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Coalescent analysis of mtDNA indicates Pleistocene divergence among three species of howler monkey (Alouatta spp.) and population subdivision within the Atlantic Coastal Forest species, A. guariba

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Abstract

We have used coalescent analysis of mtDNA cytochrome b (cyt b) sequences to estimate times of divergence of three species of Alouatta—A. caraya, A. belzebul, and A. guariba—which are in close geographic proximity. A. caraya is inferred to have diverged from the A. guariba/A. belzebul clade approximately 3.83  million years ago (MYA), with the later pair diverging approximately 1.55 MYA. These dates are much more recent than previous dates based on molecular-clock methods. In addition, analyses of new sequences from the Atlantic Coastal Forest species A. guariba indicate the presence of two distinct haplogroups corresponding to northern and southern populations with both haplogroups occurring in sympatry within Sao Paulo state. The time of divergence of these two haplogroups is estimated to be 1.2 MYA and so follows quite closely after the divergence of A. guariba and A. belzebul. These more recent dates point to the importance of Pleistocene environmental events as important factors in the diversification of A. belzebul and A. guariba. We discuss the diversification of the three Alouatta species in the context of recent models of climatic change and with regard to recent molecular phylogeographic analyses of other animal groups distributed in Brazil.

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Acknowledgments

The authors would like to thank Rodrigo S. dos Santos for critical reviews. Thanks to Marcus V. Domingues, Leon Franciatto, Paulo Noffs, and Jose Grau for the figures. The authors wish to thank Drs Zelinda Hirano Braga and Julio César de Souza Júnior of FURB (Universidade Regional de Blumenau) for samples of Alouatta. We also would like to thank two anonymous reviewers and an anonymous associate editor for detailed and helpful comments. Part of this work was carried out by using the resources of the Computational Biology Service Unit from Cornell University which is partially funded by Microsoft Corporation. This work became possible through financial aid from CAPES PRODOC grant number 0072/087 (to FMM), from CEPED-FAPESP (to CPK), and CUNY RF Awards 67468-00-36 and 68625-0037 (to EEH). Sampling from live animals was carried out in accordance with Brazilian animal care regulations and laws, and also complied with ethical standards for the treatment of animals in the guidelines of the Primate Society of Japan.

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  1. Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, Rua do Matão, Travessa 14, número 101, São Paulo, SP, CEP 05508-900, Brazil

    Felipe de Mello Martins

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

    Cristiani Gifalli-Iughetti & Celia Priszkulnik Koiffman

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

    Eugene E. Harris

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  1. Felipe de Mello Martins
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Correspondence to Felipe de Mello Martins.

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de Mello Martins, F., Gifalli-Iughetti, C., Koiffman, C.P. et al. Coalescent analysis of mtDNA indicates Pleistocene divergence among three species of howler monkey (Alouatta spp.) and population subdivision within the Atlantic Coastal Forest species, A. guariba . Primates 52, 77–87 (2011). https://doi.org/10.1007/s10329-010-0226-2

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