Thyroid Hormone Stimulates the Onset of Adult Feeding Kinematics in Zebrafish

McMenamin, Sarah K.; Carter, Casey; Cooper, W. James

doi:10.1089/zeb.2017.1453

Cited by 25 publications

(40 citation statements)

References 26 publications

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“…This decoupling may indicate the timing of the metamorphosis of A. ocellaris, which would be mainly characterized by pigmentation changes and not by drastic morphological changes, as it has been observed in grouper, flatfish, or surgeonfish. 8,11,74 In those species, it is known that thyroid hormones are controlling metamorphosis as in amphibians, 75 and it has been shown that these hormones markedly affect overall growth and development rates, as well as individual traits including pigmentation and scales, 76 feeding kinematics, 77 and morphometrics and the lateral line. 78 It is similarly likely that thyroid hormones control the morphological and pigmentation changes that occur during A. ocellaris metamorphosis.…”

Section: Dissociation Between Morphological and Pigmentation Changesmentioning

confidence: 99%

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

Roux

Salis

Lambert

et al. 2019

Developmental Dynamics

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Background The clownfish Amphiprion ocellaris is one of the rare coral reef fish species that can be reared in aquaria. With relatively short embryonic and larval development, it could be used as a model species to study the impact of global changes such as temperature rise or anthropogenic threats (eg, pollution) on the postembryonic development at molecular and endocrinological levels. Establishing a developmental table allows us to standardize sampling for the scientific community willing to conduct experiments on this species on different areas: ecology, evolution, and developmental biology. Results Here, we describe the postembryonic developmental stages for the clownfish A. ocellaris from hatching to juvenile stages (30 days posthatching). We quantitatively followed the postembryonic growth and described qualitative traits: head, paired and unpaired fins, notochord flexion, and pigmentation changes. The occurrence of these changes over time allowed us to define seven stages, for which we provide precise descriptions. Conclusions Our work gives an easy system to determine A. ocellaris postembryonic stages allowing, thus, to develop this species as a model species for coral reef fishes. In light of global warming, the access to the full postembryonic development stages of coral reef fish is important to determine stressors that can affect such processes.

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Section: Dissociation Between Morphological and Pigmentation Changesmentioning

confidence: 99%

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

Roux

Salis

Lambert

et al. 2019

Developmental Dynamics

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“…Danionellas are Danionins relatively closely related to zebrafish (McCluskey and Postlethwait 2014). Members of this miniaturized group are developmentally arrested and resemble larval Danios in several ways: adult Danionellas lack scales, barbels and many typically late-ossifying bones (Britz, Conway et al 2009, Britz andConway 2016), and they retain a larva-like pigment pattern and feeding kinematics (McMenamin, Carter et al 2017, Galindo, Sweet et al 2018. Danionellas are emerging as a novel model for studying behavior, neurobiology and brain function (Penalva, Bedke et al 2018, Schulze, Henninger et al 2018, and a hybrid genome assembly was recently completed (Kadobianskyi, Schulze et al 2019).…”

