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Selection-driven color variation in the aposematic strawberry poison frog, Oophaga pumilio

Abstract

The strawberry poison frog, Oophaga pumilio, is a striking example of natural color variation, making it a valuable system for studying the genetic and evolutionary mechanisms underlying phenotypic diversity. While most populations of this poisonous frog are bright red, frogs from Bocas del Toro Province, Panama, exhibit remarkable variation in color, both within and among island populations. This diversity in warning coloration challenges conventional models of aposematism and has fueled extensive debate about its evolutionary and genetic origins. A major obstacle to understanding this phenomenon has been the species' large genome (∼6.7 Gb). To address this, we sequenced exomes from 347 individuals across ten populations and identified genetic factors associated with color variation. Our analyses identified kit as a major candidate gene linked to blue-red polymorphism, where an increase in the proportion and organization of melanosomes with respect to other pigments contributes to blue coloration. Variation in ttc39b, a gene involved in conversion from yellow to red carotenoids, is strongly associated with the yellow-red polymorphism. We also identify bco1, a carotenoid-cleaving gene, which shows strong evidence of population differentiation and higher expression in green frogs. The haplotypes at all three loci predate population divergence and exhibit signatures of selective sweeps, indicating that selection has repeatedly acted on standing genetic variation in different populations. Our findings support a dynamic evolutionary model in which new morphs emerge through a balance of selective pressures, including predation, intraspecific competition, and mate choice.

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