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Genetic divergence in tropical anurans: deeper phylogeographic structure in forest specialists and in topographically complex regions

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Abstract

Many tropical organisms show large genetic differences among populations, yet the prevalent drivers of the underlying divergence processes are incompletely understood. We explored the effect of several habitat and natural history features (body size, macrohabitat, microhabitat, reproduction site, climatic heterogeneity, and topography) on population genetic divergence in tropical amphibians, based on a data set of 2680 DNA sequences of the mitochondrial cytochrome b gene in 39 widely distributed frog species from Brazil, Central America, Cuba, and Madagascar. Generalized linear models were implemented in an information-theoretic framework to evaluate the effects of the six predictors on genetic divergence among populations, measured as spatially corrected pairwise distances. Results indicate that topographic complexity and macrohabitat preferences have a strong effect on population divergence with species specialized to forest habitat and/or from topographically complex regions showing higher phylogeographic structure. This relationship changed after accounting for phylogenetic relatedness among taxa rendering macrohabitat preferences as the most important feature shaping genetic divergence. The remaining predictors showed negligible effects on the observed genetic divergence. A similar analysis performed using the population-scaled mutation rate (Θ) as response variable showed little effect of the predictors. Our results demonstrate greater evolutionary independence among populations of anurans from forested regions versus species from open habitats. This pattern may result from lower vagility and stringency in reproductive requirements of rainforest species. Conversely, open landscapes may offer ephemeral and unstable breeding sites suitable for vagile generalist species, resulting in reduced intraspecific divergence. Our results predict that, for a given period of time, there should be a higher chance of speciation in tropical anurans living in forests than in species adapted to open habitats.

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Acknowledgments

We are grateful to numerous friends and colleagues who have contributed samples and sequences for the present project, or provided assistance during fieldwork. In particular we would like to thank (in alphabetic order) Roberto Alonso, Franco Andreone, Adrian Garda, Sebastian Gehring, Frank Glaw, Jörn Köhler, Roger-Daniel Randrianiaina, Fanomezana Ratsoavina, Leslie Rissler, Axel Strauß, Chris Thawley, and David R. Vieites. Thanks are also due to Meike Kondermann and Gabi Keunecke for help with labwork. We are grateful to authorities in Brazil, Cuba and Madagascar for research, collection, and export permits. This study was carried with funds of the Deutsche Forschungsgemeinschaft (Grant VE247/7-1 to MV). AR and MP were supported by postdoctoral fellowships of the Humboldt Foundation. MG was supported by the Katholischer Akademischer Austauschdienst. CFBH was supported by Grants #2008/50928-1 and #2013/50741-7, São Paulo Research Foundation (FAPESP), and Grant #302518/2013-4, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Authors and Affiliations

  1. Division of Evolutionary Biology, Zoological Institute, Technical University of Braunschweig, Mendelssohnstr. 4, 38106, Braunschweig, Germany

    Ariel Rodríguez, Miriam Börner & Miguel Vences

  2. Department of Comparative Anatomy, Institute of Zoology, Jagiellonian University, ul. Gronostajowa 9, 30-387, Kraków, Poland

    Maciej Pabijan

  3. Institute of Environmental Sciences, Jagiellonian University, ul. Gronostajowa 7, 30-387, Kraków, Poland

    Maciej Pabijan

  4. DBEZ—Centro de Biociências, Universidade Federal do Rio Grande do Norte, Campus Universitário Lagoa Nova, Natal, RN, 59078-900, Brazil

    Marcelo Gehara

  5. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista “Júlio de Mesquita Filho”, Rio Claro, SP, 13506-900, Brazil

    Célio F. B. Haddad

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  1. Ariel Rodríguez
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  2. Miriam Börner
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  4. Marcelo Gehara
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  6. Miguel Vences
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Correspondence to Miguel Vences.

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Rodríguez, A., Börner, M., Pabijan, M. et al. Genetic divergence in tropical anurans: deeper phylogeographic structure in forest specialists and in topographically complex regions. Evol Ecol 29, 765–785 (2015). https://doi.org/10.1007/s10682-015-9774-7

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