Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes
Abstract 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 disse...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
BMC
2018-09-01
|
Series: | BMC Biology |
Subjects: | |
Online Access: | http://link.springer.com/article/10.1186/s12915-018-0559-7 |
_version_ | 1819067823592308736 |
---|---|
author | Pauline Salis Natacha Roux Olivier Soulat David Lecchini Vincent Laudet Bruno Frédérich |
author_facet | Pauline Salis Natacha Roux Olivier Soulat David Lecchini Vincent Laudet Bruno Frédérich |
author_sort | Pauline Salis |
collection | DOAJ |
description | Abstract 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. |
first_indexed | 2024-12-21T16:24:23Z |
format | Article |
id | doaj.art-30b50c145a1b403a822e39d9b7b949c1 |
institution | Directory Open Access Journal |
issn | 1741-7007 |
language | English |
last_indexed | 2024-12-21T16:24:23Z |
publishDate | 2018-09-01 |
publisher | BMC |
record_format | Article |
series | BMC Biology |
spelling | doaj.art-30b50c145a1b403a822e39d9b7b949c12022-12-21T18:57:29ZengBMCBMC Biology1741-70072018-09-0116111310.1186/s12915-018-0559-7Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishesPauline Salis0Natacha Roux1Olivier Soulat2David Lecchini3Vincent Laudet4Bruno Frédérich5Observatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université ParisObservatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université ParisAquarium de Canet-en-RoussillonEPHE-UPVD-CNRS, USR3278 CRIOBE, PSL Research UniversityObservatoire Océanologique de Banyuls-sur-Mer, UMR CNRS 7232 BIOM, Sorbonne Université ParisLaboratory of Functional and Evolutionary Morphology, FOCUS, University of LiègeAbstract 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.http://link.springer.com/article/10.1186/s12915-018-0559-7OntogenyDiversificationPomacentridaeColor evolutionAdaptive coloration |
spellingShingle | Pauline Salis Natacha Roux Olivier Soulat David Lecchini Vincent Laudet Bruno Frédérich Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes BMC Biology Ontogeny Diversification Pomacentridae Color evolution Adaptive coloration |
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 | Ontogeny Diversification Pomacentridae Color evolution Adaptive coloration |
url | http://link.springer.com/article/10.1186/s12915-018-0559-7 |
work_keys_str_mv | AT paulinesalis ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes AT natacharoux ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes AT oliviersoulat ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes AT davidlecchini ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes AT vincentlaudet ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes AT brunofrederich ontogeneticandphylogeneticsimplificationduringwhitestripeevolutioninclownfishes |