Historical climate changes and hybridization shaped the evolution of Atlantic Forest spinetails (Aves: Furnariidae)

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Abstract

Combining phylogeographic approaches and hybrid zone inference in a single framework is a robust way to depict respectively the biogeographic history of lineages and the evolutionary processes responsible for speciation. Here, we studied the spatiotemporal patterns of diversification and characterize the hybrid zone between two Atlantic Forest spinetails (Synallaxis ruficapilla and Synallaxis cinerea) using mitochondrial DNA and nuclear (autosomal and Z-linked) genes. We consistently recovered divergence between and within the two species during the late Pliocene and Pleistocene using an isolation with migration model. Also, our results indicate distinct levels of introgression among lineages. Ecological niche models and demographic inferences, used to infer range distributions throughout the late Quaternary, were not consistent with the hypothesis of a large river as a primary barrier responsible for the divergence of the two species. Instead, a scenario of isolation and divergence followed by geographic expansion and admixture as a consequence of Quaternary climatic oscillations was supported. Paleomodels also were not consistent with the idea that the hybrid zone originated in primary differentiation and favor a secondary contact scenario. Model fitting indicated that clines of different loci spanning the hybrid zone are coincident and concordant. The narrow cline for one Z-linked locus could be indicative of some form of post-zygotic selection hindering genetic homogenization between the two species.

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Data archiving

The sequences generated in this study were deposited in GenBank under the following accession numbers: cytb, MK920451–MK920538; ND2, MK920539–MK920623; FIB5, MK920697–MK920776; myo2, MK920624–MK920696; BRM15, MK920873–MK920920; CHDZ18, MK920825–MK920872; PLAA, MK920777–MK920824.

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Acknowledgements

The authors thank Marcos Raposo (MNRJ), Fabrício R. Santos (UFMG), Jon Fjeldså (ZMUC), Carla Fontana (MCP), and Luis F. Silveira (MZUSP) for providing some of the tissues used in this study. The authors thank Fábio S. R. Amaral, Claydson P. Assis, Luciano M. Lima, Ana C. Fazza, Tiago S. Ribeiro, and Sidnei S. Santos for their immense help in fieldwork. The authors are grateful to Rilquer Mascarenhas for help with ecological niche model analyses. The authors thank the Reserva Ecológica Michelin (Kevin Flesher) for logistic support during sampling in its area. This study was funded by Fundação de Amparo à Pesquisa do Estado de São Paulo—FAPESP (2008/05705-4; BIOTA 2013/50297-0), NSF (DEB 1343578), NASA, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 443249/2014-8, 303713/2015-1), PROPCI/UFBA (PRODOC-2013/5813), and Fundação de Amparo à Pesquisa do Estado da Bahia (FAPESB RED0045/2014, JCB0026/2016). H.B.-F. also acknowledges the CNPq Research Productivity Fellowships (307037/2018-5). Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis and Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) provided permits to collect the samples. This work was developed in the Research Center on Biodiversity and Computing (BioComp) of the Universidade de São Paulo (USP), supported by the USP Provost’s Office for Research. The authors thank two anonymous reviewers for their comments that improved this work.

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