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1. RETRACTED: The genomics of mimicry: Gene expression throughout development provides insights into convergent and divergent phenotypes in a Müllerian mimicry system

   https://doi.org/10.1111/mec.16024  

   Stuckert, Adam M. M. ; Chouteau, Mathieu ; McClure, Melanie ; LaPolice, Troy M. ; Linderoth, Tyler ; Nielsen, Rasmus ; Summers, Kyle ; MacManes, Matthew D. ( July 2021 , Molecular Ecology)

   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‐qualityde novogenome assembly for the mimic poison frogRanitomeya imitator. This assembled genome is 6.8 Gbp in size, with a contig N50 of 300 KbpR. imitatorand two colour morphs from bothRanitomeya fantasticaandR. variabiliswhichR. imitatormimics. 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 asqdprandxdh) 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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2. Variation in pigmentation gene expression is associated with distinct aposematic color morphs in the poison frog Dendrobates auratus

   https://doi.org/doi.org/10.1186/s12862-019-1410-7  

   Stuckert, A.M.M. ( April 2019 , BMC evolutionary biology)

   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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3. Evidence for a Parabasalian Gut Symbiote in Egg-Feeding Poison Frog Tadpoles in Peru

   https://doi.org/10.1007/s11692-023-09602-7  

   Weinfurther, K. D. ; Stuckert, A. M. M. ; Muscarella, M. E. ; Peralta, A. L. ; Summers, K. ( April 2023 , Evolutionary Biology)

   We report preliminary evidence of a symbiotic parabasalian protist in the guts of Peruvian mimic poison frog (Ranitomeya imitator) tadpoles. This species has biparental care and egg-feeding of tadpoles, while the relatedR. variabilisconsumes the ancestral detritus diet in their nursery pools. Each species’ diet was experimentally switched, in the field and lab. Analyses of gut gene expression revealed elevated expression of proteases in theR. imitatorfield egg-fed treatment. These digestive proteins came from parabasalians, a group of protists known to form symbiotic relationships with hosts that enhance digestion. Genes that code for these digestive proteins are not present in theR. imitatorgenome, and phylogenetic analyses indicate that these mRNA sequences are from parabasalians. Bar-coding analyses of the tadpole microbiomes further confirmed this discovery. Our findings indicate the presence of parabasalian symbiotes in the intestines of theR. imitatortadpoles, that may aid the tadpoles in protein/lipid digestion in the context of an egg diet. This may have enabled the exploitation of a key ecological niche, allowingR. imitatorto expand into an area with ecologically similar species (e.g.,R. variabilisandR. summersi). In turn, this may have enabled a Müllerian mimetic radiation, one of only a few examples of this phenomenon in vertebrates.

    

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4. Transcriptomic analyses during development reveal mechanisms of integument structuring and color production

   https://doi.org/10.1007/s10682-023-10256-2  

   Stuckert, Adam M. ; Freeborn, Layla ; Howell, Kimberly A. ; Yang, Yusan ; Nielsen, Rasmus ; Richards-Zawacki, Corinne ; MacManes, Matthew D. ( September 2023 , Evolutionary Ecology)

   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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5. Perfect mimicry between Heliconius butterflies is constrained by genetics and development

   https://doi.org/10.1098/rspb.2020.1267  

   Van Belleghem, Steven M. ; Alicea Roman, Paola A. ; Carbia Gutierrez, Heriberto ; Counterman, Brian A. ; Papa, Riccardo ( July 2020 , Proceedings of the Royal Society B: Biological Sciences)

   null (Ed.)

   Müllerian mimicry strongly exemplifies the power of natural selection. However, the exact measure of such adaptive phenotypic convergence and the possible causes of its imperfection often remain unidentified. Here, we first quantify wing colour pattern differences in the forewing region of 14 co-mimetic colour pattern morphs of the butterfly species Heliconius erato and Heliconius melpomene and measure the extent to which mimicking colour pattern morphs are not perfectly identical. Next, using gene-editing CRISPR/Cas9 KO experiments of the gene WntA , which has been mapped to colour pattern diversity in these butterflies, we explore the exact areas of the wings in which WntA affects colour pattern formation differently in H. erato and H. melpomene. We find that, while the relative size of the forewing pattern is generally nearly identical between co-mimics, the CRISPR/Cas9 KO results highlight divergent boundaries in the wing that prevent the co-mimics from achieving perfect mimicry. We suggest that this mismatch may be explained by divergence in the gene regulatory network that defines wing colour patterning in both species, thus constraining morphological evolution even between closely related species. 

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