Under pressure: evidence for selection on color-related genes in poison frogs of the genus Ranitomeya

Abstract

Aposematic organisms rely on their bright conspicuous coloration to communicate to potential predators that they are toxic and unpalatable. These aposematic phenotypes are strongly tied to survival and therefore make excellent opportunities to investigate the genetic underpinning of coloration. The genus Ranitomeya includes phenotypically diverse members of Neotropical aposematic poison frogs native to South America. Significant progress has been made in elucidating the molecular mechanisms responsible for aposematic coloration in poison frogs, which have paved the way for future studies to test hypotheses of the evolution of coloration across aposematic vertebrates. However, very little is known about whether these color related genes are under positive selection. We assembled transcriptomes from publicly available data reads sets for 9 different color morphs of poison frogs in the Ranitomeya genus that display bright conspicuous coloration (four morphs of R. imitator, two morphs of R. variabilis, two morphs of R. fantastica, one morph of R. summersi) to identify protein-coding genes responsible for color production that are under positive selection. Our results show that there are multiple genes under strong positive selection that are predicted to play roles in melanin synthesis (dct, tyrp1, irf4), iridophore development (fhl1), keratin metabolism (ovol1), pteridine synthesis (prps1, xdh), and carotenoid metabolism (adh1b, aldh2). The identification of positive selection affecting candidate color-pattern genes is consistent with the possibility that these genes mediate (in part) the molecular evolution of coloration. This may be attributed to aposematic phenotypes being directly tied to survival and reproduction in poison frogs.

Evolution and Diversification of the Aposematic Poison Frog,Oophaga pumilio,in Bocas del Toro

“…The xanthine hydrogenase (xdh), initially described as the rosy locus in Drosophila, is known to influence eye coloration 71 . It is also a gene involved in the pteridine synthesis pathway in amphibians 27 that has been shown to be under selection in dendrobatids 72 . It is also differentially expressed in different color morphs of D. auratus 70 .…”

What Makes a Mimic? Orange, Red, and Black Color Production in the Mimic Poison Frog (Ranitomeya imitator)

“… Liu et al 2014 ; Posso-Terranova and Andrés 2017 ; Stuckert et al 2019 ; Rodríguez et al 2020 ; Stuckert et al 2024 ; Twomey, et al 2020a ). In addition, several studies have identified genes related to color development under positive selection in aposematic species ( Rodríguez et al 2020 ; Linderoth et al 2023 ; Rubio et al 2024 ). Historically, evolutionary biologists have predicted that aposematism, driven by predator-imposed selective pressures, causes sympatric phenotypes among closely related species to converge on a single color pattern to promote accelerated predator learning ( Müller 1879 ; Mallet and Joron 1999 ).…”