Evolution of pigment cells and patterns: recent insights from teleost fishes

Abstract

Skin pigment patterns of vertebrates are stunningly diverse, and nowhere more so than in teleost fishes. Several species, including relatives of zebrafish, recently evolved cichlid fishes of East Africa, clownfishes, deep sea fishes, and others are providing insights into pigment pattern evolution. This overview describes recent advances in understanding periodic patterns, like stripes and spots, the loss of patterns, and the role of cell-type diversification in generating pigmentation phenotypes. Advances in this area are being facilitated by the application of modern methods of gene editing, genomics, computational analysis, and other approaches to non-traditional model organisms having interesting pigmentary phenotypes. Several topics worthy of future attention are outlined as well.

Figure 1

Periodic pattern development and evolution. (a) In zebrafish, D. rerio, dark stripes consist of melanophores (dark grey) and bluish iridophores with ordered reflecting platelets (blue), Light interstripes have densely packed yellowish iridophores with disordered reflecting platelets (yellow) and mature xanthophores (orange). Most melanophores derive from post-embryonic progenitors that differentiate during the larva-to-adult transition but some develop directly from neural crest cells and persist from the embryonic pattern (brown). Some immature xanthophores occur within stripes (pale yellow cells). (b) During post-embryonic development, cues from the tissue environment (arrow, upper left) allow iridophores to differentiate in a first interstripe after which interactions among chromatotophores drive pattern implementation, refinement, and reiteration. Some interactions have positive effects on differentiation, survival or localization (arrows), others have negative effects (bars), some are at short range (black arrows/bars) whereas others are at long range (grey arrows/bars). Iridophores of interstripes and stripes are disinct subclasses (see text). During pattern formation and homeostasis the tissue environment also provide supportive factors that regulate differentiation, survival, and proliferation (small grey circles). Summarized from [9,10,11,12•]. (c) Patten variation in Danio showing interstripes and stripes of wild-type D. rerio, and defective pattern in a mutant for colony stimulating factor 1 receptor that lacks xanthophores, and, therefore the chromatophore interactions in which xanthophores particiate. Also shown are naturally occurring patterns of other danios mentioned in main text, D. albolineatus, D. nigrofasciatus, D. aesculapii, and D. margaritatus. (d) In many African cichlids, horizonal stripes (arrow) are found on the flank and these species have lower levels of agrp2 expression (upper). When agrp2 is inactivated in a species that lacks distinct horizontal stripes, an ectopic stripe is formed (arrow, lower; modified from [25••]) (e) Theory predicts a labyrinthine transitional state between light and dark spots (left). In actual pufferfishes, genomic analyses support the notion of ancestral hybridization in labyrinthine species (modified from [38••].

Figure 2

Uniform pigmentation when light is absent. (a) The ultra-black bathypelagic fish Oneirodes eschrichtii, illustrating dark integument and lure for catching prey. Inset, scanning electron micrograph showing melanosomes (m), amongst collagen fibrils (arrowhead), beneath the epidermis (e; modified from [39••]). (b) Preserved speciments of the albino cave cichlid Lamprologus lethops (top) and a closely related surface species L. teugelsi (bottom). Photo credits, © Danté Fenolio, DEEPEND project, used with permission (a) and Melanie Stiassny (b).

Figure 3

Chromatophore diversity. (a) The flank of a wild-type zebrafish, illustrating locations of cells shown in b, c, and d. (b) Melanoleucophores (ML) with white deposits of crystalline guanine. Some of these cells, still losing the melanin derived from their melanophore precursors, are also evident (arrowhead). (c) Two of the three described classes of iridophores. I_D have disordered arrangements of reflecting platelets, occur densely packed in interstripes and have an intrinsically yellow hue. I_O have ordered arrangements of larger reflecting platelets, are sparsely arranged within stripes, and are able to change their hue physiologically from blue to yellow [12•]. Cells shown are in a mutant that lacks melanin and carotenoids, making melanophores and xanthophores invisible. (d) Xantholeucophores (XL) in the anal fin with orange carotenoids centrally and white deposits peripherally. Some fin iridophores are evident as well. Inset shows loss of orange coloration in a scarb1 mutant defective in localizing carotenoid pigments. (e) Red erythrophores (E) and orange xanthophores (X) in the fin of D. albolineatus. Fish in b, d and e were treated with epinephrine to mimic a natural physiological response in which pigment granules contract towards cell centers, allowing easier visualization. (f) Blue cyanophores (C) in the fin of Mandarin fish, Synchiropus splendidus (Figure 4d, top left). (g–i) Transmission electron micrographs illustrating subcellular differences in membrane-bound guanine crystal (GC) arrangements that give a matte white appearance to zebrafish melanoleucophores (g). When crystals tale the form of flat reflecting platelets (RP) in stacks, they can lead to iridescence, as in a zebrafish fin iridophore (h), or a matte white appearance, as in clownfish (i and Figure 4d, top middle). (j) In Pseudochromis diadema, irregularly oriented reflecting platelets are combined with carotenoids in the same cell to generate a matte violet (Figure 4d top right). Photo credits, [51] (f), [47•] (g), [52] (j). Scale bar in b for b–f, 50 μm; in g for g and h, 500 nm; in i for i and j, 2 μm.

Figure 4

Pattern variation within and between species. (a) Different positions and numbers of ornaments across three male guppies (melanophores, black arrowhead; xanthophores, brown arrowhead). (b) Egg dummies in the fins of Astatotilapia burtoni and Astatoreochromis straeleni. (c) In Anampses chyrsocephalus females (top) and males (bottom) are so different they were thought to be different species. (d) Reef fishes, from upper left: clownfish A. ocelaris, mandarinfish Synchiropus splendidus, P. diadema, Balistoides conspicillum, Xanichthys mento^T, Choerodon fasciatus^T, Parupeneus barberinoides^R, Centropyge bicolor^R, Thalassoma rueppellii^R, Apolemichthys arcuatus^T, Chaetodontoplus duboulayi^T, Rhincanthus abyssus^T, Chaetodon larvatus^R, Chaetodon ornatissimus^T, Chaetodon collare^T. Images courtesy: Lengxob Yong (a); modified from [55] (b); John E. Randall (c); ^T, Yi-Kai Tea, ^R, Luiz Rocha (d).