Abstract
The Atlantic Forest harbors a large species richness and high levels of endemism, but the processes that shaped its biodiversity are poorly studied, especially for mammals. Among them are the endemic mice Juliomys, which comprise forest dwellers distributed in southeastern and southern Brazil, northeastern Argentina, and eastern Paraguay. In this study, we investigate the phylogenetic relationships among species and perform phylogeographic analyses to evaluate the population structure and demographic scenarios through mitochondrial gene cytochrome b sequences. We investigate three hypotheses of diversification (forest refuges, montane isolate, and geomorphological events) to understand the evolution of the Juliomys species. Phylogenetic analyses recovered five clades/lineages, four of which are congruent with species currently recognized. The fifth lineage expands the range of the genus 659 km to the north and may represent a new species. The observed demographic and geographic structure of genetic diversity does not match the forest refuge hypothesis as mechanism to explain the diversification in Juliomys. Our results recovered J. rimofrons and J. ximenezi as sister species, supporting predictions of montane isolate hypothesis. We also detected a shallow genetic structure in J. pictipes and J. ossitenuis. Both phylogeographic breaks were congruent with limits of the São Paulo Basin, an area that has undergone Neogene reactivations of tectonic faults. It is suggested that geomorphological events led to a deformed landscape that influenced the dynamics of sedimentary basins and promoted an incipient population structure in J. pictipes and J. ossitenuis. Our findings demonstrate that the divergences whithin Juliomys species occurred during the Quaternary, too recently to have produced strong geographic structure.
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Data availability
Sequence data will be deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and will be publicly available. Datasets generated and/or analyzed during the current study are also available from the corresponding author on request.
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Acknowledgements
We are thankful for the curators and collection support staff: Paulo D’Andrea (LABPMR, IOC/Fiocruz), Claudia Costa (PUC-Minas), João Oliveira (MN/UFRJ), Maurício Graipel and Jorge Cherem (UFSC), for kindly providing tissues. We are grateful to Dr. Victor O. Becker and Mrs. Clemira Souza (owners of the Serra Bonita Reserve Complex) to their logistic support during fieldworks conducted in Camacan municipality. We thank the Sociedade Brasileira de Mastozoologia (SBMz) for its help in organizing the II Field Course held at RPPN Serra Bonita, where the specimen Juliomys sp. analyzed in this article was collected. We would like to thank Tom Giarla and anonymous reviewers for suggestions to improve the manuscript.
Funding
We are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), INCA/Ministry of Health-Brazil, and Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) for financial support. This study was part of the project “Characterization of terrestrial vertebrates at the RPPN Complex of Serra Bonita as an aid for its effective management,” which was supported by the Boticário Group Foundation for Nature Protection (Project No. 0818-20091). This study was also supported by Universidade Estadual de Santa Cruz (UESC) (#00220.1100.953 and #00220.1100.1048). MW received research fellowships from CNPq (309654-2020-3) and FAPERJ (E-26/201.232/2022), and a grant from FAPERJ (E-26/211.406/2019). EDH received research fellowship from CNPq (403761/2020-4) and (400172/2022-4), and a grant from FAPESP (2016/50127-5). CRB received research fellowships from CNPq (304498/2014-9) and FAPERJ (E26/010.001425/2019).
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All authors contributed to the study conception and design. Tissue and cells acquisition was performed by Carolina Pires, Marcelo Weksler, Cibele R. Bonvicino, Erika Hingst-Zaher, Martín Alvarez, and Michel B. Faria. Material preparation, data collection and edition of figures were performed by Carolina Pires, Rayque O. Lanes, and Maria Carolina Viana. Analyses and writing were performed by Carolina Pires, Marcelo Weksler, and Cibele R. Bonvicino. All authors commented on previous versions of the manuscript, reading and approving the final manuscript.
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Marcelo Weksler and Cibele R. Bonvicino are co-senior authors.
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Online Resource 3: Phylogenetic trees using codon-position partitioned models inferred for Juliomys based on the gene mt-Cytb
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Pires, C., Weksler, M., Lanes, R.O. et al. Systematics and biogeography of the Atlantic Forest endemic genus Juliomys (Rodentia: Cricetidae): A test of diversification hypothesis using mitochondrial data. J Mammal Evol 30, 695–712 (2023). https://doi.org/10.1007/s10914-023-09661-9
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DOI: https://doi.org/10.1007/s10914-023-09661-9