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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 Fundacao de Amparo a Pesquisa do Estado do Amazonas-FAPEAM 062.00962/2018). MTR thanks Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP; #2003/10335-8, 2011/50146-6), and NSF-FAPESP Dimensions of Biodiversity Program [# BIOTA 2013/50297-0, NSF -DEB 1343578] and NASA. SRR acknowledges a grant from SENESCYT (Arca de Noe Initiative). FPW thanks CNPq (Productivity Fellowship and Research Grants), FAPEAM (Biodiversa, Amazonia + 10 Programs), Serrapilheira Institute and the L'Oreal-UNESCO For Women In Science Program. APL thanks FAPEAM (Productivity Fellowship: CT & I Edital #013/2022). TH thanks CNPq (Productivity Fellowship) and CNPq/SISBIOTA [563348/2010-0]. RWA thanks CNPq (Productivity Fellowship: 307722/2021-0) and FUNCAP [FC3-00198- 00006.01.00/22]. IJR thanks Programa de Desenvolvimento Cient & imath;fico e Tecnologico Regional - PDCTR (CNPq/Funcap) Edital 03/2021, DCT-0182- 00049.01.00/21 and 04863348/2022 for a fellowship (PDCTR 301304/2022-0). MF thanks the David Rockefeller Center for Latin American Studies of Harvard University, GEF Pro-Especies and Coordenacao de Aperfeicoamento de Pessoal de N & imath;vel Superior (CAPES; Proc. 88887.927982/2023-00) for fellowships. LJCLM thanks CAPES [#88887.630472/2021-00] and FAPESP [#2022/01213-7] for scholarships.

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Integrative species delimitation and biogeography of the Rhinella margaritifera species group (Amphibia, Anura, Bufonidae) suggest an intense diversification throughout Amazonia during the last 10 million years

Publicated to:SYSTEMATICS AND BIODIVERSITY. 22 (1): 2291086- - 2024-12-31 22(1), DOI: 10.1080/14772000.2023.2291086

Authors: Fouquet, Antoine; Ferrao, Miqueias; Rodrigues, Miguel T; Werneck, Fernanda P; Prates, Ivan; Moraes, Leandro J C L; Hrbek, Tomas; Chaparro, Juan C; Lima, Albertina P; Perez, Renata; Pansonato, Andre; Carvalho, Vinicius T; Almeida, Alexandre P; Gordo, Marcelo; Farias, Izeni P; Milto, Konstantin D; Roberto, Igor J; Rojas, Rommel R; Ron, Santiago R; Guerra, Vinicius; Recoder, Renato; Camacho, Agustin; Mamani, Luis; Rainha, Raissa N; Avila, Robson W

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Abstract

The accumulation of studies delimiting species in Amazonia has not only shed light on the patterns of its outstanding species richness but also allowed a better understanding of the processes of diversification within this immense region. Nevertheless, vast knowledge gaps remain even for prominent anuran species complexes, such as the Rhinella margaritifera species group. This clade of toads comprises 23 valid species-level taxa, mainly distributed in Amazonia but also in South America's Dry Diagonal and Atlantic and trans-Andean rainforests. Species boundaries and taxonomy in this group are notoriously complex, with studies suggesting the existence of several unnamed species. Available phylogenetic information suggests an Andean-western Amazonian origin of the group with subsequent diversification within Amazonian lowlands during the last 10 Myr and secondary dispersals into other Neotropical regions. To further test this biogeographic scenario and improve knowledge on species diversity, we used an unprecedentedly large mtDNA sampling (>800 16S sequences) across the clade's distribution and comprising all but one described species. We delimited 54 Molecular Operational Taxonomic Units, which we tested further based on patterns of variation of a nuclear locus and acoustic and morphological data. This approach confirmed the existence of at least 25 candidate species, 19 of which correspond to currently recognized taxa whereas 30 remained 'unconfirmed'. Our results clarify the taxonomic status of some species but also suggest multiple introgression events that blur some mtDNA-based species boundaries. Lastly, to provide a temporal framework for the clade's diversification, we generated a time-calibrated phylogenetic tree based on a mitogenomic matrix, which confirmed a Miocene (similar to 9 Ma) western Amazonian origin and six major clades in the group, each having initially diversified in different regions within Amazonia. Most of these clades have later dispersed throughout Amazonia during the establishment of the modern Amazonian hydrographic system, i.e., in the last 6 Myr.

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