Zebrafish Pigment Pattern Formation: Insights into the Development and Evolution of Adult Form

2019 ◽  
Vol 53 (1) ◽  
pp. 505-530 ◽  
Author(s):  
Larissa B. Patterson ◽  
David M. Parichy
Keyword(s):  
Pattern Formation ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Pigment Cells ◽  
Cellular Interactions ◽  
Lineage Specification ◽  
Pigment Pattern ◽  
Adult Form ◽  
Pattern Development ◽  
Pigment Patterns

Vertebrate pigment patterns are diverse and fascinating adult traits that allow animals to recognize conspecifics, attract mates, and avoid predators. Pigment patterns in fish are among the most amenable traits for studying the cellular basis of adult form, as the cells that produce diverse patterns are readily visible in the skin during development. The genetic basis of pigment pattern development has been most studied in the zebrafish, Danio rerio. Zebrafish adults have alternating dark and light horizontal stripes, resulting from the precise arrangement of three main classes of pigment cells: black melanophores, yellow xanthophores, and iridescent iridophores. The coordination of adult pigment cell lineage specification and differentiation with specific cellular interactions and morphogenetic behaviors is necessary for stripe development. Besides providing a nice example of pattern formation responsible for an adult trait of zebrafish, stripe-forming mechanisms also provide a conceptual framework for posing testable hypotheses about pattern diversification more broadly. Here, we summarize what is known about lineages and molecular interactions required for pattern formation in zebrafish, we review some of what is known about pattern diversification in Danio, and we speculate on how patterns in more distant teleosts may have evolved to produce a stunningly diverse array of patterns in nature.

An orthologue of the kit-related gene fms is required for development of neural crest-derived xanthophores and a subpopulation of adult melanocytes in the zebrafish, Danio rerio

Development ◽  
2000 ◽  
Vol 127 (14) ◽  
pp. 3031-3044 ◽  
Author(s):  
D.M. Parichy ◽  
D.G. Ransom ◽  
B. Paw ◽  
L.I. Zon ◽  
S.L. Johnson
Keyword(s):  
Neural Crest ◽  
Danio Rerio ◽  
Receptor Tyrosine Kinase ◽  
Pigment Cell ◽  
Pigment Cells ◽  
Pigment Pattern ◽  
Cell Behaviors ◽  
Pattern Development ◽  
And Migration ◽  
Pigment Patterns

Developmental mechanisms underlying traits expressed in larval and adult vertebrates remain largely unknown. Pigment patterns of fishes provide an opportunity to identify genes and cell behaviors required for postembryonic morphogenesis and differentiation. In the zebrafish, Danio rerio, pigment patterns reflect the spatial arrangements of three classes of neural crest-derived pigment cells: black melanocytes, yellow xanthophores and silver iridophores. We show that the D. rerio pigment pattern mutant panther ablates xanthophores in embryos and adults and has defects in the development of the adult pattern of melanocyte stripes. We find that panther corresponds to an orthologue of the c-fms gene, which encodes a type III receptor tyrosine kinase and is the closest known homologue of the previously identified pigment pattern gene, kit. In mouse, fms is essential for the development of macrophage and osteoclast lineages and has not been implicated in neural crest or pigment cell development. In contrast, our analyses demonstrate that fms is expressed and required by D. rerio xanthophore precursors and that fms promotes the normal patterning of melanocyte death and migration during adult stripe formation. Finally, we show that fms is required for the appearance of a late developing, kit-independent subpopulation of adult melanocytes. These findings reveal an unexpected role for fms in pigment pattern development and demonstrate that parallel neural crest-derived pigment cell populations depend on the activities of two essentially paralogous genes, kit and fms.

scholarly journals Differential growth is a critical determinant of zebrafish pigment pattern formation

2021 ◽  
Author(s):  
Robert N. Kelsh ◽  
Jennifer P. Owen ◽  
Christian A. Yates
Keyword(s):  
Pattern Formation ◽  
Pigment Cell ◽  
Model Organism ◽  
Cell Types ◽  
Wild Type ◽  
Differential Growth ◽  
Critical Determinant ◽  
Pigment Pattern ◽  
Pattern Development ◽  
Mechanistic Basis

