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Research Article

Neotropical forest expansion during the last glacial period challenges refuge hypothesis

View ORCID ProfileYuri L. R. Leite, Leonora P. Costa, Ana Carolina Loss, Rita G. Rocha, Henrique Batalha-Filho, Alex C. Bastos, Valéria S. Quaresma, Valéria Fagundes, Roberta Paresque, Marcelo Passamani, and Renata Pardini
PNAS January 26, 2016 113 (4) 1008-1013; first published January 11, 2016; https://doi.org/10.1073/pnas.1513062113
Yuri L. R. Leite
aDepartamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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  • ORCID record for Yuri L. R. Leite
  • For correspondence: yuri_leite@yahoo.com
Leonora P. Costa
aDepartamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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Ana Carolina Loss
aDepartamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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Rita G. Rocha
aDepartamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
bDepartamento de Biologia, Centro de Estudos do Ambiente e do Mar, Campus Universitário de Santiago, Universidade de Aveiro, 3810-193, Aveiro, Portugal;
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Henrique Batalha-Filho
cDepartamento de Zoologia, Instituto de Biologia, Universidade Federal da Bahia, 40170-115, Salvador, BA, Brazil;
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Alex C. Bastos
dDepartamento de Oceanografia e Ecologia, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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Valéria S. Quaresma
dDepartamento de Oceanografia e Ecologia, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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Valéria Fagundes
aDepartamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil;
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Roberta Paresque
eDepartamento de Ciências da Saúde, Centro Universitário Norte do Espírito Santo, Universidade Federal do Espírito Santo, 29932-540, São Mateus, ES, Brazil;
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Marcelo Passamani
fDepartamento de Biologia, Universidade Federal de Lavras, 37200-000, Lavras, MG, Brazil;
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Renata Pardini
gDepartamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil
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  1. Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved December 10, 2015 (received for review July 2, 2015)

This article has a Letter. Please see:

  • The “Atlantis Forest hypothesis” does not explain Atlantic Forest phylogeography - March 16, 2016

See related content:

  • New dimension to Atlantic Forest biogeography
    - Mar 16, 2016
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Significance

The tropical forests of South America are among the most diverse and unique habitats in the world in terms of plant and animal species. One of the most popular explanations for this diversity and endemism is the idea that forests retracted and fragmented during glacial periods, forming ecological refuges, surrounded by dry lands or savannas. These historically stable forest refuges would have been responsible for maintaining the pattern of diversity and endemism observed today. Here, we show that the Atlantic Forest of eastern South America probably expanded, rather than contracted, during the last glacial period. In addition, the emerged Brazilian continental shelf played a major, yet neglected, role on the evolution of this biodiversity hotspot during the last glacial period.

Abstract

The forest refuge hypothesis (FRH) has long been a paradigm for explaining the extreme biological diversity of tropical forests. According to this hypothesis, forest retraction and fragmentation during glacial periods would have promoted reproductive isolation and consequently speciation in forest patches (ecological refuges) surrounded by open habitats. The recent use of paleoclimatic models of species and habitat distributions revitalized the FRH, not by considering refuges as the main drivers of allopatric speciation, but instead by suggesting that high contemporary diversity is associated with historically stable forest areas. However, the role of the emerged continental shelf on the Atlantic Forest biodiversity hotspot of eastern South America during glacial periods has been ignored in the literature. Here, we combined results of species distribution models with coalescent simulations based on DNA sequences to explore the congruence between scenarios of forest dynamics through time and the genetic structure of mammal species cooccurring in the central region of the Atlantic Forest. Contrary to the FRH predictions, we found more fragmentation of suitable habitats during the last interglacial (LIG) and the present than in the last glacial maximum (LGM), probably due to topography. We also detected expansion of suitable climatic conditions onto the emerged continental shelf during the LGM, which would have allowed forests and forest-adapted species to expand. The interplay of sea level and land distribution must have been crucial in the biogeographic history of the Atlantic Forest, and forest refuges played only a minor role, if any, in this biodiversity hotspot during glacial periods.

  • last glacial maximum
  • sea level
  • Atlantic Forest
  • Quaternary
  • continental shelf

Footnotes

  • ↵1To whom correspondence should be addressed. Email: yuri_leite{at}yahoo.com.
  • Author contributions: Y.L.R.L., L.P.C., and R. Pardini designed research; Y.L.R.L., L.P.C., A.C.L., R.G.R., and R. Pardini performed research; Y.L.R.L., L.P.C., A.C.L., R.G.R., H.B.-F., V.F., R. Paresque, M.P., and R. Pardini contributed new reagents/analytic tools; A.C.L., R.G.R., and H.B.-F. analyzed data; and Y.L.R.L., L.P.C., A.C.L., R.G.R., H.B.-F., A.C.B., V.S.Q., and R. Pardini wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequences reported in this paper have been deposited in the GenBank database. For a list of accession numbers, see Dataset S2.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1513062113/-/DCSupplemental.

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Forest expansion during the last glacial period
Yuri L. R. Leite, Leonora P. Costa, Ana Carolina Loss, Rita G. Rocha, Henrique Batalha-Filho, Alex C. Bastos, Valéria S. Quaresma, Valéria Fagundes, Roberta Paresque, Marcelo Passamani, Renata Pardini
Proceedings of the National Academy of Sciences Jan 2016, 113 (4) 1008-1013; DOI: 10.1073/pnas.1513062113

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Forest expansion during the last glacial period
Yuri L. R. Leite, Leonora P. Costa, Ana Carolina Loss, Rita G. Rocha, Henrique Batalha-Filho, Alex C. Bastos, Valéria S. Quaresma, Valéria Fagundes, Roberta Paresque, Marcelo Passamani, Renata Pardini
Proceedings of the National Academy of Sciences Jan 2016, 113 (4) 1008-1013; DOI: 10.1073/pnas.1513062113
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