It is misleading to use Sapajus (Robust capuchins) as a genus? A review of the evolution of the capuchins and suggestions on their systematics

The systematics and the evolutionary history of the capuchin monkeys is highly controversial. Recently, Lynch-Alfaro et al., (2012a, b) proposed to split the traditional Cebus genus into two genera, Cebus (gracile capuchins) and Sapajus (robust capuchins) and they also proposed a hypothesis to explain the evolution of these Neotropical primates ("Reinvasion of the Amazon"). Additionally, Bobli et al., (2012) suggested splitting the gracile capuchins into at least 12 species, although traditionally they had been classified into four species. Nevertheless the work of Lynch-Alfaro et al., (2012a) was criticized because of the small number of genes used and limited sample size (Nascimento et al., 2015). Good resolution of a species tree requires the correct identification of species, data from several loci, a high number of individuals per species, and careful analysis of ancient DNA data from museum specimens. Herein, we analyzed 452 capuchin monkeys (both gracile and robust groups) for four mitochondrial genes and a subset of 27 individuals for 16 mitochondrial genes. There were four main findings: 1-Genetic distance values between Cebus and Sapajus were within the range of different species within a genus but significantly less than the values among different genera of Neotropical primates. 2- Genetic diversity was considerably higher in the gracile capuchins than in the robust capuchins. 3- Neither genetic tree showed the monophylia between Cebus and Sapajus. 4- The evolutionary history of the mitochondrial haplotypes within gracile capuchins and robust capuchins began around 4-5 and 3 million years ago (MYA) respectively. Our results along with a review of karyological, morphological, and ethological data of capuchin monkeys do not support a split of the capuchins into two different genera. Also, our hypothesis, "North Amazon gracile origin, Eastern expansion and subsequent reinvasion of the Amazon," more completely explains the evolution of capuchins than does "Reinvasion of the Amazon" hypothesis of Lynch-Alfaro et al., (2012a). The Biological Species Concept (BSC) should be applied to the capuchins more than the Phylogenetic Species Concept (PSC), because we have enough data on many biological aspects of this group. The gracile capuchins should also be classified in a unique species, C. capucinus (including the traditional C. capucinus, C. albifrons and C. olivaceus) with different lineages intermixed in many geographical areas, whilst the robust capuchins should be classified into at least three species C. xantosthernos, C. nigritus and C. apella. It is difficult to apply traditional rules of systematic nomenclature to capuchins. Gracile capuchins underwent many migration events, had high gene flow and there is evidence of continuous mixture among different lineages. In contrast, robust capuchins had explosive Pleistocene radiation, colonized a wide array of extremely different biomes, and generated extreme diversity in morphology. The situation of C. apella should be similar to that of our own species. Explosive radiation occurred in humans within the last 0.1-0.2 MYA allowing us to conquer extremely different ecological conditions, even using tools. Thus, from a phylogenetic perspective, it's probably not important to focus on coat morphological differences for capuchins.