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Colloquium Paper

Inferring responses to climate dynamics from historical demography in neotropical forest lizards

View ORCID ProfileIvan Prates, Alexander T. Xue, Jason L. Brown, Diego F. Alvarado-Serrano, Miguel T. Rodrigues, Michael J. Hickerson, and Ana C. Carnaval
  1. aDepartment of Biology, City College of New York, New York, NY 10031;
  2. bDepartment of Biology, Graduate Center, City University of New York, New York, NY 10016;
  3. cCooperative Wildlife Research Laboratory, Department of Zoology, Southern Illinois University, Carbondale, IL 62901;
  4. dDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109;
  5. eDepartamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP 05508-090, Brazil;
  6. fDivision of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024

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PNAS July 19, 2016 113 (29) 7978-7985; first published July 18, 2016; https://doi.org/10.1073/pnas.1601063113
Ivan Prates
aDepartment of Biology, City College of New York, New York, NY 10031;
bDepartment of Biology, Graduate Center, City University of New York, New York, NY 10016;
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  • ORCID record for Ivan Prates
  • For correspondence: ivanprates@gmail.com
Alexander T. Xue
aDepartment of Biology, City College of New York, New York, NY 10031;
bDepartment of Biology, Graduate Center, City University of New York, New York, NY 10016;
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Jason L. Brown
aDepartment of Biology, City College of New York, New York, NY 10031;
cCooperative Wildlife Research Laboratory, Department of Zoology, Southern Illinois University, Carbondale, IL 62901;
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Diego F. Alvarado-Serrano
aDepartment of Biology, City College of New York, New York, NY 10031;
dDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109;
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Miguel T. Rodrigues
eDepartamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP 05508-090, Brazil;
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Michael J. Hickerson
aDepartment of Biology, City College of New York, New York, NY 10031;
bDepartment of Biology, Graduate Center, City University of New York, New York, NY 10016;
fDivision of Invertebrate Zoology, American Museum of Natural History, New York, NY 10024
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Ana C. Carnaval
aDepartment of Biology, City College of New York, New York, NY 10031;
bDepartment of Biology, Graduate Center, City University of New York, New York, NY 10016;
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  1. Edited by John C. Avise, University of California, Irvine, CA, and approved April 25, 2016 (received for review February 12, 2016)

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Abstract

We apply a comparative framework to test for concerted demographic changes in response to climate shifts in the neotropical lowland forests, learning from the past to inform projections of the future. Using reduced genomic (SNP) data from three lizard species codistributed in Amazonia and the Atlantic Forest (Anolis punctatus, Anolis ortonii, and Polychrus marmoratus), we first reconstruct former population history and test for assemblage-level responses to cycles of moisture transport recently implicated in changes of forest distribution during the Late Quaternary. We find support for population shifts within the time frame of inferred precipitation fluctuations (the last 250,000 y) but detect idiosyncratic responses across species and uniformity of within-species responses across forest regions. These results are incongruent with expectations of concerted population expansion in response to increased rainfall and fail to detect out-of-phase demographic syndromes (expansions vs. contractions) across forest regions. Using reduced genomic data to infer species-specific demographical parameters, we then model the plausible spatial distribution of genetic diversity in the Atlantic Forest into future climates (2080) under a medium carbon emission trajectory. The models forecast very distinct trajectories for the lizard species, reflecting unique estimated population densities and dispersal abilities. Ecological and demographic constraints seemingly lead to distinct and asynchronous responses to climatic regimes in the tropics, even among similarly distributed taxa. Incorporating such constraints is key to improve modeling of the distribution of biodiversity in the past and future.

  • phylogeography
  • population genomics
  • Amazon Forest
  • Atlantic Forest
  • climate change

Footnotes

  • ↵1To whom correspondence should be addressed. Email: ivanprates{at}gmail.com.
  • Author contributions: I.P., A.T.X., J.L.B., and D.F.A.-S., M.T.R., M.J.H., and A.C.C. designed research; I.P., A.T.X., J.L.B., and D.F.A.-S. performed research; A.T.X., J.L.B., D.F.A.-S., M.T.R., and A.C.C. contributed new reagents/analytic tools; I.P., A.T.X., J.L.B., D.F.A.-S., M.T.R., M.J.H., and A.C.C. analyzed data; and I.P., A.T.X., J.L.B., D.F.A.-S., M.T.R., M.J.H., and A.C.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution X: Comparative Phylogeography,” held January 8–9, 2016, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and video recordings of most presentations are available on the NAS website at www.nasonline.org/ILE_X_Comparative_Phylogeography.

  • This article is a PNAS Direct Submission.

  • Data deposition: The sequence(s) reported in this paper have been deposited in the Dryad Digital Repository database, datadryad.org/ (doi: 10.5061/dryad.2v1p6).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1601063113/-/DCSupplemental.

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Forest lizard phylogeography and climate change
Ivan Prates, Alexander T. Xue, Jason L. Brown, Diego F. Alvarado-Serrano, Miguel T. Rodrigues, Michael J. Hickerson, Ana C. Carnaval
Proceedings of the National Academy of Sciences Jul 2016, 113 (29) 7978-7985; DOI: 10.1073/pnas.1601063113

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Forest lizard phylogeography and climate change
Ivan Prates, Alexander T. Xue, Jason L. Brown, Diego F. Alvarado-Serrano, Miguel T. Rodrigues, Michael J. Hickerson, Ana C. Carnaval
Proceedings of the National Academy of Sciences Jul 2016, 113 (29) 7978-7985; DOI: 10.1073/pnas.1601063113
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Proceedings of the National Academy of Sciences: 113 (29)
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