Abstract

BackgroundBiologists 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.ResultsHere, 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.ConclusionsOverall, 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.

Highlights

  • Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes

  • Pigmentation, in particular color patterns, provides an incredible number of cases that allow the exploration of the interplay between ecology, evolution, and development that are at the basis of trait diversification [2,3,4,5,6]

  • Using specific drugs (e.g., TAE 684: an inhibitor of tyrosine kinase receptors expressed in zebrafish iridophores), we reveal that the white stripes are formed by iridophores and are essential for the patterning of the neighboring black stripes

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Summary

Introduction

Biologists have long been fascinated by the striking diversity of complex color patterns in tropical reef fishes. Pigmentation, in particular color patterns, provides an incredible number of cases that allow the exploration of the interplay between ecology, evolution, and development that are at the basis of trait diversification [2,3,4,5,6]. Coral reef fishes provide classical examples of complex color patterns exhibiting a huge variety, and they offer a unique opportunity to better understand, in an integrated manner, the origin of those traits [7]. Most of coral reef fish species display spots, stripes, repeated lines, eyespots, grids, etc. This diversity in color patterns serves for species recognition [8, 9], camouflage [10, 11], mimicry [12], and/or warning [13]. The underlying development controlling these patterns and their evolution, that is, their proximal mechanism, is still largely unknown [15, 16]

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