Section: Introductionmentioning

confidence: 99%

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Mauri

Donahue

et al. 2019

Preprint

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BackgroundChanges in post-embryonic developmental trajectories can profoundly alter adult phenotypes and life history transitions. In vertebrate clades with complex, biphasic life cycles, thyroid hormone (TH) regulates metamorphosis, and alterations to TH metabolism underlie famous cases of paedomorphosis. We tested the requirement for TH in multiple post-embryonic developmental processes in the zebrafish, and asked if TH loss was associated with paedomorphosis in miniaturized Danionellas.ResultsWe found that TH regulates the relative growth of different body parts in zebrafish, inhibiting head growth at juvenile stages. The lateral line also showed sensitivity to the hormone: head neuromasts were inhibited by TH, while trunk neuromasts required TH for their proliferation. While several aspects of Danionella morphology resembled that of larval zebrafish, these species did not resemble hypothyroid zebrafish in their shape or lateral line, and these fish showed functional thyroid follicles.ConclusionsAlthough zebrafish do not undergo a discrete ecological transformation, we found that multiple tissues go through a protracted metamorphosis, and that TH ushers in growth patterns and processes typical of juveniles. We found no evidence that compromised TH metabolism is responsible for paedomorphosis in Danionellas. Nonetheless, modulations to TH-sensitive pathways affect evolutionarily-relevant traits, and are likely important targets for adaptation.Bullet PointsThyroid hormone regulates shifts in relative growth trajectories in different zebrafish tissuesThyroid hormone inhibits head growth in juvenile zebrafish, and regulates juvenile growth patternsThyroid hormone stimulates formation of neuromast canals in the head and ‘stitches’ on the trunk of zebrafishDanionella, the miniaturized sister group to Danio morphologically resemble larval zebrafish and do not form neuromast canalsHypothyroidism is not the cause of paedomorphosis in DanionellaGrant SponsorsNIH R00GM105874NIH R03HD091634Burroughs Wellcome Collaborative Research Travel Grant 1017439

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“…T 3 has a pleiotropic effect and influences numerous target genes (Rastorguev et al, 2016;Viguerie & Langin, 2003). TH is known to influence timing and rate of multiple developmental events in fish (Blanton & Specker 2007;Brown, 1997;de Jesus, Toledo, & Simpas, 1998;Guillot et al, 2016;Janz, 2000;McMenamin & Parichy, 2013;McMenamin, Carter, & Cooper, 2017;Parichy, Reedy, & Erickson, 2006;Shkil, Kapitanova, Borisov, Abdissa, & Smirnov, 2012;Singh & Nüsslein-Volhard, 2015), including pigment pattern development (Guillot et al, 2016;Jegstrup & Rosenkilde, 2003;McMenamin et al, 2014;Prazdnikov & Shkil, 2016;Yoo, Takeuchi, Tagawa, & Seikai, 2000). Thus, manipulation of TH status is an appropriate method to test the hypothetical role of heterochronies in the formation of cichlid pigment pattern diversity.…”

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confidence: 99%

Experimental evidence of the role of heterochrony in evolution of the Mesoamerican cichlids pigment patterns

Prazdnikov

Shkil

2018

Evolution and Development

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The Mesoamerican cichlids display a spectacular diversity of pigment patterns, which serve a variety of functions and serve as a strong selective trait for this lineage. The development and variation of coloration in the Mesoamerican cichlids have been detailed by several groups. In particular, Říčan, Musilová, Muška, and Novák () and Říčan, Piálek, Dragová, and Novák () determined homology of pattern and revealed four alternative types of coloration and their ontogeny. In this work, this group posed an “ontogenetic timing hypothesis” proposing heterochronic shifts underlying major transitions in the evolution of the Mesoamerican cichlids. Here, we experimentally test this hypothesis by experimentally altering timing of pigment pattern formation in the convict cichlid Amatitlania nigrofasciata, a member of the Mesoamerican cichlids, via manipulations of thyroid hormone (TH) function. The response of different pigment cell lineages to TH‐perturbations revealed that the transition from larval to juvenile coloration in the convict cichlid is under the control of TH‐signaling. Importantly, hormonally induced changes in the timing of pigment cell lineages’ development resulted in shifts of coloration ontogeny type observed between lineages and led to the appearance of phenotypes mimicking those in phylogenetically close and distant species. Thus, our findings support the hypothesis that simple changes in ontogenetic timing underlies species specific patterns in pigmentation and provide new perspectives for studying the role of endocrine signaling in the evolution of cichlids.

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Thyroid Hormone Stimulates the Onset of Adult Feeding Kinematics in Zebrafish

Cited by 25 publications

References 26 publications

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

Staging and normal table of postembryonic development of the clownfish (Amphiprion ocellaris)

Thyroid hormone coordinates developmental trajectories but does not underlie developmental truncation in Danionins

Experimental evidence of the role of heterochrony in evolution of the Mesoamerican cichlids pigment patterns

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