Differential gene expression and gene variants drive color and pattern development in divergent color morphs of a mimetic poison frog

Abstract

Evolutionary biologists have long investigated the ecological contexts, evolutionary forces, and proximate mechanisms that produce the diversity of animal coloration we see in the natural world. In aposematic species, color and pattern is directly tied to survival and thus understanding the origin of the phenotype has been a focus of both theoretical and empirical inquiry. In order to better understand this diversity, we examined gene expression in skin tissue during development in four different color morphs of the aposematic mimic poison frog, Ranitomeya imitator. We identified a suite of candidate color-related genes a priori and identified the pattern of expression in these genes over time, differences in expression of these genes between the mimetic morphs, and genetic variants that differ between color morphs. We identified several candidate color genes that are differentially expressed over time or across populations, as well as a number of color genes with fixed genetic variants between color morphs. Many of the color genes we discovered in our dataset are involved in the canonical Wnt signaling pathway, including several fixed SNPs between color morphs. Further, many genes in this pathway were differentially expressed at different points in development (e.g., lef1, tyr, tyrp1). Importantly, Wnt signaling pathway genes are overrepresented relative to expression in Xenopus tropicalis. Taken together, this provides evidence that the Wnt signaling pathway is contributing to color pattern production in R. imitator, and is an excellent candidate for producing some of the differences in color pattern between morphs. In addition, we found evidence that sepiapterin reductase is likely important in the production of yellow-green coloration in this adaptive radiation. Finally, two iridophore genes (arfap1, gart) draw a strong parallel to previous work in another dendrobatid, indicating that these genes are also strong candidates for differential color production. We have used high throughput sequencing throughout development to examine the evolution of coloration in a rapid mimetic adaptive radiation and found that these divergent color patterns are likely to be affected by a combination of developmental patterns of gene expression, color morph-specific gene expression, and color morph-specific gene variants.