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Multipotent neural crest (NC) progenitors generate an astonishing array of derivatives, including neuronal, skeletal components and pigment cells (chromatophores), but the molecular mechanisms allowing balanced selection of each fate remain unknown. In zebrafish, melanocytes, iridophores and xanthophores, the three chromatophore lineages, are thought to share progenitors and so lend themselves to investigating the complex gene regulatory networks (GRNs) underlying fate segregation of NC progenitors. Although the core GRN governing melanocyte specification has been previously established, those guiding iridophore and xanthophore development remain elusive. Here we focus on the iridophore GRN, where mutant phenotypes identify the transcription factors Sox10, Tfec and Mitfa and the receptor tyrosine kinase, Ltk, as key players. Here we present expression data, as well as loss and gain of function results, guiding the derivation of an initial iridophore specification GRN. Moreover, we use an iterative process of mathematical modelling, supplemented with a Monte Carlo screening algorithm suited to the qualitative nature of the experimental data, to allow for rigorous predictive exploration of the GRN dynamics. Predictions were experimentally evaluated and testable hypotheses were derived to construct an improved version of the GRN, which we showed produced outputs consistent with experimentally observed gene expression dynamics. Our study reveals multiple important regulatory features, notably a sox10-dependent positive feedback loop between tfec and ltk driving iridophore specification; the molecular basis of sox10 maintenance throughout iridophore development; and the cooperation between sox10 and tfec in driving expression of pnp4a, a key differentiation gene. We also assess a candidate repressor of mitfa, a melanocyte-specific target of sox10. Surprisingly, our data challenge the reported role of Foxd3, an established mitfa repressor, in iridophore regulation. Our study builds upon our previous systems biology approach, by incorporating physiologically-relevant parameter values and rigorous evaluation of parameter values within a qualitative data framework, to establish for the first time the core GRN guiding specification of the iridophore lineage.

The pattern of alternating blue and golden stripes displayed by adult zebrafish is composed of three kinds of pigment cells: black melanophores, yellow xanthophores, and silvery-blue iridophores. We analyzed the dynamics of xanthophores during stripe morphogenesis in vivo with long-term time-lapse imaging. Larval xanthophores start to proliferate at the onset of metamorphosis and give rise to adult xanthophores covering the flank before the arrival of stem-cell–derived iridophores and melanophores. Xanthophores compact to densely cover the iridophores forming the interstripe, and they acquire a loose stellate shape over the melanophores in the stripes. Thus, xanthophores, attracted by iridophores and repelling melanophores, sharpen and color the pattern. Variations on these cell behaviors may contribute to the generation of color pattern diversity in fish.

The adult striped pattern of zebrafish is composed of melanophores, iridophores and xanthophores arranged in superimposed layers in the skin. Previous studies have revealed that the assembly of pigment cells into stripes involves heterotypic interactions between all three chromatophore types. Here we investigate the role of homotypic interactions between cells of the same chromatophore type. Introduction of labelled progenitors into mutants lacking the corresponding cell type allowed us to define the impact of competitive interactions via long-term in vivo imaging. In the absence of endogenous cells, transplanted iridophores and xanthophores show an increased rate of proliferation and spread as a coherent net into vacant space. By contrast, melanophores have a limited capacity to spread in the skin even in the absence of competing endogenous cells. Our study reveals a key role for homotypic competitive interactions in determining number, direction of migration and individual spacing of cells within chromatophore populations. Melanophores, iridophores and xanthophores are pigment-cell types that interact to form the stripes in zebrafish. Here, the authors study the interaction between cells of the same kind and show that each pigment-cell type covers the skin by contact based competition.

The fitness of male guppies (Poecilia reticulata) highly depends on the size and number of their black, blue, and orange ornaments. Recently, progress has been made regarding the genetic mechanisms underlying male guppy pigment pattern formation, but we still know little about the pigment cell organization within these ornaments. Here, we investigate the pigment cell distribution within the black, blue, and orange trunk spots and selected fin color patterns of guppy males from three genetically divergent strains using transmission electron microscopy. We identified three types of pigment cells and found that at least two of these contribute to each color trait. Further, two pigment cell layers, one in the dermis and the other in the hypodermis, contribute to each trunk spot. The pigment cell organization within the black and orange trunk spots was similar between strains. The presence of iridophores in each of the investigated color traits is consistent with a key role for this pigment cell type in guppy color pattern formation.

Based on their cell ultrastructure, two types of erythrophores in the spotted skin regions of brown trout ( Salmo trutta ) were previously described. To test the hypothesis regarding the origin of a new cell type following genome duplication, we analysed the gene and paralogue gene expression patterns of erythrophores in brown trout skin. In addition, the ultrastructure of both erythrophore types was precisely examined using transmission electron microscopy (TEM) and correlative light microscopy and electron microscopy (CLEM). Ultrastructural differences between the sizes of erythrophore inclusions were confirmed; however, the overlapping inclusion sizes blur the distinction between erythrophore types, which we have instead defined as cell subtypes. Nevertheless, the red spots of brown trout skin with subtype 2 erythrophores, exhibited unique gene expression patterns. Many of the upregulated genes are involved in melanogenesis or xanthophore differentiation. In addition, sox10 , related to progenitor cells, was also upregulated in the red spots. The expressions of paralogues derived from two genome duplication events were also analysed. Multiple paralogues were overexpressed in the red spots compared with other skin regions, suggesting that the duplicated gene copies adopted new functions and contributed to the origin of a new cell subtype that is characteristic for red spot. Possible mechanisms regarding erythrophore origin are proposed and discussed. To the best of our knowledge, this is the first study to evaluate pigment cell types in the black and red spots of brown trout skin using the advanced CLEM approach together with gene expression profiling.