The skin patterns of vertebrates are formed by complex interactions between pigment-producing cells during development. Adult zebrafish (Danio rerio), a model organism for investigating the underlying patterning processes, display alternating horizontal blue and golden stripes, generated by the self-organisation of three pigment cell-types. Mathematical studies in which these cells are modelled as individual agents communicating via short- and long-range interactions have produced breakthroughs in the understanding of pattern development. These models, incorporating all experimentally evidenced cell-cell interactions, replicate many aspects of wild-type and mutant zebrafish patterns. Although received wisdom suggested that initial iridophore distribution was pivotal in orienting patterning, here we show that growth can override its influence. Altered growth sequences can generate further pattern modulation, including vertical stripes and maze-like patterns. We demonstrate that ventrally-biased (asymmetric) growth of the skin field explains two key zebrafish pattern development features which are otherwise obscure (dorso-ventral pattern asymmetry, and predominant ventral-to-dorsal migration of melanophores) in wild-type and multiple zebrafish mutants, and in the related species Danio nigrofasciatus. By identifying biased growth as a novel patterning mechanism, our study will inform future investigations into the mechanisms and evolution of fish pigment patterning and vertebrate pigment pattern formation. Furthermore, our work has implications for the mechanistic basis of human pigmentation defects.

scholarly journals Evolution of Endothelin signaling and diversification of adult pigment pattern in Danio fishes

2018 ◽  
Author(s):  
Jessica E. Spiewak ◽  
Emily J. Bain ◽  
Jin Liu ◽  
Kellie Kou ◽  
Samantha L. Sturiale ◽  
...  
Keyword(s):  
Pigment Cell ◽  
Pigment Cells ◽  
Close Relative ◽  
Cellular Mechanisms ◽  
Cell Behaviors ◽  
Adult Form ◽  
Evolutionary Changes ◽  
Endothelin 3 ◽  
Skin Pigment ◽  
Pigment Patterns

AbstractFishes of the genus Danio exhibit diverse pigment patterns that serve as useful models for understanding the genes and cell behaviors underlying the evolution of adult form. Among these species, zebrafish D. rerio exhibit several dark stripes of melanophores with sparse iridophores that alternate with light interstripes of dense iridophores and xanthophores. By contrast, the closely related species D. nigrofasciatus has an attenuated pattern with fewer melanophores, stripes and interstripes. Here we demonstrate species differences in iridophore development that presage the fully formed patterns. Using genetic and transgenic approaches we identify the secreted peptide Endothelin-3 (Edn3)—a known melanogenic factor of tetrapods—as contributing to reduced iridophore proliferation and fewer stripes and interstripes in D. nigrofasciatus. We further show the locus encoding this factor is expressed at lower levels in D. nigrofasciatus owing to cis-regulatory differences between species. Finally, we show that functions of two paralogous loci encoding Edn3 have been partitioned between skin and non-skin iridophores. Our findings reveal genetic and cellular mechanisms contributing to pattern differences between these species and suggest a model for evolutionary changes in Edn3 requirements across vertebrates.Author SummaryNeural crest derived pigment cells generate the spectacular variation in skin pigment patterns among vertebrates. Mammals and birds have just a single skin pigment cell, the melanocyte, whereas ectothermic vertebrates have several pigment cells including melanophores, iridophores and xanthophores, that together organize into a diverse array of patterns. In the teleost zebrafish, Danio rerio, an adult pattern of stripes depends on interactions between pigment cell classes and between pigment cells and their tissue environment. The close relative, D. nigrofasciatus has fewer stripes and prior analyses suggested a difference between these species that lies extrinsic to the pigment cells themselves. A candidate for mediating this difference is Endothelin-3 (Edn3), essential for melanocyte development in warm-blooded animals, and required by all three classes of pigment cells in an amphibian. We show that Edn3 specifically promotes iridophore development in Danio, and that differences in Edn3 expression contribute to differences in iridophore complements, and striping, between D. rerio and D. nigrofasciatus. Our study reveals a novel function for Edn3 and provides new insights into how changes in gene expression yield morphogenetic outcomes to effect diversification of adult form.

scholarly journals A complex genetic architecture in zebrafish relatives Danio quagga and D. kyathit underlies development of stripes and spots

2021 ◽  
Author(s):  
Braedan M. McCluskey ◽  
Susumu Uji ◽  
Joseph L. Mancusi ◽  
John H. Postlethwait ◽  
David M. Parichy
Keyword(s):  
Genetic Architecture ◽  
Genetic Basis ◽  
Evolutionary Genetics ◽  
Sister Species ◽  
Pigment Cells ◽  
Induced Mutations ◽  
Pigment Pattern ◽  
Wide Range ◽  
Pattern Development ◽  
Pigment Patterns

