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Molecular phylogenetic inference of the howler monkey radiation (Primates: Alouatta)

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Abstract

Howler monkeys (Alouatta), comprising between nine and 14 species and ranging from southern Mexico to northern Argentina, are the most widely distributed platyrrhines. Previous phylogenetic studies of howlers have used chromosomal and morphological characters and a limited number of molecular markers; however, branching patterns conflict between studies or remain unresolved. We performed a new phylogenetic analysis of Alouatta using both concatenated and coalescent-based species tree approaches based on 14 unlinked non-coding intergenic nuclear regions. Our taxon sampling included five of the seven South American species (Alouatta caraya, Alouatta belzebul, Alouatta guariba, Alouatta seniculus, Alouatta sara) and the two recognized species from Mesoamerica (Alouatta pigra, Alouatta palliata). Similarly to previous studies, our phylogenies supported a Mesoamerican clade and a South American clade. For the South American howlers, both methods recovered the Atlantic Forest endemic A. guariba as sister to all remaining South American species, albeit with moderate support. Moreover, we found no support for the previously proposed sister relationship between A. guariba and A. belzebul. For the first time, a clade composed of A. sara and A. caraya was identified. The relationships among the other South American howlers, however, were not fully supported. Our estimates for divergence times within Alouatta are generally older compared to estimates in earlier studies. However, they conform to recent studies proposing a Miocene age for the Isthmus of Panama and for the uplift of the northern Andes. Our results also point to an early genetic isolation of A. guariba in the Atlantic Forest, in agreement with the hypothesis of biotic exchange across South American rain forests in the Miocene. Collectively, these findings contribute to a better understanding of the diversification processes among howler monkey species; however, they also suggest that further comprehension of the evolutionary history of the Alouatta radiation will rely on broadened taxonomic, geographic, and genomic sampling.

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Acknowledgments

We thank Dr. Derek Wildman (University of Illinois), Cristiani Gifalli-Iughetti (University of São Paulo), and Dr. Liliana Cortés-Ortiz (University of Michigan) for graciously sharing DNA samples of Alouatta with us. We also thank the various members of the Carnaval lab for feedback on the initial manuscript and University of São Paulo/Hemocentro Ribeirão Preto members for assistance with DNA sequencing. This research was funded by the City College of New York, the National Science Foundation (NSF), and a Professional Staff Congress-City University of New York award (66309-0044) to E.E.H.; A. Carnaval acknowledges funding by the NSF, the São Paulo Research Foundation, and the National Aeronautics and Space Administration, through the Dimensions of Biodiversity Program (DEB 1343578).

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Authors and Affiliations

  1. Department of Biology, City College of New York, New York, NY, USA

    Esmeralda D. Doyle, Ivan Prates & Ana Carolina Carnaval

  2. Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI, USA

    Ivan Prates

  3. Instituto de Estudos Costeiros, Universidade Federal Do Pará, Campus de Bragança, Belém, PA, Brazil

    Iracilda Sampaio

  4. Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil

    Celia Koiffmann

  5. Departamento de Genética, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, SP, Brazil

    Wilson Araujo Silva Jr.

  6. The Graduate Center, The City University of New York, New York, NY, USA

    Ana Carolina Carnaval

  7. Department of Biological Sciences and Geology, Queensborough Community College, The City University of New York, New York, NY, USA

    Eugene E. Harris

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  1. Esmeralda D. Doyle
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Doyle, E.D., Prates, I., Sampaio, I. et al. Molecular phylogenetic inference of the howler monkey radiation (Primates: Alouatta). Primates 62, 177–188 (2021). https://doi.org/10.1007/s10329-020-00854-x

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