Ontogenetic and phylogenetic simplification during white stripe evolution in clownfishes

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.Electronic supplementary materialThe online version of this article (10.1186/s12915-018-0559-7) contains supplementary material, which is available to authorized users.

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

“…In the context of this study, we define metamorphosis as a postembryonic developmental step triggered by thyroid hormones and characterized by ecological, behavioral, morphological, and physiological changes. For the clownfish A. ocellaris , metamorphosis involves acquisition of three white stripes and corresponds to the transition of the juvenile phase . Indeed, when the white stripes appear on the head and body of A. ocellaris , a change of swimming behavior is observed in the tank: Larvae swim in the water column, while metamorphic and postmetamorphic fish swim closer to substrates.…”

“…In addition, they possess peculiar anatomical traits to graze filamentous algae and to produce sounds during numerous social interactions . The clownfish also provide a unique model for the evolution of pigment pattern that allows the study of how ecology and development can permit and constrain the diversification of complex patterns . Last, clownfishes developed unique symbiotic relationships with giant sea anemones.…”

“…Thus, clownfish is a new model species with a high potential to further study evolutionary and developmental processes in a unique ecological framework. However, to date, only few data are available on its postembryonic development . Establishing a developmental table for this species would be of particular interest to conduct evo‐devo studies such as those listed above.…”

“…[38][39][40] The clownfish also provide a unique model for the evolution of pigment pattern that allows the study of how ecology and development can permit and constrain the diversification of complex patterns. 30,41,42 Last, clownfishes developed unique symbiotic relationships with giant sea anemones. The recruitment of the young juveniles in their host, the development of the mechanisms preventing the stinging of the sea anemone nematocysts, the variable host specificity displayed by the different species, and the mechanisms by which several clownfish can share the same host are all basic biological issues that can be studied using this model and that can impact more broadly other kinds of symbiotic relationships between eukaryotic organisms.…”

“…However, to date, only few data are available on its postembryonic development. 27,42,43 Establishing a developmental table for this species would be of particular interest to conduct evo-devo studies such as those listed above.…”