Multiple Pigment Cell Types Contribute to the Black, Blue, and Orange Ornaments of Male Guppies (Poecilia reticulata)

Kottler, Verena A.; Koch, Iris; Flötenmeyer, Matthias; Hashimoto, Hisashi; Weigel, Detlef; Dreyer, Christine

doi:10.1371/journal.pone.0085647

Cited by 39 publications

(44 citation statements)

References 61 publications

(114 reference statements)

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“…Similar patterns of organisation have been found in other fish species, though in general chromatophores in teleosts are not necessarily organised into strict layers (Kaleta, ; Kottler et al. ), while many studies (Takahashi & Kondo, ; Inaba et al. ; Frohnhöfer et al.…”

Section: Introductionsupporting

confidence: 60%

Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids

2015

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Skin pigmentation in animals is an important trait with many functions. The present study focused on two closely related salmonid species, marble trout (Salmo marmoratus) and brown trout (S. trutta), which display an uncommon labyrinthine (marble-like) and spot skin pattern, respectively. To determine the role of chromatophore type in the different formation of skin pigment patterns in the two species, the distribution and ultrastructure of chromatophores was examined with light microscopy and transmission electron microscopy. The presence of three types of chromatophores in trout skin was confirmed: melanophores; xanthophores; and iridophores. In addition, using correlative microscopy, erythrophore ultrastructure in salmonids was described for the first time. Two types of erythrophores are distinguished, both located exclusively in the skin of brown trout: type 1 in black spot skin sections similar to xanthophores; and type 2 with a unique ultrastructure, located only in red spot skin sections. Morphologically, the difference between the light and dark pigmentation of trout skin depends primarily on the position and density of melanophores, in the dark region covering other chromatophores, and in the light region with the iridophores and xanthophores usually exposed. With larger amounts of melanophores, absence of xanthophores and presence of erythrophores type 1 and type L iridophores in the black spot compared with the light regions and the presence of erythrophores type 2 in the red spot, a higher level of pigment cell organisation in the skin of brown trout compared with that of marble trout was demonstrated. Even though the skin regions with chromatophores were well defined, not all the chromatophores were in direct contact, either homophilically or heterophilically, with each other. In addition to short-range interactions, an important role of the cellular environment and long-range interactions between chromatophores in promoting adult pigment pattern formation of trout are proposed.

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Section: Introductionsupporting

confidence: 60%

Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids

2015

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“…The ornaments of male guppies are formed by neural crest‐derived melanophores, xanthophores, and iridophores that are arranged in thick layers in the dermis and hypodermis (Fujii, ; Fujii and Taguchi, ; Gundersen and Rivera, ; Kottler et al., , ; Sauka‐Spengler and Bronner‐Fraser, ; Takeuchi, , ). Female guppies, which lack conspicuous colors, are camouflaged by a net‐like reticulate pattern that covers the whole body (Goodrich et al., ; Kottler et al., , ; Tripathi et al., ). This pattern is composed of large, corolla melanophores interspersed with xanthophores and iridophores (Figure A) (Goodrich et al., ; Kottler et al., , ).…”

Section: Introductionmentioning

confidence: 99%

“…Female guppies, which lack conspicuous colors, are camouflaged by a net‐like reticulate pattern that covers the whole body (Goodrich et al., ; Kottler et al., , ; Tripathi et al., ). This pattern is composed of large, corolla melanophores interspersed with xanthophores and iridophores (Figure A) (Goodrich et al., ; Kottler et al., , ). A second type of melanophores, called dendritic, is associated with more superficial skin layers close to the scales (Figure A,B) (Goodrich et al., ; Kottler et al., , ).…”

Section: Introductionmentioning

confidence: 99%

“…This pattern is composed of large, corolla melanophores interspersed with xanthophores and iridophores (Figure A) (Goodrich et al., ; Kottler et al., , ). A second type of melanophores, called dendritic, is associated with more superficial skin layers close to the scales (Figure A,B) (Goodrich et al., ; Kottler et al., , ). Dendritic and some corolla melanophores are distributed irregularly over the whole body of males and females (Figure A) (Goodrich et al., ).…”

Section: Introductionmentioning

confidence: 99%

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Adenylate cyclase 5is required for melanophore and male pattern development in the guppy (Poecilia reticulata)

Kottler

Künstner

Koch

et al. 2015

Pigment Cell Melanoma Res

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Guppies (Poecilia reticulata) are colorful fish that have attracted the attention of pigmentation researchers for almost a century. Here, we report that the blond phenotype of the guppy is caused by a spontaneous mutation in the guppy ortholog of adenylate cyclase 5 (adcy5). Using double digest restriction site-associated DNA sequencing (ddRADseq) and quantitative trait locus (QTL) mapping, we linked the blond phenotype to a candidate region of 118 kb, in which we subsequently identified a 2-bp deletion in adcy5 that alters splicing and leads to a premature stop codon. We show that adcy5, which affects life span and melanoma growth in mouse, is required for melanophore development and formation of male orange pigmentation traits in the guppy. We find that some components of the male orange pattern are particularly sensitive to loss of Adcy5 function. Our work thus reveals a function for Adcy5 in patterning of fish color ornaments.

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“…This occurs either as the result of 125 direct modification by Pb, or indirectly through interactions as a result of 126 xanthophore reductions or removal (Kottler 2013(Kottler , 2014(Kottler , 2015. Overall 127 dendritic melanophore structure is of a much "finer" appearance as 128 compared to non-Pb.…”

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confidence: 99%

The Cellular Expression and Genetics of Purple Body (Pb) inPoecilia reticulata, and its Interactions with Asian Blau (Ab) and Blond (bb) under Reflected and Transmitted Light

Squire

2017

Preprint

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Mature Purple Body and Non-Purple Body male guppies differ from each other in several ways. Non-Purple males may have large numbers of xanthophores, erythrophores, and blue iridophores, in addition to the usual dendritic, corolla and punctate melanophores. Fewer violet iridophores are found. In contrast, homozygous Purple Body males lack collected and clustered xanthophores, although isolated single xanthophores remain. Violet iridophores and blue iridophores (violet-blue chromatophores units) abound. The dendrites of dendritic melanophores are finer and form chains with each other. Punctate and corolla melanophores in areas comprising orange ornaments are greatly reduced in number. The heterozygous Purple Body male has erythrophores similar to those of non-Purple males, but yellow pigment is reduced. The melanophores are not as greatly changed in orange ornaments. In Domestic Guppy strains, and at least in one suspected instance in wild-type, melanophore structure and populations may be further modified by one or more additional autosomal genes.

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Multiple Pigment Cell Types Contribute to the Black, Blue, and Orange Ornaments of Male Guppies (Poecilia reticulata)

Cited by 39 publications

References 61 publications

Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids

Comparison of pigment cell ultrastructure and organisation in the dermis of marble trout and brown trout, and first description of erythrophore ultrastructure in salmonids

Adenylate cyclase 5is required for melanophore and male pattern development in the guppy (Poecilia reticulata)

The Cellular Expression and Genetics of Purple Body (Pb) inPoecilia reticulata, and its Interactions with Asian Blau (Ab) and Blond (bb) under Reflected and Transmitted Light

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