Blue, Black, and Stripes: Evolution and Development of Color Production and Pattern Formation in Lizards and Snakes

Kuriyama, Takeo; Murakami, Arata; Brandley, Matt; Hasegawa, Masami

doi:10.3389/fevo.2020.00232

Cited by 16 publications

(12 citation statements)

References 105 publications

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“…Knowledge is building up on the development of Squamate pigmentation (McLean et al, 2017;Andrade et al, 2019;Kuriyama et al, 2020;Ullate-Agote et al, 2020), clearly showing that there are similarities with the zebrafish in terms of gene regulation and expression. Thus, it is now important to understand how different chromatophores are specified and migrate in these species.…”

Section: Discussionmentioning

confidence: 99%

Characterization of the Leucistic Texas Rat Snake Pantherophis obsoletus

Ullate-Agote

Tzika

2021

Front. Ecol. Evol.

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Albinism and leucism are phenotypes resulting from impaired melanin pigmentation in the skin and skin appendages. However, melanin pigmentation of eyes remains unaffected in leucism. Here, using transmission electron microscopy, we show that the leucistic morph of the Texas rat snake (Pantherophis obsoletus lindheimeri) lacks both melanophores and xanthophores in its skin and exhibits a uniform ivory white color generated by iridophores and collagen fibers. In addition, we sequenced the full genome of a leucistic individual and obtained a highly-contiguous near-chromosome quality assembly of 1.69 Gb with an N50 of 14.5 Mb and an L50 of 29 sequences. Using a candidate-gene approach, we then identify in the leucistic genome a single-nucleotide deletion that generates a frameshift and a premature termination codon in the melanocyte inducing transcription factor (MITF) gene. This mutation shortens the translated protein from 574 to 286 amino acids, removing the helix-loop-helix DNA-binding domain that is highly conserved among vertebrates. Genotyping leucistic animals of independent lineages showed that not all leucistic individuals carry this single-nucleotide deletion. Subsequent gene expression analyses reveal that all leucistic individuals that we analyzed exhibit a significantly decreased expression of MITF. We thus suggest that mutations affecting the regulation and, in some cases, the coding sequence of MITF, the former probably predating the latter, could be associated with the leucistic phenotype in Texas rat snakes. MITF is involved in the development and survival of melanophores in vertebrates. In zebrafish, a classical model species for pigmentation that undergoes metamorphosis, larvae and adults of homozygous mitfa mutants lack melanophores, show an excess of iridophores and exhibit reduced yellow pigmentation. On the contrary, in the leucistic Texas rat snake, a non-metamorphic species, only iridophores persist. Our results suggest that fate determination of neural-crest derived melanophores and xanthophores, but not of iridophores, could require the expression of MITF during snake embryonic development.

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Section: Discussionmentioning

confidence: 99%

Characterization of the Leucistic Texas Rat Snake Pantherophis obsoletus

Ullate-Agote

Tzika

2021

Front. Ecol. Evol.

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“…In recent decades, the genetic basis of artificially selected variation has begun to be mapped in many organisms used in agriculture, floriculture and the pet trade, including the genetic mapping of a large number of genes responsible for flower color variation ( Park et al 2007 ; Giovannini et al 2021 ), melanin-based coat color in domestic mammals ( Cieslak et al 2011 ), plumage patterns, and colors in birds ( Domyan and Shapiro 2017 ; Price-Waldman and Stoddard 2021 ), and chromatophore distribution in squamates and fishes ( Guo et al 2021 ). These variants can affect genes involved in the enzymatic production, transport, and deposition of pigments such as the melanin and carotenoid pathways ( Mundy et al 2016 ; Courtier-Orgogozo and Martin 2020 ), or can be caused by genes that affect signaling or cell type differentiation [as with chromatophore distribution in squamates ( Kuriyama et al 2020 )]. The extensive set of artificial and domesticated genetic variants has been used repeatedly both for studies of genotype-to-phenotype relationship, and for understanding the genetics of disease states in humans ( Andersson 2016 ).…”