AbstractVertebrate pigmentation is a fundamentally important, multifaceted phenotype. Zebrafish, Danio rerio, has been a valuable model for understanding genetics and development of pigment pattern formation due to its genetic and experimental tractability, advantages that are shared across several Danio species having a striking array of pigment patterns. Here, we use the sister species D. quagga and D. kyathit, with stripes and spots, respectively, to understand how natural genetic variation impacts phenotypes at cellular and organismal levels. We first show that D. quagga and D. kyathit phenotypes resemble those of wild-type D. rerio and several single locus mutants of D. rerio, respectively, in a morphospace defined by pattern variation along dorsoventral and anteroposterior axes. We then identify differences in patterning at the cellular level between D. quagga and D. kyathit by repeated daily imaging during pattern development and quantitative comparisons of adult phenotypes, revealing that patterns are similar initially but diverge ontogenetically. To assess the genetic architecture of these differences, we employ reduced-representation sequencing of second-generation hybrids. Despite the similarity of D. quagga to D. rerio, and D. kyathit to some D. rerio mutants, our analyses reveal a complex genetic basis for differences between D. quagga and D. kyathit, with several quantitative trait loci contributing to variation in overall pattern and cellular phenotypes, epistatic interactions between loci, and abundant segregating variation within species. Our findings provide a window into the evolutionary genetics of pattern-forming mechanisms in Danio and highlight the complexity of differences that can arise even between sister species. Further studies of natural genetic diversity underlying pattern variation in D. quagga and D. kyathit should provide insights complementary to those from zebrafish mutant phenotypes and more distant species comparisons.Author SummaryPigment patterns of fishes are diverse and function in a wide range of behaviors. Common pattern themes include stripes and spots, exemplified by the closely related minnows Danio quagga and D. kyathit, respectively. We show that these patterns arise late in development owing to alterations in the development and arrangements of pigment cells. In the closely related model organism zebrafish (D. rerio) single genes can switch the pattern from stripes to spots. Yet, we show that pattern differences between D. quagga and D. kyathit have a more complex genetic basis, depending on multiple genes and interactions between these genes. Our findings illustrate the importance of characterizing naturally occuring genetic variants, in addition to laboratory induced mutations, for a more complete understanding of pigment pattern development and evolution.

Origin and behaviour of pigment cells in sea urchin embryos

Zygote ◽  
1999 ◽  
Vol 8 (S1) ◽  
pp. S42-S43 ◽  
Author(s):  
Tetsuya Kominami
Keyword(s):  
Sea Urchin ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Pigment Cells ◽  
Cleavage Stage ◽  
Fate Map ◽  
Blastula Stage ◽  
Cell Stage ◽  
Stage Embryo ◽  
Founder Cells

Sea urchin pluteus larvae contain dozens of pigment cells in their ectoderm. These pigment cells are the descendants of the veg2 blastomeres of the 60-cell stage embryo. According to the fate map made by Ruffins and Ettensohn, the prospective pigment cells occupy the central region of the vegetal plate. Most of these prospective pigment cells exclusively give rise to pigment cells. Therefore, specification of the pigment cell lineage should occur at some point between the 60-cell and mesenchyme blastula stage. However, the detailed process of the specification of the pigment lineage is unknown.When are pigment cells specified? Are cell interactions necessary for the specification? Do founder cells exist? To answer these questions, I treated embryos with Ca2+-free seawater during the cleavage stage and examined the number of pigment cells observed in pluteus larvae. Treatment at 5.5–8.5 h and especially 7.5–10.5 h postfertilisation markedly reduced the number of pigment cells. The decrease was statistically significant. On the other hand, the treatment at 3.5–6.5 h or 9.5–12.5 h never reduced the number of pigment cells. By examining the frequency of the appearance of embryos whose numbers of pigment cells were less than 20, it was also found that the numbers of pigment cells were frequently in multiples of 4. Embryos having 4, 8, 12, 16 and 20 pigment cells were more frequently observed. Statistics indicated that the frequency of appearance was not random. These results indicated that cell contacts are necessary for the specification of pigment cells and that the specification occurs from 7 to 10 h postfertilisation. The results also suggest that the founder cells, if they exist, divide twice before they differentiate into pigment cells.

