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Research Article

Diversification of the Pristimantis conspicillatus group (Anura: Craugastoridae) within distinct neotropical areas throughout the Neogene

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Abstract

Determining the relative importance of dispersal and vicariance events across neotropical regions is a major goal in biogeography. These events are thought to be related to important landscape changes, notably the transition of Amazonia toward its modern hydrological configuration ca. 10 million years ago. We investigated the spatio-temporal context of the diversification of one of the major lineages of Pristimantis, a widespread and large genus of direct-developing Neotropical frogs. We gathered a spatially and taxonomically extensive sampling of mitochondrial DNA sequences from 754 Pristimantis gr. conspicillatus specimens, which led to delimiting 75 Operational Taxonomic Units (OTUs). Complete mitogenomes of 35 of these OTUs were assembled and collated with two nuDNA loci to reconstruct a time-calibrated phylogeny. We identified five major clades that diverged around the Oligocene-Miocene transition and that are largely restricted to distinct Neotropical regions i.e. Western Amazonia (P. conspicillatus clade), the Brazilian Shield (P. fenestratus clade), the Atlantic Forest (P. ramagii clade), the Guiana Shield (P. vilarsi clade) and the northern Andes (P. nicefori clade). The majority of the diversification events within these clades occurred in-situ from the early Miocene onward. Yet, a few ancient dispersal/vicariance events are inferred to have occurred among trans-Andean forests, the Atlantic Forest, the Brazilian and the Guiana Shields, but almost none in the last 10 Ma. The radical landscape transformations during the Miocene caused by the Andean orogeny and hydrological barriers such as the Pebas System and the subsequent transcontinental configuration of the Amazon drainage is a likely explanation for the isolation of the different clades within the P. gr. conspicillatus.

Acknowledgements

This study benefited from an “Investissement d’Avenir” grant managed by the Agence Nationale de la Recherche (CEBA, ref. ANR-10-LABX-25-01; TULIP, ref. ANR-10-LABX-0041; ANAEE-France: ANR-11-INBS-0001). AF and FPW acknowledge the French/Brazilian GUYAMAZON program action (IRD, CNRS, CTG, CIRAD and Brazilian Fundação de Amparo à Pesquisa do Estado do Amazonas-FAPEAM 062.00962/2018). MTR thanks Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo à Pesquisa do Estado de São Paulo [FAPESP grant numbers: 2003/10335-8, 2011/50146-6, and NSF-FAPESP Dimensions of Biodiversity Program [grant numbers: BIOTA 2013/50297-0, NSF-DEB 1343578] and NASA. SRR acknowledges a grant from SENESCYT (Arca de Noé Initiative). AFJ received PhD scholarships from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–Brasil (CAPES # 001) and Programa i-COOP (# COOPA20188) from Consejo Superior de Investigaciones Científicas (CSIC), Spain. FPW thanks CNPq (Productivity Fellowship), FAPEAM, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES (Visiting Professor Fellowship), and the L’Oréal-UNESCO For Women In Science Program. TH thanks CNPq (Productivity Fellowship) and CNPq/SISBIOTA [563348/2010-0]. Financial support was received through a research grant from the National Council for Scientific and Technological Development (CNPq #446935/2014-0). We warmly thank P-O Antoine, J. Cornuault, F. Condamine, A. Iribar-Pelozuelo, S. Manzi, J. Murienne, and U. Suescun for their help in the lab or for insights on the manuscript. J. Allen, S. Castroviejo-Fisher, J. Chretien, M. Chouteau, A. J. Crawford, F. Dal Vechio, J. M. Guellere, S. Marques-Souza, M. Dewynter, G. Gagliardi, B. P. Noonan, J. M. Padial, I. Prates, V. Premel, R. Recoder, M.A. Sena, M. Teixeira Jr., the staff from the Amphibians and Reptiles Collection and the Genetics Resources Collection at INPA, and Arcadis-Logos, kindly provided material or field assistance. PUCE museum shared samples under their care, Centro URKU and SERFOR granted sampling permits in Peru. Research in Colombia was conducted under expedient No. RCI0005-00-2018 issued by Autoridad Nacional de Licencias Ambientales (ANLA).

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplemental material

Supplemental material for this article can be accessed here: https://doi.org/10.1080/14772000.2022.2130464.

Associate Editors: Dr Christoph Bleidorn & Dr Peter D. Olson

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