Bar, stripe and spot development in sand-dwelling cichlids from Lake Malawi

Abstract

Background Melanic patterns such as horizontal stripes, vertical bars and spots are common among teleost fishes and often serve roles in camouflage or mimicry. Extensive research in the zebrafish model has shown that the development of horizontal stripes depends on complex cellular interactions between melanophores, xanthophores and iridophores. Little is known about the development of horizontal stripes in other teleosts, and even less is known about bar or spot development. Here, we compare chromatophore composition and development of stripes, bars and spots in two cichlid species of sand-dwellers from Lake Malawi— Copadichromis azureus and Dimidiochromis compressiceps . Results (1) In D. compressiceps, stripes are made of dense melanophores underlaid by xanthophores and overlaid by iridophores. Melanophores and xanthophores are either loose or absent in interstripes, and iridophores are dense. In C. azureus, spots and bars are composed of a chromatophore arrangement similar to that of stripes but are separated by interbars where density of melanophores and xanthophores is only slightly lower than in stripes and iridophore density appears slightly greater. (2) Stripe, bar and spot chromatophores appear in the skin at metamorphosis. Stripe melanophores directly differentiate along horizontal myosepta into the adult pattern. In contrast, bar number and position are dynamic throughout development. As body length increases, new bars appear between old ones or by splitting of old ones through new melanophore appearance, not migration. Xanthophore and iridophore distributions follow melanophore patterns. (3) Metamorphic pigmentation arises in cichlids in a fashion similar to that described in zebrafish: melanophore progenitors derived from the medial route of neural crest migration migrate from the vicinity of the neural tube to the skin during metamorphosis. Conclusion The three pigment cell types forming stripes, bars and spots arise in the skin at metamorphosis. Stripes develop by differentiation of melanophores along horizontal myosepta, while bars do not develop along patent anatomical boundaries and increase in number in relation with body size. We propose that metamorphic melanophore differentiation and migratory arrest upon arrival to the skin lead to stripe formation, while bar formation must be supported by extensive migration of undifferentiated melanophores in the skin.

Developmental and Cellular Basis of Vertical Bar Color Patterns in the East African Cichlid Fish Haplochromis latifasciatus

“…However, compared to most other bared haplochromine cichlids, the vertical bars in H. latifasciatus are fixed in number (mostly four and in some strains five) and are relatively thick. Our study shows that vertical bar number remains constant over the course of development in H. latifasciatus ( Figures 1F-R, 2D-M and Supplementary Figure S1), which contrasts with a recent study on the Lake Malawi cichlid Copadichromis azureus, a species with unfixed bar number and thinner bars (Hendrick et al, 2019). In C. azureus, vertical bars split during development resulting in an increase of bar number (Hendrick et al, 2019).…”

“…Among teleosts, the zebrafish Danio rerio and the Medaka Oryzias latipes are the main model organisms for investigation of pigmentation (Meyer et al, 1993(Meyer et al, , 1995Kelsh et al, 1996;Nagao et al, 2014;Irion and Nüsslein-Volhard, 2019;Patterson and Parichy, 2019). More recently, African cichlid fishes with their richness in color patterns are increasingly studied to understand the molecular mechanisms of color pattern formation including but not limited to egg spot patterns (Henning and Meyer, 2012;Santos et al, 2014Santos et al, , 2016, blotch patterns (Streelman et al, 2003;Roberts et al, 2009), amelanism (Kratochwil et al, 2019b), horizontal stripe patterns (Ahi and Sefc, 2017;Kratochwil et al, 2018;Hendrick et al, 2019) and pigment distribution more generally (Albertson et al, 2014). And although progress has been made identifying target genes and loci that drive evolutionary diversification in cichlids (Roberts et al, 2009;Kratochwil et al, 2018) and play key roles in adaptation and speciation (Seehausen et al, 1999;Elmer et al, 2009;Maan and Sefc, 2013), the developmental and cellular mechanisms of pigmentation phenotypes have been barely studied.…”

“…For the mechanisms of color pattern formation, mainly (horizontal) stripe patterns have received attention because the most commonly studied "model" teleost, the zebrafish, carries this characteristic pattern. Vertical bars are less studied, with the exception of recent detailed description of the convict cichlid Amatitlania nigrofasciata (Prazdnikov and Shkil, 2019), studies in Amphiprioninae, the anemone fishes (Salis et al, 2018;Roux et al, 2019) and Lake Malawi cichlids (Hendrick et al, 2019). Bar patterns are presumably adaptive as such disruptive coloration breaks the outline of the individual and thereby constitutes a form of camouflage, in particular in visually complex habitats (Seehausen et al, 1999;Maan and Sefc, 2013).…”

Variation on a theme: pigmentation variants and mutants of anemonefish

“…Interactions between zebrafish chromatophores include long-range as well as short-range effects [14,46] such as: (1) iridophores attract melanophores in high numbers and induce their aggregation into prospective stripe areas (positive longrange); (2) iridophores exclude melanophores from interstripes (negative short-range), (3) xanthophores exclude melanophores from interstripes (negative short-range), and (4) positive and negative interactions between iridophores and xanthophores being required to confine the shape of interstripes (short range). Similarly, the addition of bars (vertical main axis) in the cichlid Copadichromis azureus requires cell-cell communication, with xanthophores and iridophores following the pattern of melanophore distribution [18].…”

Neural innervation as a potential trigger of morphological color change and sexual dimorphism in cichlid fish

“…Teleost fishes lend themselves well for studying the developmental and cellular mechanisms and the molecular bases of color and color change phenotypes [12][13][14][15] . With their richness in pigmentation patterns, fishes in the family Cichlidae (cichlid fishes) are an attractive model for studying how genomic changes facilitate variation in molecular and developmental mechanisms and thereby the evolution of pigmentation phenotypes [15][16][17][18][19][20] . Cichlid fishes also offer remarkable examples for morphological color change, color polymorphism and polyphenisms as well as sexual dichromatism, traits that have received much less attention, especially from a molecular and cellular perspective.…”