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Abstract Skin coloration and patterning play a key role in animal survival and reproduction. As a result, color phenotypes have generated intense research interest. In aposematic species, color phenotypes can be important in avoiding predation and in mate choice. However, we still know little about the underlying genetic mechanisms of color production, particularly outside of a few model organisms. Here we seek to understand the genetic mechanisms underlying the production of different colors and how these undergo shifting expression patterns throughout development. To answer this, we examine gene expression of two different color patches(yellow and green) in a developmental time series from young tadpoles through adults in the poison frogOophaga pumilio.We identified six genes that were differentially expressed between color patches in every developmental stage (casq1, hand2, myh8, prva, tbx3,andzic1).Of these,hand2, myh8, tbx3,andzic1have either been identified or implicated as important in coloration in other taxa.Casq1andprvabuffer Ca2+and are a Ca2+transporter, respectively, and may play a role in preventing autotoxicity to pumiliotoxins, which inhibit Ca2+-ATPase activity. We identify further candidate genes (e.g.,adh, aldh1a2, asip, lef1, mc1r, tyr, tyrp1, xdh), and identify a suite of hub genes that likely play a key role in integumental reorganization during development (e.g., collagen type I–IV genes, lysyl oxidases) which may also affect coloration via structural organization of chromatophores that contribute to color and pattern. Overall, we identify the putative role of a suite of candidate genes in the production of different color types in a polytypic, aposematic species.
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Piebaldism and chromatophore development in reptiles are linked to the tfec gene
Reptiles display great diversity in color and pattern, yet much of what we know about vertebrate coloration comes from classic model species such as the mouse and zebrafish. Captive-bred ball pythons (Python regius) exhibit a remarkable degree of color and pattern variation. Despite the wide range of Mendelian color phenotypes available in the pet trade, ball pythons remain an overlooked species in pigmentation research. Here, we investigate the genetic basis of the recessive piebald phenotype, a pattern defect characterized by patches of unpigmented skin (leucoderma). We performed whole-genome sequencing and used a case-control approach to discover a nonsense mutation in the gene encoding the transcription factor tfec, implicating this gene in the leucodermic patches in ball pythons. We functionally validated tfec in a lizard model (Anolis sagrei) using the gene editing CRISPR/Cas9 system and TEM imaging of skin. Our findings show that reading frame mutations in tfec affect coloration and lead to a loss of iridophores in Anolis, indicating that tfec is required for chromatophore development. This study highlights the value of captive-bred ball pythons as a model species for accelerating discoveries on the genetic basis of vertebrate coloration.
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- Award ID(s):
- 1827647
- PAR ID:
- 10486606
- Publisher / Repository:
- Cell Press
- Date Published:
- Journal Name:
- Current Biology
- Volume:
- 33
- Issue:
- 4
- ISSN:
- 0960-9822
- Page Range / eLocation ID:
- 755 to 763.e3
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Background: Color and pattern phenotypes have clear implications for survival and reproduction in many species. However, the mechanisms that produce this coloration are still poorly characterized, especially at the genomic level. Here we have taken a transcriptomics-based approach to elucidate the underlying genetic mechanisms affecting color and pattern in a highly polytypic poison frog. We sequenced RNA from the skin from four different color morphs during the final stage of metamorphosis and assembled a de novo transcriptome. We then investigated differential gene expression, with an emphasis on examining candidate color genes from other taxa. Results: Overall, we found differential expression of a suite of genes that control melanogenesis, melanocyte differentiation, and melanocyte proliferation (e.g., tyrp1, lef1, leo1, and mitf) as well as several differentially expressed genes involved in purine synthesis and iridophore development (e.g., arfgap1, arfgap2, airc, and gart). Conclusions: Our results provide evidence that several gene networks known to affect color and pattern in vertebrates play a role in color and pattern variation in this species of poison frog.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1016/j.cub.2023.01.004
