Neotropical forest expansion during the last glacial period challenges refuge hypothesis

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 p...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 113; no. 4; pp. 1008 - 1013
Main Authors Leite, Yuri L. R., Costa, Leonora P., Loss, Ana Carolina, Rocha, Rita G., Batalha-Filho, Henrique, Bastos, Alex C., Quaresma, Valéria S., Fagundes, Valéria, Paresque, Roberta, Passamani, Marcelo, Pardini, Renata
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 26.01.2016
National Acad Sciences
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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.
AbstractList 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.
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. 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.
Author Costa, Leonora P.
Paresque, Roberta
Quaresma, Valéria S.
Passamani, Marcelo
Pardini, Renata
Leite, Yuri L. R.
Bastos, Alex C.
Batalha-Filho, Henrique
Fagundes, Valéria
Rocha, Rita G.
Loss, Ana Carolina
Author_xml – sequence: 1
  givenname: Yuri L. R.
  surname: Leite
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  organization: Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
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  givenname: Leonora P.
  surname: Costa
  fullname: Costa, Leonora P.
  organization: Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 3
  givenname: Ana Carolina
  surname: Loss
  fullname: Loss, Ana Carolina
  organization: Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 4
  givenname: Rita G.
  surname: Rocha
  fullname: Rocha, Rita G.
  organization: Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 5
  givenname: Henrique
  surname: Batalha-Filho
  fullname: Batalha-Filho, Henrique
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– sequence: 6
  givenname: Alex C.
  surname: Bastos
  fullname: Bastos, Alex C.
  organization: Departamento de Oceanografia e Ecologia, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 7
  givenname: Valéria S.
  surname: Quaresma
  fullname: Quaresma, Valéria S.
  organization: Departamento de Oceanografia e Ecologia, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 8
  givenname: Valéria
  surname: Fagundes
  fullname: Fagundes, Valéria
  organization: Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, 29075-910, Vitória, ES, Brazil
– sequence: 9
  givenname: Roberta
  surname: Paresque
  fullname: Paresque, Roberta
  organization: Departamento de Ciências da Saúde, Centro Universitário Norte do Espírito Santo, Universidade Federal do Espírito Santo, 29932-540, São Mateus, ES, Brazil
– sequence: 10
  givenname: Marcelo
  surname: Passamani
  fullname: Passamani, Marcelo
  organization: Departamento de Biologia, Universidade Federal de Lavras, 37200-000, Lavras, MG, Brazil
– sequence: 11
  givenname: Renata
  surname: Pardini
  fullname: Pardini, Renata
  organization: Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, 05508-090, São Paulo, SP, Brazil
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Issue 4
Keywords continental shelf
last glacial maximum
Atlantic Forest
Quaternary
sea level
Language English
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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.
Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved December 10, 2015 (received for review July 2, 2015)
ORCID 0000-0002-0248-8738
OpenAccessLink https://www.pnas.org/content/pnas/113/4/1008.full.pdf
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Snippet The forest refuge hypothesis (FRH) has long been a paradigm for explaining the extreme biological diversity of tropical forests. According to this hypothesis,...
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...
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SubjectTerms Biodiversity
Biodiversity hot spots
Biogeography
Biological Sciences
Climate
Climatic conditions
Continental shelves
Ecosystem
Evolution, Molecular
Forest ecosystems
Forests
Genetic structure
Glaciers
Habitats
Hypothesis testing
Mathematical models
Phylogeography
Physical Sciences
Rainforests
Speciation
Tropical forests
Title Neotropical forest expansion during the last glacial period challenges refuge hypothesis
URI https://www.jstor.org/stable/26467525
http://www.pnas.org/content/113/4/1008.abstract
https://www.ncbi.nlm.nih.gov/pubmed/26755597
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https://www.proquest.com/docview/1761078347
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https://pubmed.ncbi.nlm.nih.gov/PMC4743791
Volume 113
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