Genetic Bases Of Aposematic Traits: Insights from the Skin Transcriptional Profiles of Oophaga Poison Frogs

Abstract

18Aposematic organisms advertise their defensive toxins to predators using a variety 19 of warning signals, including bright coloration. While most Neotropical poison frogs 20 (Dendrobatidae) rely on crypsis to avoid predators, Oophaga poison frogs from South 21 America advertise their chemical defenses, a complex mix of diet-derived alkaloids, by 22 using conspicuous hues. The present study aimed to characterize the skin transcriptomic 23 profiles of the South American clade of Oophaga poison frogs (O. anchicayensis, O. 24 solanensis, O. lehmanni and O. sylvatica). Our analyses showed very similar 25 transcriptomic profiles for these closely related species in terms of functional annotation 26 and relative abundance of gene ontology terms expressed. Analyses of expression profiles 27 of Oophaga and available skin transcriptomes of cryptic anurans allowed us to propose 28 possible mechanisms for the active sequestration of alkaloid-based chemical defenses and 29to highlight some genes that may be potentially involved in resistance mechanisms to 30 avoid self-intoxication and skin coloration. In doing so, we provide an important 31 molecular resource for the study of warning signals that will facilitate the assembly and 32 annotation of future poison frog genomes. 33 34 KEYWORDS 35Dendrobatids, RNA sequencing, transcriptomes, gene ontology, candidate 36 genes. 37 coloration, and the resistance mechanisms to avoid self-intoxication. 54The frogs of this complex inhabit the lowland Pacific rainforests of the 55 Colombian and Ecuadorian Chocó. Preliminary molecular data from nuclear and 56 mitochondrial markers showed a similar genetic background among lineages in contrast 57to an extraordinary diversity of morphotypes [7]. Individuals from different allopatric 58 lineages can be relatively homogeneous, striped, or spotted, and their colors range from 59 bright red, to orange and yellow (Fig 1) [8]. These polymorphic coloration patterns serve 60 as a warning signal of their chemical defenses [9], a complex mix of diet-derived 61 alkaloids secreted by the dermal glands [10, 11]. Although these chemicals may involve 62 metabolism and transport through other tissues, the final accumulation of toxins as well 63 as the production of pigmentary cells is performed in the skin tissue of these organisms 64 even during the adult stage [12][13][14]. Thus, we expected that the genes, pathways, and/ or 65 gene networks potentially associated with coloration, alkaloid metabolism, transport and 66 storage, to be expressed in the skin of these lineages. 67Although the lineages of the Oophaga studied here display a wide variety of 68 warning signals, most of them share a black background coloration (Fig 1). In adult frogs, 69 this melanistic coloration is controlled by the lack of iridophores and xanthophores in the 70 dermal chromatophore unit, as well as the size and dispersion pattern of the melanin-71 containing organelles (melanosomes) within the dermal melanophores [15]. Thus, we 72 also hypothesized that in adult individuals...