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

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.