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Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences

Primates volume 56, pages 145–161 (2015)Cite this article

Abstract

Some previous genetic studies have been performed to resolve the molecular phylogenetics of the squirrel monkeys (Saimiri). However, these studies did not show consensus in how many taxa are within this genus and what the relationships among them are. For this reason, we sequenced 2,237 base pairs of the mt COI and COII genes in 218 Saimiri individuals. All, less 12 S. sciureus sciureus from French Guyana, were sampled in the wild. These samples represented all the living Saimiri taxa recognized. There were four main findings of this study. (1) Our analysis detected 17 different Saimiri groups: albigena, cassiquiarensis, five polyphyletic macrodon groups, three polyphyletic ustus groups, sciureus, collinsi, boliviensis, peruviensis, vanzolinii, oerstedii and citrinellus. Four different phylogenetic trees showed the Central American squirrel monkey (S. oerstedii) as the most differentiated taxon. In contrast, albigena was indicated to be the most recent taxon. (2) There was extensive hybridization and/or historical introgression among albigena, different macrodon groups, peruviensis, sciureus and collinsi. (3) Different tests showed that our maximum likelihood tree was consistent with two species of Saimiri: S. oerstedii and S. sciureus. If no cases of hybridization were detected implicating S. vanzolinii, this could be a third recognized species. (4) We also estimated that the first temporal splits within this genus occurred around 1.4–1.6 million years ago, which indicates that the temporal split events within Saimiri were correlated with Pleistocene climatic changes. If the biological species concept is applied because, in this case, it is operative due to observed hybridization in the wild, the number of species within this genus is probably more limited than recently proposed by other authors. The Pleistocene was the fundamental epoch when the mitochondrial Saimiri diversification process occurred.

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Acknowledgments

Thanks go to Dr. Diana Alvarez, Pablo Escobar-Armel, Luisa Fernanda Castellanos-Mora and Nicolás Lichilín for their respective help in obtaining Saimiri samples during the last 14 years. The sampling procedures employed in this work complied with all the protocols approved by the Ethical Committee of the Pontificia Universidad Javeriana (No. 45684) and the laws of the Ministerio de Ambiente, Vivienda y Desarrollo Territorial (R 1256) from Colombia. This research adhered to the stipulations set by the American Society of Primatologists. Many thanks go to the Peruvian Ministry of Environment, to the PRODUCE (Oficio No 5225), from Peru, the Consejo Nacional del Ambiente and the Instituto Nacional de Recursos Naturales (INRENA, Peru), to the Colección Boliviana de Fauna (Dr. Julieta Vargas; La Paz, Bolivia), to CITES Bolivia (permissions 01482, 01483, 01737, 01738, 01739, 01740, 01741) and to the Ministerio del Ambiente (permission HJK-9788) in Coca (Ecuador) for their role in facilitating the obtainment of the collection permits in Peru, Bolivia and Ecuador. Also many thanks to the Brazilian institutions for collaborating with this study (IBAMA protocol number 77933). All animal sampling in French Guiana was carried out in accordance with French animal care regulations and laws. The first author also thanks the Ticuna, Yucuna, Yaguas, Witoto and Cocama Indian communities at the Colombian Amazon, the Bora, Ocaina, Shipibo-Comibo, Capanahua, Angoteros, Orejón, Yaguas, Cocama, Kishuarana and Alama in the Peruvian Amazon, the Sirionó, and Chacobo in the Bolivian Amazon and the Marubos, Kulina, Maku and Waimiri-Atroari communities in the Brazilian Amazon. Dr. Joseph Shostell helped with the English syntax.

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Authors and Affiliations

  1. Unidad de Genética. Laboratorio de Genética de Poblaciones-Biología Evolutiva. Departamento de Biología. Facultad de Ciencias, Pontificia Universidad Javeriana, Cra 7A No 43-82, Bogotá, DC, Colombia

    Manuel Ruiz-García & Kelly Luengas-Villamil

  2. Secretaria Distrital Ambiental (SDA), Bogotá, DC, Colombia

    Norberto Leguizamon

  3. Laboratoire des Interactions Virus-Hotes, Institut Pasteur de la Guyane, 23 avenue Pasteur, BP 6010, 97306, Cayenne Cedex, French Guiana

    Benoit de Thoisy

  4. Instituto Veterinario de Investigaciones Tropicales y de Altura, Estación Experimental, Iquitos, Peru

    Hugo Gálvez

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  1. Manuel Ruiz-García
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  2. Kelly Luengas-Villamil
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Correspondence to Manuel Ruiz-García.

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Ruiz-García, M., Luengas-Villamil, K., Leguizamon, N. et al. Molecular phylogenetics and phylogeography of all the Saimiri taxa (Cebidae, Primates) inferred from mt COI and COII gene sequences. Primates 56, 145–161 (2015). https://doi.org/10.1007/s10329-014-0452-0

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Keywords

  • Saimiri
  • Phylogenetics and phylogeography
  • Mitochondrial COI and COII genes
  • Biological species concept
  • Pleistocene climatic changes