The multi-level regulation of clownfish metamorphosis by 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:10.1016/j.celrep.2023.112661

Cited by 14 publications

(20 citation statements)

References 83 publications

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“…This trend is similar to what has been observed in other fish species such as sea bass 21,52 , but contrasts with the situation of other species such as the clownfish. Thyroid hormones are known to play a role in the regulation of metabolism in mammals 53 , so it is likely that a similar regulatory process occurs during the development of E. malabaricus larvae, as it has been recently observed in the development of clownfish larvae 15 . Larval development and metamorphosis are very sensitive periods during which larvae must face a myriad of challenges: disperse into the open ocean, find food, escape from predators, locate and swim toward a suitable habitat, metamorphose and settle.…”

Section: Metamorphosis Is Accompanied By a Metabolic Shiftmentioning

confidence: 85%

“…It is well known that in many fish species this ecological transition is accompanied by a change in color vision 45 . Since TH appeared critical in the regulation of genes involved in vision in salmonids, zebrafish and clownfish 14,15,46,47 , we investigated the regulation of genes encoding for visual opsin. We expected to find at least eight visual cone opsin genes in E. malabaricus according to the phylogeny of opsin genes in teleosts 48 (opnsw1, opnsw2Aa, opnsw2Ab, opnsw2B, rh2A, rh2B, rh2C, opnlw) and one rhodopsin gene (rh1) 48,49 .…”

Section: Th Involvement In Spine Elongation and Regressionmentioning

confidence: 99%

“…These changes are thought to be initiated and coordinated by a surge of TH, which regulates various signaling pathways through the action of specific transcription factors known as thyroid hormone receptors (TRα, TRβ). For example, there is evidence that TH is associated with the transition between oceanic and coral reef environments in the convict surgeonfish 9 , controls pigmentation changes in zebrafish, clownfish, and grouper 10,11 , regulates ossification processes in zebrafish and flatfishes 12,13 and is involved in the shift of visual perception by controlling the expression of opsin genes in many species 14,15 . More recently, it has also been suggested that the metabolic changes that occur during larval development in teleosts may be regulated by TH, as demonstrated in clownfish 15 .…”

Section: Introductionmentioning

confidence: 99%

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The transcriptional landscape underlying metamorphosis in the Malabar grouper (Epinephelus malabaricus)

Huerlimann,

Roux,

Maeda

et al. 2023

Preprint

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Teleost fishes typically have a bi-phasic life cycle with a transition between larval and juvenile phases called metamorphosis, which is known to be regulated by thyroid hormones (TH). However, other hormonal systems might be involved as it is the case in amphibians in which corticosteroids are interacting with TH pathway to trigger and regulate metamorphosis. Unfortunately, such interplay is poorly understood in teleost fishes. In order to investigate the potential involvement of these two hormonal pathways, we used the Malabar grouper (Epinephelus malabaricus) as a model system. We assembled a chromosome-scale genome and conducted a transcriptomic analysis of nine larval developmental stages. We studied the expression patterns of genes involved in TH and corticoid pathways, as well as four biological processes known to be regulated by TH in other teleost species: ossification, pigmentation, visual perception, and metabolism. Interestingly, we observed an interplay between TH and corticosteroid coinciding with metamorphosis and, more surprisingly, an early activation of both pathways was observed suggesting their implication in early larval development. Overall, our data reveal that on a common background (TH controlling metamorphosis) evolution is assembling species-specific peculiarities that allow to precisely align the molecular completion of metamorphosis with the ecological constraints.

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Section: Metamorphosis Is Accompanied By a Metabolic Shiftmentioning

confidence: 85%

Section: Th Involvement In Spine Elongation and Regressionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The transcriptional landscape underlying metamorphosis in the Malabar grouper (Epinephelus malabaricus)

Huerlimann,

Roux,

Maeda

et al. 2023

Preprint

Self Cite

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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: (B) Thyroid Hormone Actionmentioning

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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“…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 (Mc-Menamin 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 by thyroid hormones

Cited by 14 publications

References 83 publications

The transcriptional landscape underlying metamorphosis in the Malabar grouper (Epinephelus malabaricus)

The transcriptional landscape underlying metamorphosis in the Malabar grouper (Epinephelus malabaricus)

Thyroid hormone links environmental signals to DNA methylation

Tank color influence on the Tomato Clownfish Amphiprion frenatus metamorphosis

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