The zebrafish is a model organism for pattern formation in vertebrates. Understanding what drives the formation of its coloured skin motifs could reveal pivotal to comprehend the mechanisms behind morphogenesis. The motifs look and behave like reaction–diffusion Turing patterns, but the nature of the underlying physico-chemical processes is very different, and the origin of the patterns is still unclear. Here we propose a minimal model for such pattern formation based on a regulatory mechanism deduced from experimental observations. This model is able to produce patterns with intrinsic wavelength, closely resembling the experimental ones. We mathematically prove that their origin is a Turing bifurcation occurring despite the absence of cell motion, through an effect that we call differential growth. This mechanism is qualitatively different from the reaction–diffusion originally proposed by Turing, although they both generate the short-range activation and the long-range inhibition required to form Turing patterns. Pigment pattern formation in zebrafish depends on the interactions between the pigment cells. Here the authors present a mathematical model based on mutual interaction of pigment cells in the absence of cell motion, revising the current model of the pattern formation that relies on reaction–diffusion Turing patterns.

Nature's best-known example of colorful, changeable, and diverse skin patterning is found in cephalopods. Color and pattern changes in squid skin are mediated by the action of thousands of pigmented chromatophore organs in combination with subjacent light-reflecting iridophore cells. Chromatophores (brown, red, yellow pigment) are innervated directly by the brain and can quickly expand and retract over underlying iridophore cells (red, orange, yellow, green, blue iridescence). Here, we present the first spectral account of the colors that are produced by the interaction between chromatophores and iridophores in squid (Loligo pealeii). Using a spectrometer, we have acquired highly focused reflectance measurements of chromatophores, iridophores, and the quality and quantity of light reflected when both interact. Results indicate that the light reflected from iridophores can be filtered by the chromatophores, enhancing their appearance. We have also measured polarization aspects of iridophores and chromatophores and show that, whereas structurally reflecting iridophores polarize light at certain angles, pigmentary chromatophores do not. We have further measured the reflectance change that iridophores undergo during physiological activity, from \"off\" to various degrees of \"on\", revealing specifically the way that colors shift from the longer end (infra-red and red) to the shorter (blue) end of the spectrum. By demonstrating that three color classes of pigments, combined with a single type of reflective cell, produce colors that envelop the whole of the visible spectrum, this study provides an insight into the optical mechanisms employed by the elaborate skin of cephalopods to give the extreme diversity that enables their dynamic camouflage and signaling.

Body coloration plays a major role in fish ecology and is predominantly generated using two principles: a) absorbance combined with reflection of the incoming light in pigment colors and b) scatter, refraction, diffraction and interference in structural colors. Poikilotherms, and especially fishes possess several cell types, so-called chromatophores, which employ either of these principles. Together, they generate the dynamic, multi-color patterns used in communication and camouflage. Several chromatophore types possess motile organelles, which enable rapid changes in coloration. Recently, we described red fluorescence in a number of marine fish and argued that it may be used for private communication in an environment devoid of red. Here, we describe the discovery of a chromatophore in fishes that regulates the distribution of fluorescent pigments in parts of the skin. These cells have a dendritic shape and contain motile fluorescent particles. We show experimentally that the fluorescent particles can be aggregated or dispersed through hormonal and nervous control. This is the first description of a stable and natural cytoskeleton-related fluorescence control mechanism in vertebrate cells. Its nervous control supports suggestions that fluorescence could act as a context-dependent signal in some marine fish species and encourages further research in this field. The fluorescent substance is stable under different chemical conditions and shows no discernible bleaching under strong, constant illumination.

Abnormal pigmentation of Senegalese sole has been described as one problem facing the full exploitation of its commercial production. To improve our understanding of flatfish pigmentation of this commercially important species we have evaluated eleven genes related to two different processes of pigmentation: melanophore differentiation, and melanin production. The temporal distribution of gene expression peaks corresponds well with changes in pigmentation patterns and the intensity of skin melanization. Several gene ratios were also examined to put in perspective possible genetic markers for the different stages of normal pigmentation development. Further, the phenotypic changes that occur during morphogenesis correspond well with the main transitions in gene expression that occur. Given the dramatic phenotypic alterations which flatfish undergo, including the asymmetric coloration that occurs between the ocular and the blind side, and the synchrony of the two processes of morphogenesis and pigmentation ontogenesis, these species constitute an interesting model for the study of pigmentation. In this study we present a first approximation towards explaining the genetic mechanisms for regulating pigmentation ontogeny in Senegalese sole, Solea senegalensis.