Transcriptomic signatures of carotenoid-based color polytypism in Oophaga granulifera (Anura: Dendrobatidae).

Abstract

Aposematic phenotypes advertise their unprofitability to predators by means of colorful warning signals. The Neotropical family Dendrobatidae comprises some of the prime examples of aposematism in amphibians but with pronounced intraspecific variation in some species, particularly in the genus Oophaga. We herein compare the skin spectral reflectance, pigment composition and gene expression of individuals with aposematic (red) and cryptic (green) phenotypes of Oophaga granulifera from Costa Rica. Our findings reveal that accumulation of keto-carotenoids, xanthophylls, and β-carotene in the skin are responsible for the red aposematic phenotype in this species. Several differentially expressed pigmentation genes, particularly some in the carotenoid metabolism pathway, are strongly associated with the distinction between red and green skin phenotypes. Green frogs also show pronounced up-regulation of the bco1 gene which has been associated to ketocarotenoid-based polymorphisms in other species and represents a strong candidate for additional enzymatic studies. We found no clear candidate ketolase gene but the ketolation enhancer ttc39b was upregulated in the liver of red O. granulifera, aligning with previous studies that underscore the importance of this ancillary gene for keto-carotenoid metabolism. Gene ontology enrichments indicate that, along with the carotenoid metabolism genes, red frogs upregulate the metabolism of amino acids, lipids and the mitochondrial energy production, markedly in the liver but also in the skin. These results suggest a close association between increased keto-carotenoid accumulation and a higher metabolic rate in the red frogs which is congruent with macroevolutionary patterns in the family and behavioral observations in this species.