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International Journal of Primatology

, Volume 39, Issue 6, pp 1068–1104 | Cite as

How Many Species, Taxa, or Lineages of Cebus albifrons (Platyrrhini, Primates) Inhabit Ecuador? Insights from Mitogenomics

  • Manuel Ruiz-GarcíaEmail author
  • Sebastián Sánchez-Castillo
  • María Ignacia Castillo
  • Kelly Luengas
  • Juan Manuel Ortega
  • Pablo Moreno
  • Luis Albuja
  • Christian Miguel Pinto
  • Joseph Mark Shostell
Article

Abstract

A first step in protecting groups of similarly structured organisms is to place them into discrete taxa. Molecular genetics and phylogeny allow us to rebuild the evolutionary history of these taxa. The Neotropics has roughly 34% of Earth’s primate diversity. However, the systematics of Neotropical primates is complex and controversial. The untufted (gracile) capuchins are traditionally classified as four species: Cebus albifrons, C. capucinus, C. olivaceus, and C. kaapori. Of these, Cebus albifrons has confusing intraspecific systematics with a large number of fragmented and isolated populations throughout its geographical distribution, and up to 13 morphological subspecies. The number of taxa of this species in Ecuador, some areas of northern and eastern Colombia, and Trinidad Island is particularly debated. Primatologists have defined two taxa of C. albifrons in Ecuador: a trans-Andean population: C. a. aequatorialis (or C. aequatorialis) and a cis-Andean population: C. a. yuracus (or C. yuracus). To better understand the systematics of this species, we sequenced the mitogenomes of 136 Cebus albifrons, two Cebus olivaceus, and one Cebus kaapori. Our phylogenetic analyses revealed at least nine significantly different haplogroups of C. albifrons in Ecuador, four of which contained exemplars from both the trans-Andean Pacific Ecuador and the cis-Andean Ecuadorian Amazon. The splits of these Ecuadorian haplogroups, and the initial diversification within them, occurred during the Middle to Late Pliocene and the beginning of the Pleistocene. Individuals we analyzed from Vichada Department in eastern Colombia were genetically distinct from other groups of C. albifrons, agreeing with morphological studies which consider it a full subspecies (C. a. albifrons). Phylogenetic analyses showed two different gracile capuchin taxa on Trinidad Island: C. a. trininatis and C. o. brunneus. We conclude that a large portion of the gracile capuchin taxa form a unique species with a complex of populations and subspecies. The species has conserved its reproductive integrity by repeated episodes of reticulation and high levels of gene flow.

Keywords

Cebus albifrons Ecuador Gracile capuchins Mitogenomics Pleistocene Pliocene Spatial structure Systematics 

Notes

Acknowledgments

We thank Dr. Diana Alvarez, Pablo Escobar-Armel, Nicolás Lichilín, Luisa Fernanda Castellanos-Mora, Armando Castellanos, Andrés Laguna, and Lina Argüello for their respective help in obtaining capuchin samples during the last 20 years. We thank Dr. Horacio Schneider and Dr. Iracilda Sampaio for providing DNA samples of Cebus olivaceus and Cebus kaapori. We express our appreciation to the Ministerio del Ambiente Ecuatoriano (MAE) in Santo Domingo de Tsáchilas and in Coca, the Instituto von Humboldt (Colombia), the Peruvian Ministry of Environment, PRODUCE (Dirección Nacional de Extracción y Procesamiento Pesquero), Consejo Nacional del Ambiente and the Instituto Nacional de Recursos Naturales (INRENA) from Peru, the Colección Boliviana de Fauna (Dr. Julieta Vargas), and CITES Bolivia for their role in facilitating the obtainment of the collection permits in Ecuador, Colombia, Peru, and Bolivia. We extend special thanks to the many people of diverse Indian tribes in Ecuador (Kichwa, Huaorani, Shuar, and Achuar), in Colombia (Jaguas, Ticunas, Huitoto, Cocama, Tucano, Nonuya, Yuri, and Yucuna), in Peru (Bora, Ocaina, Shipigo-Comibo, Capanahua, Angoteros, Orejón, Cocama, Kishuarana, and Alamas), and Bolivia (Sirionó, Canichana, Cayubaba, and Chacobo) for their assistance in obtaining samples of white-faced capuchins. We also acknowledge the editor and reviewers for their suggestions to improve the quality of the manuscript.

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Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Manuel Ruiz-García
    • 1
    Email author
  • Sebastián Sánchez-Castillo
    • 1
  • María Ignacia Castillo
    • 1
  • Kelly Luengas
    • 1
  • Juan Manuel Ortega
    • 1
  • Pablo Moreno
    • 2
  • Luis Albuja
    • 3
  • Christian Miguel Pinto
    • 3
  • Joseph Mark Shostell
    • 4
  1. 1.Laboratorio de Genética de Poblaciones Molecular-Biología Evolutiva, Unidad de Genética Departamento de Biología, Facultad de CienciasPontificia Universidad JaverianaBogotáColombia
  2. 2.Instituto Nacional de BiodiversidadQuitoEcuador
  3. 3.Instituto de Ciencias BiológicasEscuela Politécnica NacionalQuitoEcuador
  4. 4.Math, Science and Technology DepartmentUniversity of Minnesota CrookstonCrookstonUSA

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