A quantitative modelling approach to zebrafish pigment pattern formation

Owen, Jennifer P.; Kelsh, Robert N.; Yates, Christian A.

doi:10.7554/elife.52998

“…Silver staining and micro-CT imaging may more thoroughly describe zebrafish mutants that have already been identified with effects on larval, juvenile, and adult pigmentation (Parichy, 2006), and our work with the nacre / casper zebrafish highlights the potential to identify new mutants with subtler effects on pigment localization or concentration. Zebrafish are frequently used for studying complex animal pigmentation patterning, including computational models of pigment cell interactions (Owen et al, 2020) or studies of human skin color (Lamason et al, 2005). High-resolution, whole-animal 3D images of melanin could help experimentally confirm such studies.…”

Section: Resultsmentioning

confidence: 99%

Whole-organism 3D Quantitative Characterization of Zebrafish Melanin by Silver Deposition Micro-CT

Katz¹,

Yakovlev²,

Vanselow³

et al. 2021

Preprint

1

0

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Melanin-rich zebrafish melanophores are used to study pigment development, human skin color, and as a large-scale screening phenotype. To facilitate more detailed whole-body, computational analyses of melanin content and morphology, we have combined X-ray microtomography (micro-CT), a non-destructive, full-volume imaging modality, with a novel application of ionic silver staining to characterize melanin distribution in whole zebrafish larvae. Normalized micro-CT reconstructions of silver-stained fish consistently reproduced pigment patterns seen by light microscopy, and allowed direct quantitative comparisons of melanin content across wild-type and mutant samples, for both dramatic and subtle phenotypes not previously described. Silver staining of melanin for micro-CT provides proof-of-principle for whole-body, three-dimensional computational phenomic analysis of a particular cell type at cellular resolution, with potential applications in other model organisms and human melanoma biopsies. Whole-organism, high-resolution phenotyping is a challenging ideal, but provides superior context for functional studies of mutations, diseases, and environmental influences.

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“…The current understanding of adult pigment pattern development in D. rerio has been informed by dozens of mutants [4,5,17,23,32,[34][35][36][37][38][39][40][41][42][43]. Yet it remains unclear if mutants isolated in the laboratory are representative of natural variation within or between species.…”

Section: Top)mentioning

confidence: 99%

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

McCluskey

¹

,

Uji

²

,

Mancusi

³

et al. 2021

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Vertebrate 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.

show abstract

“…The current understanding of adult pigment pattern development in D. rerio has been informed by dozens of mutants [4,5,16,22,31,[33][34][35][36][37][38][39][40][41][42]. Yet it remains unclear if mutants isolated in the laboratory are representative of natural variation within or between species.…”

Section: Introductionmentioning

confidence: 99%

A complex genetic architecture in zebrafish relativesDanio quaggaandD. kyathitunderlies development of stripes and spots

McCluskey

¹

,

Uji

²

,

Mancusi

³

et al. 2021

Preprint

View full text Add to dashboard Cite

Vertebrate 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.

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A quantitative modelling approach to zebrafish pigment pattern formation

Cited by 53 publications

References 64 publications

Whole-organism 3D Quantitative Characterization of Zebrafish Melanin by Silver Deposition Micro-CT

Whole-organism 3D Quantitative Characterization of Zebrafish Melanin by Silver Deposition Micro-CT

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

A complex genetic architecture in zebrafish relativesDanio quaggaandD. kyathitunderlies development of stripes and spots

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