RESUMO
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).
Assuntos
Cebus/classificação , Cebus/genética , Genoma Mitocondrial/genética , Repetições de Microssatélites/genética , Filogenia , Animais , ColômbiaRESUMO
We analyzed 156 specimens of diverse howler monkey taxa (Alouatta; Atelidae, Primates) for different mitochondrial genes (5,567 base pairs), with special emphasis on A. palliata and related taxa. Our results showed no relevant differences among individuals of different putative taxa, A. p. palliata, A. p. aequatorialis, A. coibensis coibensis, and A. c. trabeata. We found no spatial differences in genetic structure of A. p. palliata throughout Costa Rica, Nicaragua, and Honduras. A. p. mexicana (genetic distance: 1.6-2.1%) was the most differentiated taxon within A. palliata. Therefore, we postulate the existence of only 2 clearly defined subspecies within A. palliata (A. p. palliata and A. p. mexicana). A. palliata and A. pigra (traditionally considered a subspecies of A. palliata) are 2 clearly differentiated species as was demonstrated by Cortés-Ortiz and colleagues in 2003, with a temporal split between the 2 species around 3.6-3.7 million years ago (MYA). Our results with the Median Joining Network procedure showed that the ancestors of the cis-Andean Alouatta gave rise to the ancestors of the trans-Andean Alouatta around 6.0-6.9 MYA. As Cortés-Ortiz et al. showed, A. sara and A. macconnelli are differentiable species from A. seniculus, although the first 2 taxa were traditionally considered subspecies of A. seniculus. Our findings agree with the possibility that the ancestor of A. sara gave rise to the ancestor of A. pigra in northern South America. In turn, the ancestor of A. pigra originated the ancestor of A. palliata. Two of our results strongly support the hypothesis that the South American A. palliata (the putative A. p. aequatorialis) was the original population of this species; it has high genetic diversity and no evidence of population expansion. The Central America A. palliata is the derived population. It has low genetic diversity and there is clear evidence of population expansion. However, A. palliata and A. pigra probably migrated into Central America by 2 different routes: the Isthmus of Panama (A. palliata) and Caribbean island arch (A. pigra). Finally, the red howler monkeys from the island of Trinidad in the Caribbean Sea were not A. macconnelli (= A. s. stramineus) as Groves maintained in his influential 2001 publication on primate taxonomy. This taxon is more related to A. s. seniculus, although it formed a monophyletic clade. Future molecular and karyotypic studies will show if the Trinidad red howler monkeys should be considered as an extension of the Venezuelan taxon, A. arctoidea, as a subspecies of A. seniculus(A. s. seniculus), or, in the case of extensive chromosomal rearrangements, even a new species.