnmt3mentioning

confidence: 99%

Thyroid hormone links environmental signals to DNA methylation

Seebacher,

Little

2024

Phil. Trans. R. Soc. B

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“…Additionally, we have shown differences in TH levels between distinct ecotypes of anemonefish, which are associated with metabolic differences, although we still do not know if there is a link with energy expenditure [20,21]. The anemonefish Amphiprion percula can live in association with different species of sea anemones (figure 2 b ).…”

Section: Thyroid Hormones and Ecologymentioning

confidence: 99%

“…When the larvae are ready to settle on a reef, their metamorphosis is triggered [2,88]. Studies on surgeonfish have shown that the peak of TH is initiated early on, while the larvae are still in the open ocean, and that the entry in the reef corresponds to the falling limb of the TH peak [21,89,90] (figure 3). The triggers initiating metamorphosis are still not understood.…”

Section: Salinity Acclimationmentioning

confidence: 99%

“…With the effects of TH we described so far, it is no surprise that TH impact the activity of lipid metabolism enzymes, therefore influencing energy availability in the transforming larvae [92]. Furthermore, transcriptomic analysis of larval development in several fish species have revealed differences in transcript levels of genes involved in metabolic pathways, namely glycolysis, the citric acid cycle, and fatty acid β-oxidation [21,93]. In anemonefish, metamorphosis marks the shift between anaerobic and aerobic metabolism and TH are involved in the regulation of this transition [21].…”

Section: Salinity Acclimationmentioning

confidence: 99%

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The ecological function of thyroid hormones

Zwahlen,

Gairin,

Vianello

et al. 2024

Phil. Trans. R. Soc. B

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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’.

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“…Metamorphosis is a postembryonic developmental transformation process and is crucial for maintaining adult reef fish populations that are particularly sensitive to the anthropogenic stressors affecting coral reefs (McMenamin and Parichy 2013; Lecchini et al 2017). During the period of metamorphosis, the larvae undergo complex morphological changes and remarkable growth that transform them into juveniles within a short time (Pérez‐Domínguez and Holt 2006; Roux et al 2023). For Clown Anemonefish A. ocellaris , the metamorphosis involves forming three white bands, corresponding to the transition to the juvenile phase (Salis et al 2018).…”

Section: Introductionmentioning

confidence: 99%

Tank color influence on the Tomato Clownfish Amphiprion frenatus metamorphosis

et al. 2023

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The environmental color positively influenced the development of some fish species. Thus, we evaluated whether different aquarium colors affect the metamorphosis process of tomato clownfish Amphiprion frenatus. Operationally, we distributed the A. frenatus larvae in white (WA), yellow (YA), blue (BA), and black aquaria (BLA) and accompanied the larvae development until 61‐DPH. We showed that environmental color influences the early development of tomato clownfish and their metamorphosis process. 87.2 % of the larvae in the BLA treatment completed the metamorphosis and reached the juvenile stage in block I and 59.3 % in block II. These high percentiles of metamorphosed larvae were not found in other tank colors. Thus, our results suggest that the metamorphosis of A. frenatus could be accelerated if the larviculture occurs in darker color conditions, especially black aquaria. This result has practical and economic implications since the tomato clownfish specimens were commercialized at the juvenile stage.

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The Multi-Level Regulation of Clownfish Metamorphosis Through Thyroid Hormones

Cited by 6 publications

References 3 publications

Thyroid hormone links environmental signals to DNA methylation

Thyroid hormone links environmental signals to DNA methylation

The ecological function of thyroid hormones

Tank color influence on the Tomato Clownfish Amphiprion frenatus metamorphosis

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