The mystery of the origins of Cebus albifrons malitiosus and Cebus albifrons hypoleucus: mitogenomics and microsatellite analyses revealed an amazing evolutionary history of the Northern Colombian white-fronted capuchins

Abstract

Knowledge of the genetic units of species is fundamental to the conservation of biodiversity. This is true for all regions, including the Neotropics where the Earth has its greatest diversity, including roughly 34% of primate species, a group that has almost 60% of its taxa threatened with extinction. The untufted (gracile) capuchins are medium-sized Neotropical primates, traditionally classified in four species: Cebus albifrons, C. capucinus, C. olivaceus, and C. kaapori. They have a very confusing intra-specific systematics with a large number of fragmented and isolated populations throughout their geographical distributions. We sequenced a large sample of gracile capuchins, including all of the recognized species, to offset the paucity of phylogenic and phylogeographic data regarding this group and to try to understand their phylogeny and evolution. A set of 189 gracile and robust capuchins were sequenced for their mitogenomes whereas another set of 394 gracile and robust capuchins were sequenced at two individual mitochondrial genes (mtCOI-COII). Additionally, 41 Colombian gracile capuchins were geno typified at eight nuclear DNA microsatellites. Our main findings are as follows: (1) Nineteen different groups of gracile capuchin were detected with the mitogenomics data set and more than twenty significant groups and sub-groups were identified with the mtCOI-COII genes; (2) The temporal splits of the older gracile capuchin haplogroups expanded between 2 and 4 million years ago (MYA), during the Pliocene; (3) The two most northern taxa of Colombian C. albifrons (malitiosus and hypoleucus) are the same taxon (C. a. hypoleucus) as was claimed by Cabrera. This taxon represents an old colonization event from the Amazon to current northern Colombia. It is intensely hybridized (evidence from both mitochondrial and nuclear genes) with a haplogroup of C. capucinus (H3) and also has an influx of robust capuchins; (4) Three different and independent migrations of C. albifrons from the Amazon arrived to northern Colombia giving rise to C. a. hypoleucus (including malitiosus), C. a versicolor (including leucocephalus, cesarae, and pleei), and C. a. adustus; (5) On the Caribbean island of Trinidad, two different gracile capuchin taxa exist, one autochthonous, which could correspond to a fourth migration into northwestern South America (C. a. trinitatis) and probably another one, introduced more recently (C. olivaceus brunneus); (6) The values of the genetic distance analyses, the inexistence of reciprocal mitochondrial monophylia for many clades of gracile capuchins and the strong hybridization detected with nuclear microsatellites, especially among hypoleucus (malitiosus), C. capucinus-H3, versicolor, and cesarae, support that all the gracile capuchins belong to one unique superspecies: C. capucinus (senior name for all the gracile capuchins).

Keywords:

• Cebus
• gracile capuchins
• malitiosus
• hypoleucus
• mitogenomics
• nuclear DNA microsatellites
• hybridization
• northern Colombia

Acknowledgements

Thanks to Dr. Diana Alvarez, Pablo Escobar-Armel, Nicolás Lichilín, Luisa Fernanda Castellanos-Mora, and Armando Castellanos, for their respective help in obtaining capuchins samples during the last 20 years. Many thanks to Dr. Horacio Schneider and to Dr. Iracilda Sampaio to provide DNA samples of one Cebus olivaceus and one Cebus kaapori. Thanks to the Ministerio del Ambiente Ecuatoriano (MAE) in Santo Domingo de Tsáchilas and in Coca, to the Instituto von Humboldt (Colombia), to 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, to the Colección Boliviana de Fauna (Dr. Julieta Vargas), and to CITES Bolivia for their role in facilitating the obtainment of the collection permits in Ecuador, Colombia, Peru and Bolivia. The first author also thanks the help of 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) by their assistance in obtaining samples of white faced capuchins.

Disclosure statement

The authors report no conflicts of interest. The authors alone are responsible for the content and writing of this article.