Thyroid hormones regulate the formation and environmental plasticity of white bars in clownfishes.

Pauline Salis, Natacha Roux, Delai Huang, Anna Marcionetti, Pierick Mouginot, Mathieu Reynaud, Océane Salles, Nicolas Salamin, Benoit Pujol, David M Parichy, Serge Planes, Vincent Laudet
Author Information
  1. Pauline Salis: Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 Biologie Intégrative des Organismes Marins, Sorbonne Université Paris, 66650 Banyuls-sur-Mer, France. ORCID
  2. Natacha Roux: Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 Biologie Intégrative des Organismes Marins, Sorbonne Université Paris, 66650 Banyuls-sur-Mer, France. ORCID
  3. Delai Huang: Department of Biology, University of Virginia, Charlottesville, VA 22903. ORCID
  4. Anna Marcionetti: Department of Computational Biology, University of Lausanne, 1015, Lausanne, Switzerland.
  5. Pierick Mouginot: Ecole Pratique des Hautes Etudes, Paris Siences et Lettres Research University, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan, France. ORCID
  6. Mathieu Reynaud: Marine Eco-Evo-Devo Unit, Okinawa Institute of Science and Technology, Onna son, Okinawa 904-0495 Japan. ORCID
  7. Océane Salles: Ecole Pratique des Hautes Etudes, Paris Siences et Lettres Research University, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan, France.
  8. Nicolas Salamin: Department of Computational Biology, University of Lausanne, 1015, Lausanne, Switzerland. ORCID
  9. Benoit Pujol: Ecole Pratique des Hautes Etudes, Paris Siences et Lettres Research University, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan, France.
  10. David M Parichy: Department of Biology, University of Virginia, Charlottesville, VA 22903. ORCID
  11. Serge Planes: Ecole Pratique des Hautes Etudes, Paris Siences et Lettres Research University, Université de Perpignan Via Domitia, CNRS, USR 3278 Centre de Recherches Insulaires et Observatoire de l'environnement, F-66360 Perpignan, France.
  12. Vincent Laudet: Marine Eco-Evo-Devo Unit, Okinawa Institute of Science and Technology, Onna son, Okinawa 904-0495 Japan; vincent.laudet@oist.jp.

Abstract

Determining how plasticity of developmental traits responds to environmental conditions is a challenge that must combine evolutionary sciences, ecology, and developmental biology. During metamorphosis, fish alter their morphology and color pattern according to environmental cues. We observed that juvenile clownfish () modulate the developmental timing of their adult white bar formation during metamorphosis depending on the sea anemone species in which they are recruited. We observed an earlier formation of white bars when clownfish developed with () than with (). As these bars, composed of iridophores, form during metamorphosis, we hypothesized that timing of their development may be thyroid hormone (TH) dependent. We treated clownfish larvae with TH and found that white bars developed earlier than in control fish. We further observed higher TH levels, associated with rapid white bar formation, in juveniles recruited in than in , explaining the faster white bar formation. Transcriptomic analysis of recruits revealed higher expression of , a dual oxidase implicated in TH production as compared to recruits. Finally, we showed that is an essential regulator of iridophore pattern timing in zebrafish. Taken together, our results suggest that TH controls the timing of adult color pattern formation and that shifts in expression and TH levels are associated with ecological differences resulting in divergent ontogenetic trajectories in color pattern development.

