Renewed diversification following Miocene landscape turnover in a Neotropical butterfly radiation

Nicolas Chazot, Keith R. Willmott, Gerardo Lamas, André V.L. Freitas, Florence Piron-Prunier, Carlos F. Arias, James Mallet, Donna Lisa De-Silva, Marianne Elias

Research output: Contribution to journalArticlepeer-review

7 Scopus citations

Abstract

Aim: The landscape of the Neotropical region has undergone dynamic evolution throughout the Miocene, with the extensive Pebas wetland occupying western Amazonia between 23 and c. 10 Ma and the continuous uplift of the Andes mountains. The complex interaction between the Andes and Amazonia probably influenced the trajectory of Neotropical biodiversity, but evidence from time-calibrated phylogenies of groups that diversified during this period is lacking. We investigate the role of these landscape transformations in the dynamics of diversification in the Neotropical region using a 26-Myr-old endemic butterfly radiation. Location: Neotropics. Time period: Oligocene to present. Major taxa studied: Ithomiini butterflies. Methods: We generated one of the most comprehensive time-calibrated molecular phylogenies of a large clade of Neotropical insects, the butterfly tribe Ithomiini, comprising 340 species (87% of extant species) and spanning 26 Myr of diversification. We applied a large array of birth–death models and historical biogeography estimations to assess the dynamics of diversification and biotic interchanges, especially at the Amazonia–Andes interface. Results: Our results suggest that the Amazonian Pebas wetland system played a major role in the timing and geography of diversification of Ithomiini, by constraining dispersal and diversification in the Amazon basin until c. 10 Ma. During the Pebas wetland period, Ithomiini diversification mostly took place in the Andes, where terrestrial habitats were not affected. An explosion of interchanges with Amazonia and with the Northern Andes accompanied the demise of the Pebas system (11–8 Ma) and was followed by local diversification in those areas, which led to a substantial renewal of diversification. Main conclusions: Many studies on Neotropical diversity have focused only on the Andes, whereas we show that it is the waxing and waning of the Pebas mega-wetland, interacting with Andean uplift, that determined the timing and patterns of regional interchanges and diversification in Ithomiini.

Original languageEnglish
Pages (from-to)1118-1132
Number of pages15
JournalGlobal Ecology and Biogeography
Volume28
Issue number8
DOIs
StatePublished - Aug 2019
Externally publishedYes

Bibliographical note

Funding Information:
?onselho Nacional de Desenvolvimento ?ientD?fico e TecnolD?gico, Grant/ Award Number: 303834/2015-3 and 563332/2010-7; Agence Nationale de la Recherche, Grant/Award Number: ANR-14-?E02-0011-01; Fundação de Amparo à Pesquisa do Estado de São Paulo, Grant/Award Number: 2011/50225- 3 and 2012/50260-6; National Science Foundation, Grant/Award Number: DEB- 1256742

Funding Information:
This project was funded by an Action Thématique Incitative sur Programme (ATIP) (?entre National de la Recherche Scientifique [?NRS], France) grant awarded to M.E., with D.L.D.-S. as a postdoctoral researcher. N.?. was funded by a doctoral fellowship from Ecole Doctorale 227 (France) and BE?? (Biodiversity and Ecosystem services in a ?hanging ?limate). M.E. acknowledges additional funding by the Agence Nationale de la Recherche (ANR) grant SPE?REP (ANR-14-?E02-0011-01). J.M. acknowledges funding from Natural Environment Research ?ouncil (NER?) and Biotechnology and Biological Sciences Research ?ouncil (BBSR?). We thank the authorities of Peru, Ecuador and Brazil (Sistema de Autorização e Informação em Biodiversidade [SISBIO] no. 10438-1) for providing research and collection permits, in addition to many assistants and colleagues for their help in the field and with databasing museum specimens. Molecular work was performed at the GenePool (University of Edinburgh, UK), ?entro de Biologia Molecular e Engenharia Genética – Universidade de ?ampinas (?BMEG-Unicamp) (Brazil)