Section: Introductionmentioning

confidence: 99%

A large deletion at the cortex locus eliminates butterfly wing patterning

Hanly

Livraghi

Heryanto

et al. 2022

G3 Genes|Genomes|Genetics

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As the genetic basis of natural and domesticated variation has been described in recent years, a number of hotspot genes have been repeatedly identified as the targets of selection, Heliconius butterflies display a spectacular diversity of pattern variants in the wild and the genetic basis of these patterns has been well-described. Here we sought to identify the mechanism behind an unusual pattern variant that is instead found in captivity, the ivory mutant, in which all scales on both the wings and body become white or yellow. Using a combination of autozygosity mapping and coverage analysis from 37 captive individuals, we identify a 78kb deletion at the cortex wing patterning locus, a gene which has been associated with wing pattern evolution in H. melpomene and 10 divergent lepidopteran species. This deletion is undetected among 458 wild Heliconius genomes samples, and its dosage explains both homozygous and heterozygous ivory phenotypes found in captivity. The deletion spans a large 5’ region of the cortex gene that includes a facultative 5’UTR exon detected in larval wing disk transcriptomes. CRISPR mutagenesis of this exon replicates the wing phenotypes from coding knock-outs of cortex, consistent with a functional role of ivory-deleted elements in establishing scale color fate. Population demographics reveal that the stock giving rise to the ivory mutant has a mixed origin from across the wild range of H. melpomene, and supports a scenario where the ivory mutation occurred after the introduction of cortex haplotypes from Ecuador. Homozygotes for the ivory deletion are inviable while heterozygotes are the targets of artificial selection, joining 40 other examples of allelic variants that provide heterozygous advantage in animal populations under artificial selection by fanciers and breeders. Finally, our results highlight the promise of autozygosity and association mapping for identifying the genetic basis of aberrant mutations in captive insect populations.

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“…2017). Skin color in non-avian reptiles and lower vertebrates is determined by layers of multiple chromatophores (Patterson and Parichy 2019; Kuriyama et al . 2020).…”

Section: Introductionmentioning

confidence: 99%

Stripes and loss of color in ball pythons (Python regius) are associated with variants affecting endothelin signaling

Dao

Lederer

Tabor

et al. 2022

Preprint

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Color patterns in non-avian reptiles are beautifully diverse, but little is known about the genetics and development of these patterns. Here we investigated color patterning in pet ball pythons (Python regius), which have been bred to show color phenotypes that differ dramatically from the wildtype form. We report that several color phenotypes in pet animals are associated with putative loss-of-function variants in the gene encoding endothelin receptor EDNRB1: (i) frameshift variants in EDNRB1 are associated with conversion of the normal mottled color pattern to all-white skin (leucism), (ii) missense variants affecting conserved sites of the EDNRB1 protein are associated with dorsal, longitudinal stripes, and (iii) substitutions at EDNRB1 splice donors are associated with subtle changes in patterning compared to wildtype. We propose that these phenotypes are caused by loss of specialized color cells (chromatophores), with loss ranging from severe (leucism) to moderate (dorsal striping) to mild (subtle changes in patterning). Our study is the first to describe variants affecting endothelin signaling in a non-avian reptile and suggests that reductions in endothelin signaling in ball pythons can produce a variety of color phenotypes, depending on the degree of color cell loss.

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Blue, Black, and Stripes: Evolution and Development of Color Production and Pattern Formation in Lizards and Snakes

Cited by 16 publications

References 105 publications

Characterization of the Leucistic Texas Rat Snake Pantherophis obsoletus

Characterization of the Leucistic Texas Rat Snake Pantherophis obsoletus

A large deletion at the cortex locus eliminates butterfly wing patterning

Stripes and loss of color in ball pythons (Python regius) are associated with variants affecting endothelin signaling

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