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Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes

BACKGROUND: Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. However, the origins and evolution of this diversity are still poorly understood. Disentangling the evolution of simple color patterns offers the opportunity to dissect both...

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Autores principales: Salis, Pauline, Roux, Natacha, Soulat, Olivier, Lecchini, David, Laudet, Vincent, Frédérich, Bruno
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6123960/
https://www.ncbi.nlm.nih.gov/pubmed/30180844
http://dx.doi.org/10.1186/s12915-018-0559-7
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author Salis, Pauline
Roux, Natacha
Soulat, Olivier
Lecchini, David
Laudet, Vincent
Frédérich, Bruno
author_facet Salis, Pauline
Roux, Natacha
Soulat, Olivier
Lecchini, David
Laudet, Vincent
Frédérich, Bruno
author_sort Salis, Pauline
collection PubMed
description BACKGROUND: Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. However, the origins and evolution of this diversity are still poorly understood. Disentangling the evolution of simple color patterns offers the opportunity to dissect both ultimate and proximate causes underlying color diversity. RESULTS: Here, we study clownfishes, a tribe of 30 species within the Pomacentridae that displays a relatively simple color pattern made of zero to three vertical white stripes on a dark body background. Mapping the number of white stripes on the evolutionary tree of clownfishes reveals that their color pattern diversification results from successive caudal to rostral losses of stripes. Moreover, we demonstrate that stripes always appear with a rostral to caudal stereotyped sequence during larval to juvenile transition. Drug treatments (TAE 684) during this period leads to a dose-dependent loss of stripes, demonstrating that white stripes are made of iridophores and that these cells initiate the stripe formation. Surprisingly, juveniles of several species (e.g., Amphiprion frenatus) have supplementary stripes when compared to their respective adults. These stripes disappear caudo-rostrally during the juvenile phase leading to the definitive color pattern. Remarkably, the reduction of stripe number over ontogeny matches the sequences of stripe losses during evolution, showing that color pattern diversification among clownfish lineages results from changes in developmental processes. Finally, we reveal that the diversity of striped patterns plays a key role for species recognition. CONCLUSIONS: Overall, our findings illustrate how developmental, ecological, and social processes have shaped the diversification of color patterns during the radiation of an emblematic coral reef fish lineage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0559-7) contains supplementary material, which is available to authorized users.
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spelling pubmed-61239602018-09-10 Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes Salis, Pauline Roux, Natacha Soulat, Olivier Lecchini, David Laudet, Vincent Frédérich, Bruno BMC Biol Research Article BACKGROUND: Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. However, the origins and evolution of this diversity are still poorly understood. Disentangling the evolution of simple color patterns offers the opportunity to dissect both ultimate and proximate causes underlying color diversity. RESULTS: Here, we study clownfishes, a tribe of 30 species within the Pomacentridae that displays a relatively simple color pattern made of zero to three vertical white stripes on a dark body background. Mapping the number of white stripes on the evolutionary tree of clownfishes reveals that their color pattern diversification results from successive caudal to rostral losses of stripes. Moreover, we demonstrate that stripes always appear with a rostral to caudal stereotyped sequence during larval to juvenile transition. Drug treatments (TAE 684) during this period leads to a dose-dependent loss of stripes, demonstrating that white stripes are made of iridophores and that these cells initiate the stripe formation. Surprisingly, juveniles of several species (e.g., Amphiprion frenatus) have supplementary stripes when compared to their respective adults. These stripes disappear caudo-rostrally during the juvenile phase leading to the definitive color pattern. Remarkably, the reduction of stripe number over ontogeny matches the sequences of stripe losses during evolution, showing that color pattern diversification among clownfish lineages results from changes in developmental processes. Finally, we reveal that the diversity of striped patterns plays a key role for species recognition. CONCLUSIONS: Overall, our findings illustrate how developmental, ecological, and social processes have shaped the diversification of color patterns during the radiation of an emblematic coral reef fish lineage. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12915-018-0559-7) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-05 /pmc/articles/PMC6123960/ /pubmed/30180844 http://dx.doi.org/10.1186/s12915-018-0559-7 Text en © Laudet et al. 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Salis, Pauline
Roux, Natacha
Soulat, Olivier
Lecchini, David
Laudet, Vincent
Frédérich, Bruno
Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title_full Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title_fullStr Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title_full_unstemmed Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title_short Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
title_sort ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6123960/
https://www.ncbi.nlm.nih.gov/pubmed/30180844
http://dx.doi.org/10.1186/s12915-018-0559-7
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