The evolution of polymorphism in the warning coloration of the Amazonian poison frog Adelphobates galactonotus

Abstract

While intraspecific variation in aposematic signals can be selected for by different predatory responses, their evolution is also contingent on other processes shaping genetic variation. We evaluate the relative contributions of selection, geographic isolation, and random genetic drift to the evolution of aposematic color polymorphism in the poison frog Adelphobates galactonotus, distributed throughout eastern Brazilian Amazonia. Dorsal coloration was measured for 111 individuals and genetic data were obtained from 220 individuals at two mitochondrial genes (mtDNA) and 7963 Single Nucleotide Polymorphisms (SNPs). Four color categories were described (brown, blue, yellow, orange) and our models of frog and bird visual systems indicated that each color was distinguishable for these taxa. Using outlier and correlative analyses we found no compelling genetic evidence for color being under divergent selection. A time-calibrated mtDNA tree suggests that the present distribution of dorsal coloration resulted from processes occurring during the Pleistocene. Separate phylogenies based on SNPs and mtDNA resolved the same well supported clades, each containing different colored populations. Ancestral character state analysis provided some evidence for evolutionary transitions in color type. Genetic structure was more strongly associated with geographic features, than color category, suggesting that the distribution of color is explained by localized processes. Evidence for geographic isolation together with estimates of low effective population size implicates drift as playing a key role in color diversification. Our results highlight the relevance of considering the neutral processes involved with the evolution of traits with important fitness consequences.

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Acknowledgements

We thank the Editor and two anonymous reviewers for insightful comments that greatly improved this manuscript. Estação Científica Ferreira Penna and ICMBio provided valuable support and facilities at ICMBio Caxiuanã Station. R.M. Brabo, P.M. Brabo, M.R. da Silva, J.M.P. dos Santos, J.L.F. da Costa, E.P de Souza, J.N.B. Carneiro, A.P. Farias, M.F.M. Pedroso, J.A. da Costa Filho, G. O. da Silva, C.A. Lopes for field assistance. Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) provided collection permits (# 36135-1). Financial support was provided by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (Project 472198/2011-4) and Programa Ciência sem Fronteiras (Project 401327/2012-4). Support was also provided by a PVE fellowship to AS (312315/2012-0), SWE fellowship to DR (200292/2014-5), a PDJ fellowship for PIS (151409/2013-7), PhD fellowship from CNPq (141886/2012-9) to DR, and a BEV fellowship from CNPq (170211/2012-6) to AA, a research fellowship (312674/2013-9) to TCSAP. PM receives an Academy of Finland postdoctoral fellowship (grant # 316294).

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DR, AS, and APL designed the project. DR, APL, AS, and PIS collected samples. TCSA-P and MSH contribued useful discussion. TCSA-P, MSH and YOCB contributed samples and useful discussion. DR and AA measured, analyzed and interpreted the color data. AS, PIS, ILK, PM and RD analyzed and interpreted genetic data. DR and AS wrote the manuscript with contributions from all co-authors.

Correspondence to Adam Stow.

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Rojas, D., Lima, A.P., Momigliano, P. et al. The evolution of polymorphism in the warning coloration of the Amazonian poison frog Adelphobates galactonotus. Heredity (2019). https://doi.org/10.1038/s41437-019-0281-4

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