Funding Information:
This project was funded by an Action Th?matique Incitative sur Programme (ATIP) (Centre National de la Recherche Scientifique [CNRS], France) grant awarded to M.E., with D.L.D.-S. as a postdoctoral researcher. N.C. was funded by a doctoral fellowship from Ecole Doctorale 227 (France) and BECC (Biodiversity and Ecosystem services in a Changing Climate). M.E. acknowledges additional funding by the Agence Nationale de la Recherche (ANR) grant SPECREP (ANR-14-CE02-0011-01). J.M. acknowledges funding from Natural Environment Research Council (NERC) and Biotechnology and Biological Sciences Research Council (BBSRC). We thank the authorities of Peru, Ecuador and Brazil (Sistema de Autoriza??o e Informa??o em Biodiversidade [SISBIO] no. 10438-1) for providing research and collection permits, in addition to many assistants and colleagues for their help in the field and with databasing museum specimens. Molecular work was performed at the GenePool (University of Edinburgh, UK), Centro de Biologia Molecular e Engenharia Gen?tica ? Universidade de Campinas (CBMEG-Unicamp) (Brazil) and the Service de Syst?matique Mol?culaire UMS2700 (2AD) of the Mus?um National d'Histoire Naturelle (MNHN) (France). We are grateful to Niklas Wahlberg for providing unpublished sequences of Greta diaphanus. We thank Fabien Condamine and H?l?ne Morlon for constructive discussions about time-dependent diversification analyses. A.V.L.F. thanks CNPq (grant 303834/2015-3), Rede de Pesquisa e Conserva??o de Lepidopteros (RedeLep)-Sistema Nacional de Pesquisa em Biodiversidade (SISBIOTA-Brasil)/CNPq (563332/2010-7), National Science Foundation (DEB-1256742), FAPESP (grants 2011/50225-3, 2012/50260-6 and 2013/50297-0) and United States Agency for International Development (USAID) and the U.S. National Academy of Sciences (NAS) under the Partnerships for Enhanced Engagement in Research (PEER) program (sponsor grant award no. AID-OAA-A-11-00012) (Mapping and Conserving Butterfly Biodiversity in the Brazilian Amazon). K.R.W. thanks the National Geographic Society, the Leverhulme Trust, the Darwin Initiative, the National Science Foundation (DEB-0103746 and DEB-0639861), the Florida Museum of Natural History and the University of Florida. Finally, we thank four anonymous reviewers for their constructive comments on previous versions of the manuscript.

Funding Information:
and the Service de Systématique Moléculaire UMS2700 (2AD) of the Muséum National d’Histoire Naturelle (MNHN) (France). We are grateful to Niklas Wahlberg for providing unpublished sequences of Greta diaphanus. We thank Fabien ?ondamine and Hélène Morlon for constructive discussions about time-dependent diversification analyses. A.V.L.F. thanks ?NPq (grant 303834/2015-3), Rede de Pesquisa e ?onservação de Lepidopteros (RedeLep)-Sistema Nacional de Pesquisa em Biodiversidade (SISBIOTA-Brasil)/?NPq (563332/2010-7), National Science Foundation (DEB-1256742), FAPESP (grants 2011/50225-3, 2012/50260-6 and 2013/50297-0) and United States Agency for International Development (USAID) and the U.S. National Academy of Sciences (NAS) under the Partnerships for Enhanced Engagement in Research (PEER) program (sponsor grant award no. AID-OAA-A-11-00012) (Mapping and ?onserving Butterfly Biodiversity in the Brazilian Amazon). K.R.W. thanks the National Geographic Society, the Leverhulme Trust, the Darwin Initiative, the National Science Foundation (DEB-0103746 and DEB-0639861), the Florida Museum of Natural History and the University of Florida. Finally, we thank four anonymous reviewers for their constructive comments on previous versions of the manuscript.

Publisher Copyright:
© 2019 John Wiley & Sons Ltd

Keywords

  • Andes
  • Ithomiini
  • Neotropics
  • Pebas system
  • Western Andean Portal
  • biogeography
  • butterflies
  • diversification
  • phylogeny

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