Keywords

References

  1. Nat Commun. 2020 Dec 15;11(1):6391 [PMID: 33319779]
  2. Genome Biol Evol. 2009 Nov 25;1:479-93 [PMID: 20333216]
  3. G3 (Bethesda). 2018 May 4;8(5):1795-1806 [PMID: 29599177]
  4. Proc Biol Sci. 2017 Mar 29;284(1851): [PMID: 28356453]
  5. Dev Dyn. 2009 Dec;238(12):2975-3015 [PMID: 19891001]
  6. PLoS Genet. 2018 Sep 18;14(9):e1007538 [PMID: 30226839]
  7. Elife. 2015 Dec 23;4: [PMID: 26701906]
  8. Science. 2014 Sep 12;345(6202):1358-61 [PMID: 25170046]
  9. Curr Biol. 2015 Mar 30;25(7):949-54 [PMID: 25802153]
  10. Trends Genet. 2019 Apr;35(4):265-278 [PMID: 30819536]
  11. Proc Natl Acad Sci U S A. 2016 Nov 15;113(46):13245-13250 [PMID: 27799530]
  12. BMC Evol Biol. 2012 Nov 02;12:212 [PMID: 23122007]
  13. Dev Cell. 2019 Dec 2;51(5):645-657.e4 [PMID: 31708433]
  14. Evodevo. 2020 Oct 7;11:20 [PMID: 33042514]
  15. Mol Ecol. 2009 Sep;18(18):3763-80 [PMID: 19732339]
  16. Elife. 2017 Oct 30;6: [PMID: 29083300]
  17. Trends Ecol Evol. 2008 Sep;23(9):502-10 [PMID: 18644658]
  18. J Endocrinol. 2007 Mar;192(3):615-26 [PMID: 17332529]
  19. Curr Top Dev Biol. 2013;103:127-65 [PMID: 23347518]
  20. Nat Commun. 2017 Oct 19;8(1):993 [PMID: 29051478]
  21. Elife. 2019 May 29;8: [PMID: 31140974]
  22. Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6543-9 [PMID: 15851679]
  23. J Genet Genomics. 2019 Feb;46(2):101-104 [PMID: 30867122]
  24. Elife. 2017 Sep 06;6: [PMID: 28875931]
  25. Cereb Cortex. 2015 Jul;25(7):1735-45 [PMID: 24436321]
  26. Pigment Cell Melanoma Res. 2019 May;32(3):391-402 [PMID: 30633441]
  27. Zebrafish. 2008 Dec;5(4):297-307 [PMID: 19133828]
  28. J Biosci. 2005 Feb;30(1):65-74 [PMID: 15824442]
  29. Front Endocrinol (Lausanne). 2019 Jun 14;10:383 [PMID: 31258515]
  30. Mol Cell Endocrinol. 2020 Feb 15;502:110678 [PMID: 31830511]
  31. Annu Rev Genet. 2019 Dec 3;53:505-530 [PMID: 31509458]
  32. J Exp Zool A Comp Exp Biol. 2003 Jul 1;298(1):32-43 [PMID: 12840837]
  33. Biol Open. 2019 Feb 22;8(2): [PMID: 30700401]
  34. Trends Ecol Evol. 2010 Aug;25(8):459-67 [PMID: 20557976]
  35. BMC Biol. 2018 Sep 5;16(1):90 [PMID: 30180844]
  36. Evol Dev. 2003 Jan-Feb;5(1):9-18 [PMID: 12492404]
  37. PLoS One. 2014 May 30;9(5):e98449 [PMID: 24878777]
  38. Gen Comp Endocrinol. 1985 Dec;60(3):450-4 [PMID: 3935513]
  39. J Evol Biol. 2008 May;21(3):705-15 [PMID: 18355186]
  40. Dev Dyn. 2019 Jul;248(7):545-568 [PMID: 31070818]
  41. Curr Biol. 2011 Sep 27;21(18):R726-37 [PMID: 21959163]

Grants

  1. R35 GM122471/NIGMS NIH HHS

MeSH Term

Adaptation, Physiological
Animals
Fishes
Sea Anemones
Skin Pigmentation
Thyroid Hormones

Chemicals

Thyroid Hormones

Word Cloud

Created with Highcharts 10.0.0whiteformationTHdevelopmentalmetamorphosispatterntimingbarsplasticityenvironmentalcolorobservedclownfishbarfishadultrecruitedearlierdevelopeddevelopmentthyroidhigherlevelsassociatedrecruitsexpressionhormonesclownfishesDeterminingtraitsrespondsconditionschallengemustcombineevolutionarysciencesecologybiologyaltermorphologyaccordingcuesjuvenilemodulatedependingseaanemonespeciescomposediridophoresformhypothesizedmayhormonedependenttreatedlarvaefoundcontrolrapidjuvenilesexplainingfasterTranscriptomicanalysisrevealeddualoxidaseimplicatedproductioncomparedFinallyshowedessentialregulatoriridophorezebrafishTakentogetherresultssuggestcontrolsshiftsecologicaldifferencesresultingdivergentontogenetictrajectoriesThyroidregulatepigmentation

Similar Articles

Cited By (16)