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Pigmentation Variants and Mutants of Anemonefish Klann et al. EvoDevo (2021) 12:8 https://doi.org/10.1186/s13227-021-00178-x EvoDevo REVIEW Open Access Variation on a theme: pigmentation variants and mutants of anemonefsh Marleen Klann1, Manon Mercader1, Lilian Carlu1, Kina Hayashi1,2,3, James Davis Reimer3,4 and Vincent Laudet1,5* Abstract Pigmentation patterning systems are of great interest to understand how changes in developmental mechanisms can lead to a wide variety of patterns. These patterns are often conspicuous, but their origins remain elusive for many marine fsh species. Dismantling a biological system allows a better understanding of the required components and the deciphering of how such complex systems are established and function. Valuable information can be obtained from detailed analyses and comparisons of pigmentation patterns of mutants and/or variants from normal pat‑ terns. Anemonefshes have been popular marine fsh in aquaculture for many years, which has led to the isolation of several mutant lines, and in particular color alterations, that have become very popular in the pet trade. Additionally, scattered information about naturally occurring aberrant anemonefsh is available on various websites and image platforms. In this review, the available information on anemonefsh color pattern alterations has been gathered and compiled in order to characterize and compare diferent mutations. With the global picture of anemonefsh mutants and variants emerging from this, such as presence or absence of certain phenotypes, information on the patterning system itself can be gained. Keywords: Pigmentation, Anemonefsh, Variation, Mutants Introduction erythrophores that are distinguished by color and con- Body coloration, or pigmentation, plays an essential part tain carotenoids and/or pteridines; (3) silver/iridescent in every animal’s survival strategy. Pigmentation is not iridophores which contain guanine crystals, and (4) white only important for predator avoidance or protection leucophores which bear uric acid. against UV radiation, but also for reproductive success Typically, chromatophore precursor/progenitor cells and more generally social interactions [10, 21, 33]. In fsh, are established during embryonic development and set skin pigmentation depends on the distribution of pig- aside to later on contribute larval/adult chromatophores. ment cells, also called chromatophores, which are deriva- In zebrafsh (Danio rerio), currently the major model spe- tives of the neural crest, and are typically classifed based cies for pigment pattern development in teleost fsh, two on the colored pigments or types of crystals they bear as distinct populations of precursors are formed, one for well as their ultrastructure [15]. Te major teleost chro- xanthophores and one for melano- and iridophores [5]. matophores are (1) brown blackish melanophores that In medaka (Oryzias latipes), the xanthophore precursor contain melanin; (2) yellow/orange/red xanthophores/ is still multipotent and can produce either xanthophores or closely related leucophores [40]. In zebrafsh, chroma- tophores must be formed continuously throughout their *Correspondence: [email protected] life to maintain their characteristic striped pattern [25, 1 Marine Eco‑Evo‑Devo Unit, Okinawa Institute of Science 45]. and Technology, 1919‑1 Tancha, Onna‑son, Okinawa 904‑0495, Japan Full list of author information is available at the end of the article © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Klann et al. EvoDevo (2021) 12:8 Page 2 of 16 Patterns in general can be formed by two main princi- were observed and captured in the wild. Other mutants ples: (1) cell autonomously by (genetic) pre-positioning are the result of aquaculture crosses, either made on pur- cues or (2) by cell–cell communication [46]. Te mech- pose or by accident. In this review, we aim to describe anisms for stripe formation (horizontal main axis) in the main anemonefsh mutants available in addition to zebrafsh are relatively well understood. All three chro- natural variants, as they could be signifcant in provid- matophore cell types (melanophores, xanthophores and ing clues on the underlying genetic mechanisms of pig- iridophores, no leucophores are present in zebrafsh) ment pattern formation in these fsh. Here, the term interact and communicate to establish the adult color “mutant” therefore refers to an established line from an pattern of dark stripes and bright interstripes. Some evi- aquaculture company, with the strain name written in dence suggests that this mode of patterning follows the parentheses. For these lines it is known that the observed Turing model, according to which the number of stripes pigmentation phenotype is based on a fxed genetic trait, increases with the growth of the fsh [41]. Interactions or in other words, a mutation. Breeding schemes and out- between zebrafsh chromatophores include long-range as comes detailed and provided on aquaculture companies’ well as short-range efects [14, 46] such as: (1) iridophores websites can be used to infer heritability, although this attract melanophores in high numbers and induce their will need to be genetically confrmed in the future. Te aggregation into prospective stripe areas (positive long- term “variant” is used for wild individuals that display a range); (2) iridophores exclude melanophores from inter- coloration alteration, as it generally remains unknown stripes (negative short-range), (3) xanthophores exclude if the phenotype is based on a fxed, inheritable muta- melanophores from interstripes (negative short-range), tion. However, often these wild variants are based on a and (4) positive and negative interactions between irido- mutation, since wild-caught aberrant individuals have phores and xanthophores being required to confne the served on several occasions as founders in the establish- shape of interstripes (short range). Similarly, the addition ment of new strains in aquaculture (as mentioned above). of bars (vertical main axis) in the cichlid Copadichromis Although there are some polymorphic traits in several azureus requires cell–cell communication, with xantho- species of anemonefsh (numbers of bars, degree of mela- phores and iridophores following the pattern of melano- nism, bar regression with age), these will not be the focus phore distribution [18]. of the present paper as these are complex situations that Extensive zebrafsh and medaka mutant collections are often related to environmentally driven phenotypic have facilitated research on many aspects of pigmenta- plasticity. Studies of several of these polymorphic traits tion, such as fate specifcation, survival, proliferation, are currently underway in our laboratory. and diferentiation [23, 24, 46]. In both taxa, research- ers have mainly focused on embryonic phenotypes, and Color pattern formation in anemonefshes there is an extensive overlap of identifed parallel phe- Anemonefshes (subfamily Amphiprioninae) are a mono- notypes. Te strategy of using mutants identifed during phyletic group within the Pomacentridae (damselfsh) large genetic screenings and then subsequently identify- family, comprising 30 species in two genera: Amphiprion ing the genes underlying their unusual phenotypes has (29 species) and Premnas (monospecifc) [54]. Tey are therefore been very fruitful. However, such a strategy well known for their ability to establish mutualistic sym- has been limited to established model organisms that are biotic relationships with sea anemones and their brilliant well set up in terms of mutagenesis, genetic screening, color patterns have been proposed to be either a social and experimental genetics [26, 47]. Although research on display allowing species recognition [58] or an apose- both zebrafsh and medaka have efectively led to great matic trait warning of harmful stings from their host [36]. scientifc breakthroughs in our understanding of pig- Adult anemonefshes display a relatively simple and ment pattern formation, they represent only a small frac- robust color pattern comprising zero to three vertical tion of living biodiversity, and therefore new Evo-Devo white bars usually with a black outline on an orange- model species have been developed in the past few years. to-red body (Fig. 1A). Interspecifc variations manifest Among these newer models, anemonefshes are color- mainly in the number of white bars, as well as the color ful coral reef fsh that ofer great promise to enlarge and of the body and the fns [31, 52, 58]. Tis characteristic deepen our knowledge
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