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Ancient divergence and recent population expansion in a leaf frog endemic to the southern Brazilian Atlantic forest

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Abstract

The evolutionary history of Neotropical organisms has been often interpreted through broad-scale generalizations. The most accepted model of diversification for the Brazilian Atlantic forest (BAF) rely on putative historical stability of northern areas and massive past habitat replacement of its southern range. Here, we use the leaf frog Phyllomedusa distincta, endemic to the southern BAF, to better understand diversification patterns within this underexplored rainforest region. We used an integrative approach coupling fine-scale sampling and multilocus sequence data, with traditional and statistical phylogeographic (multilocus approximate Bayesian computation) methods to explore alternative hypotheses of diversification. We also employed species paleodistribution modeling to independently verify habitat stability upon a spatially explicit model. Our data support two divergent lineages with coherent geographic distribution that span throughout northern and southern ranges. Demographic estimates suggested the Southern lineage has experienced a recent population expansion, whereas the Northern lineage remained more stable. Hypothesis testing supports a scenario of ancient vicariance with recent population expansion. The paleodistribution model revealed habitat discontinuity during the Last Glacial Maximum (LGM) with one area of putative stability within the range of the Northern lineage. Evidence on genetic structure, demography, and paleodistribution of P. distincta support a historically heterogeneous landscape for the southern BAF, with both areas of forest stability and regions where forest occupation is probably recent. We also associate the southern end of the Cubatão shear zone with a phylogeographic break in the BAF. Taken together, our results argue for the idea of multiple mechanisms generating diversity in this biome and underscore the need of fine-scale data in revealing more detailed pictures.

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Acknowledgments

This work was supported by São Paulo Research Foundation (FAPESP)—grants #2005/52727-5 and #2006/56938-3 to JA, #2008/50928-1 and #2013/50741-7 to CFBH, and fellowship grant #2011/51392-0 to MTCT; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—grant #300612/2008-7 to CFBH; and Fundação para a Ciência e a Tecnologia (FCT)—project #PTDC/BIA-BEC/105093/2008 (funded by Fundo Europeu de Desenvolvimento Regional through the Programa Operacional Factores de Competitividade program and Portuguese national funds) to FS, and fellowship grants #SFRH/BD/61689/2009 to TOB and #SFRH/BPD/87721/2012 to FS (under the Programa Operacional Potencial Humano-Quadro de Referência Estratégico Nacional funds from the European Social Fund and Portuguese Ministério da Educação e Ciência). We are further grateful to Elaine M. Lucas (Unochapecó/Brazil), Miguel Trefault Rodrigues (USP/Brazil), and Selvino Neckel de Oliveira (UFSC/Brazil) for tissue donations; all members of UNESP/RC Herpetology Lab from 2009 to 2013, in particular, João Paulo de Cortes, for sample collections; José Carlos Brito for assisting in species distribution modeling analysis; and Andrew J. Crawford and an anonymous reviewer for their helpful comments and suggestions.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

The research was conducted in accordance with Brazilian legislation governing standards of ethical procedures for collecting and scientific studies, and under consent and approval of Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio - permission 25906-1 and 2).

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Authors and Affiliations

  1. CIBIO-InBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, Laboratório Associado, Universidade do Porto, Campus Agrário de Vairão, 4485-661, Vairão, Portugal

    Tuliana O. Brunes & Fernando Sequeira

  2. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto (UP), 4169-007, Porto, Portugal

    Tuliana O. Brunes

  3. Departamento de Zoologia, Instituto de Biociências, Universidade Estadual Paulista (UNESP), 13506-900, Rio Claro, São Paulo, Brazil

    Maria Tereza C. Thomé & Célio F. B. Haddad

  4. Departamento de Ciências Biológicas, Universidade Federal de São Paulo (UNIFESP), 09972-270, Diadema, Brazil

    João Alexandrino

Authors
  1. Tuliana O. Brunes
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  2. Maria Tereza C. Thomé
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  3. João Alexandrino
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  4. Célio F. B. Haddad
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  5. Fernando Sequeira
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Corresponding author

Correspondence to Tuliana O. Brunes.

Electronic supplementary material

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Online Resource 1

Supplementary materials and methods. (PDF 188 kb)

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Supplementary results. (PDF 717 kb)

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Brunes, T.O., Thomé, M.T.C., Alexandrino, J. et al. Ancient divergence and recent population expansion in a leaf frog endemic to the southern Brazilian Atlantic forest. Org Divers Evol 15, 695–710 (2015). https://doi.org/10.1007/s13127-015-0228-4

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  • DOI: https://doi.org/10.1007/s13127-015-0228-4

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