Genetic basis of aposematic coloration in a mimetic radiation of poison frogs

Abstract

The evolution of mimicry in a single species or population has rippling inter and intraspecific effects across ecological communities, providing a fascinating mechanism of phenotypic diversification. In this study we present the first identification of genes underlying Müllerian mimicry in a vertebrate, the Peruvian mimic poison frog,Ranitomeya imitator. We sequenced 124R. imitatorexomes and discovered loci with both strong divergence between different mimetic morphs and phenotypic associations within an intraspecific admixture zone, implicatingmc1r,asip,bsn,retsat, andkrt8.2in the evolution of mimetic color phenotypes. We confirmed these associations for most candidate genes through linkage mapping in a lab-reared pedigree. We also sequenced transcriptomes from the model species, allowing tests for introgression and revealing that the mimetic resemblance betweenR. imitatorand the models evolved independently. Selection analyses of the candidate genes show that the mimicry phenotypes likely have evolved through selective sweeps acting on polygenic variation. Our results suggest that the evolutionary origins and molecular mechanisms underlying mimicry phenotypes in vertebrates may be radically different from those previously documented in invertebrates such as the iconicHeliconiusbutterfly mimicry complex.One Sentence SummaryMüllerian mimicry evolved through independent selective sweeps on color and pattern loci in the mimic poison frog.

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 ).…”

“…To date, there are four known R. imitator color morphs that occur in sympatry with three congeneric model species ( Symula et al 2001 ; Stuckert et al 2014 ). Significant progress has been made in identifying the genes underlying color production in poison frogs ( Stuckert et al 2019 ; Twomey, et al 2020a ; Rodríguez et al 2020 ; Linderoth et al 2023 ). Of particular relevance is a recent study by Stuckert et al (2024) which examined gene expression of whole-skin samples from R. imitator , Ranitomeya fantastica , and Ranitomeya variabilis.…”