A common goal in evolutionary biology is to discern the mechanisms that produce the astounding diversity of morphologies seen across the tree of life. Aposematic species, those with a conspicuous phenotype coupled with some form of defence, are excellent models to understand the link between vivid colour pattern variations, the natural selection shaping it, and the underlying genetic mechanisms underpinning this variation. Mimicry systems in which multiple species share the same conspicuous phenotype can provide an even better model for understanding the mechanisms of colour production in aposematic species, especially if comimics have divergent evolutionary histories. Here we investigate the genetic mechanisms by which vivid colour and pattern are produced in a Müllerian mimicry complex of poison frogs. We did this by first assembling a high-quality de novo genome assembly for the mimic poison frog Ranitomeya imitator. This assembled genome is 6.8 Gbp in size, with a contig N50 of 300 Kbp R. imitator and two colour morphs from both Ranitomeya fantastica and R. variabilis which R. imitator mimics. We identified a large number of pigmentation and patterning genes that are differentially expressed throughout development, many of them related to melanocyte development, melanin synthesis, iridophore development and guanine synthesis. Polytypic differences within species may be the result of differences in expression and/or timing of expression, whereas convergence for colour pattern between species does not appear to be due to the same changes in gene expression. In addition, we identify the pteridine synthesis pathway (including genes such as qdpr and xdh) as a key driver of the variation in colour between morphs of these species. Finally, we hypothesize that genes in the keratin family are important for producing different structural colours within these frogs.
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Variation in pigmentation gene expression is associated with distinct aposematic color morphs in the poison frog Dendrobates auratus
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.
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- Award ID(s):
- 1655336
- NSF-PAR ID:
- 10092531
- Date Published:
- Journal Name:
- BMC evolutionary biology
- Volume:
- 19
- Issue:
- 85
- ISSN:
- 1471-2148
- Page Range / eLocation ID:
- 1-15
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract A common goal in evolutionary biology is to discern the mechanisms that produce the astounding diversity of morphologies seen across the tree of life. Aposematic species, those with a conspicuous phenotype coupled with some form of defence, are excellent models to understand the link between vivid colour pattern variations, the natural selection shaping it, and the underlying genetic mechanisms underpinning this variation. Mimicry systems in which multiple species share the same conspicuous phenotype can provide an even better model for understanding the mechanisms of colour production in aposematic species, especially if comimics have divergent evolutionary histories. Here we investigate the genetic mechanisms by which vivid colour and pattern are produced in a Müllerian mimicry complex of poison frogs. We did this by first assembling a high‐quality
de novo genome assembly for the mimic poison frogRanitomeya imitator . This assembled genome is 6.8 Gbp in size, with a contig N50 of 300 KbpR .imitator and two colour morphs from bothRanitomeya fantastica andR .variabilis whichR .imitator mimics. We identified a large number of pigmentation and patterning genes that are differentially expressed throughout development, many of them related to melanocyte development, melanin synthesis, iridophore development and guanine synthesis. Polytypic differences within species may be the result of differences in expression and/or timing of expression, whereas convergence for colour pattern between species does not appear to be due to the same changes in gene expression. In addition, we identify the pteridine synthesis pathway (including genes such asqdpr andxdh ) as a key driver of the variation in colour between morphs of these species. Finally, we hypothesize that genes in the keratin family are important for producing different structural colours within these frogs. -
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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 frog
Oophaga 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, andzic1 have either been identified or implicated as important in coloration in other taxa.Casq1 andprva buffer 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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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/doi.org/10.1186/s12862-019-1410-7