Mechanisms of pigment pattern formation in the quail embryo

Development ◽  
1990 ◽  
Vol 109 (1) ◽  
pp. 81-89 ◽  
Author(s):  
M.K. Richardson ◽  
A. Hornbruch ◽  
L. Wolpert
Keyword(s):  
Pattern Formation ◽  
Neural Crest ◽  
Larval Fish ◽  
Dorsal Surface ◽  
Neural Crest Cells ◽  
Mirror Image ◽  
Differential Migration ◽  
Pigment Pattern ◽  
Pigment Patterns ◽  
Local Cues

One hypothesis to account for pigment patterning in birds is that neural crest cells migrate into all feather papillae. Local cues then act upon the differentiation of crest cells into melanocytes. This hypothesis is derived from a study of the quail-chick chimaera (Richardson et al., Development 107, 805–818, 1989). Another idea, derived from work on larval fish and amphibia, is that pigment patterns arise from the differential migration of crest cells. We want to know which of these mechanisms can best account for pigment pattern formation in the embryonic plumage of the quail wing. Most of the feather papillae on the dorsal surface of the wing are pigmented, while many on the ventral surface are white. When ectoderm from unpigmented feather papillae is grown in culture, it gives rise to melanocytes. This indicates that neural crest cells are present in white feathers but that they fail to differentiate. If the wing tip is inverted experimentally then the pigment pattern is inverted also. This is difficult to explain in terms of a model based on migratory pathways, unless one assumes that the pathways became re-routed. When an extra polarizing region is grafted to the anterior margin of the wing bud, a duplication develops in: (1) the pattern of skeletal elements; (2) the pattern of feather papillae; (3) the feather pigment pattern. The pigment pattern was not a precise mirror image although some groups of papillae showed a high degree of symmetry in their pigmentation. Both the tip inversions and the duplications produce discontinuities in the feather and pigment patterns. No evidence of intercalation was found in these cases. We conclude that pigment patterning in birds is determined by local cues acting on melanocyte differentiation, rather than by the differential migration of crest cells. Positional values along the anteroposterior axis of the pigment pattern are determined by a gradient of positional information. Thus the pigment patterns, feather patterns and cartilage patterns of the wing may all be specified by a similar mechanism.

scholarly journals Modelling stripe formation in zebrafish: an agent-based approach

2015 ◽  
Vol 12 (112) ◽  
pp. 20150812 ◽  
Author(s):  
Alexandria Volkening ◽  
Björn Sandstede
Keyword(s):  
Laser Ablation ◽  
Pattern Formation ◽  
Long Range ◽  
Pigment Cell ◽  
Experimental Results ◽  
Fish Growth ◽  
Pigment Cells ◽  
Stripe Pattern ◽  
Agent Based ◽  
Long Range Interactions

Zebrafish have distinctive black stripes and yellow interstripes that form owing to the interaction of different pigment cells. We present a two-population agent-based model for the development and regeneration of these stripes and interstripes informed by recent experimental results. Our model describes stripe pattern formation, laser ablation and mutations. We find that fish growth shortens the necessary scale for long-range interactions and that iridophores, a third type of pigment cell, help align stripes and interstripes.

scholarly journals Macromere cell fates during sea urchin development

Development ◽  
1991 ◽  
Vol 113 (4) ◽  
pp. 1085-1091 ◽  
Author(s):  
R.A. Cameron ◽  
S.E. Fraser ◽  
R.J. Britten ◽  
E.H. Davidson
Keyword(s):  
Sea Urchin ◽  
Pigment Cell ◽  
Cell Lineage ◽  
Cell Types ◽  
Cellular Migration ◽  
The Other ◽  
Pigment Cells ◽  
Basal Cells ◽  
Cell Fates ◽  
Gut Pigment

This paper examines the cell lineage relationships and cell fates in embryos of the sea urchin Strongylocentrotus purpuratus leading to the various cell types derived from the definitive vegetal plate territory or the veg2 tier of cells. These cell types are gut, pigment cells, basal cells and coelomic pouches. They are cell types that constitute embryonic structures through cellular migration or rearrangement unlike the relatively non-motile ectoderm cell types. For this analysis, we use previous knowledge of lineage to assign macromeres to one of four types: VOM, the oral macromere; VAM, the aboral macromere, right and left VLM, the lateral macromeres. Each of the four macromeres contributes progeny to all of the cell types that descend from the definitive vegetal plate. Thus in the gut each macromere contributes to the esophagus, stomach and intestine, and the stripe of labeled cells descendant from a macromere reflects the re-arrangement of cells that occurs during archenteron elongation. Pigment cell contributions exhibit no consistent pattern among the four macromeres, and are haphazardly distributed throughout the ectoderm. Gut and pigment cell contributions are thus radially symmetrical. In contrast, the VOM blastomere contributes to both of the coelomic pouches while the other three macromeres contribute to only one or the other pouch. The total of the macromere contribution amounts to 60% of the cells constituting the coelomic pouches.

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