Chromatic discrimination in fixed saturation levels from tufted capuchin monkeys with different color vision genotypes.

Recent research has proposed new approaches to investigate color vision in Old World Monkeys by measuring suprathreshold chromatic discrimination. In this study, we aimed to extend this approach to New World Monkeys with different color vision genotypes by examining their performance in chromatic discrimination tasks along different fixed chromatic saturation axes. Four tufted capuchin monkeys were included in the study, and their color vision genotypes were one classical protanope, one classical deuteranope, one non-classical protanope, and a normal trichromat. During the experiments, the monkeys were required to perform a chromatic discrimination task using pseudoisochromatic stimuli with varying target saturations of 0.06, 0.04, 0.03, and 0.02 u'v' units. The number of errors made by the monkeys along different chromatic axes was recorded, and their performance was quantified using the binomial probability of their hits during the tests. Our results showed that dichromatic monkeys made more errors near the color confusion lines associated with their specific color vision genotypes, while the trichromatic monkey did not demonstrate any systematic errors. At high chromatic saturation, the trichromatic monkey had significant hits in the chromatic axes around the 180° chromatic axis, whereas the dichromatic monkeys had errors in colors around the color confusion lines. At lower saturation, the performance of the dichromatic monkeys became more challenging to differentiate among the three types, but it was still distinct from that of the trichromatic monkey. In conclusion, our findings suggest that high saturation conditions can be used to identify the color vision dichromatic phenotype of capuchin monkeys, while low chromatic saturation conditions enable the distinction between trichromats and dichromats. These results extend the understanding of color vision in New World Monkeys and highlight the usefulness of suprathreshold chromatic discrimination measures in exploring color vision in non-human primates.

Phylogeography, genetic diversity, and intraspecific genetic structure of the black-horned capuchin (Sapajus nigritus).

Recent molecular studies have clarified the overarching taxonomy of capuchin monkeys, but intraspecific genetic diversity remains unexplored for most capuchin species. One example is Sapajus nigritus, the southernmost capuchin monkey, found in Brazil and Argentina; its phenotypic diversity has been recognized as two geographic subspecies, but the intraspecific genetic structure of this taxon is poorly known. Here, we sampled across most of this species' geographic distribution, producing a newly sequenced data set for genetic analyses that included 78 individuals from 14 populations. We investigated the intraspecific diversity, genetic structure, and evolutionary history using three mitochondrial markers. Our results indicated that S. nigritus populations exhibited high levels of genetic structure. We found strong support for two monophyletic clades within this species with a deep phylogenetic split, and clear separation from other related taxa. Vicariance events seem to have played a prevalent role in shaping S. nigritus genetic differentiation. The Paraíba do Sul River may have driven the deep divergence between southern and northern clades, whereas the Tietê River may have had a weaker, more recent effect on the divergence of populations within the southern clade.

A New Assessment of Robust Capuchin Monkey (Sapajus) Evolutionary History Using Genome-Wide SNP Marker Data and a Bayesian Approach to Species Delimitation.

Robust capuchin monkeys, Sapajus genus, are among the most phenotypically diverse and widespread groups of primates in South America, with one of the most confusing and often shifting taxonomies. We used a ddRADseq approach to generate genome-wide SNP markers for 171 individuals from all putative extant species of Sapajus to access their evolutionary history. Using maximum likelihood, multispecies coalescent phylogenetic inference, and a Bayes Factor method to test for alternative hypotheses of species delimitation, we inferred the phylogenetic history of the Sapajus radiation, evaluating the number of discrete species supported. Our results support the recognition of three species from the Atlantic Forest south of the São Francisco River, with these species being the first splits in the robust capuchin radiation. Our results were congruent in recovering the Pantanal and Amazonian Sapajus as structured into three monophyletic clades, though new morphological assessments are necessary, as the Amazonian clades do not agree with previous morphology-based taxonomic distributions. Phylogenetic reconstructions for Sapajus occurring in the Cerrado, Caatinga, and northeastern Atlantic Forest were less congruent with morphology-based phylogenetic reconstructions, as the bearded capuchin was recovered as a paraphyletic clade, with samples from the Caatinga biome being either a monophyletic clade or nested with the blond capuchin monkey.

Mapping Retrotransposon LINE-1 Sequences into Two Cebidae Species and Homo sapiens Genomes and a Short Review on Primates.

This work focuses on the distribution of LINE-1 (a Long Interspersed Nuclear Element) in primates and its role during evolution and as a constituent of the architecture of primate genomes. To pinpoint the LINE-1 repeat distribution and its role among primates, LINE-1 probes were mapped onto chromosomes of Homo sapiens (Hominidae, Catarrhini), Sapajus apella, and Cebus capucinus (Cebidae, Platyrrhini) using fluorescence in situ hybridisation (FISH). The choice of platyrrhine species are due to the fact they are taxa characterised by a high level of rearrangements; for this reason, they could be a useful model for the study of LINE-1 and chromosome evolution. LINE-1 accumulation was found in the two Cebidae at the centromere of almost all acrocentric chromosomes 16-22 and on some bi-armed chromosomes. LINE-1 pattern was similar in the two species but only for chromosomes 6, 8, 10, and 18, due to intrachromosomal rearrangements in agreement with what was previously hypothesised as through g banding. LINE-1 interstitial accumulation was found in humans on the 1, 8, 9, 13-15, and X chromosomes; on chromosomes 8, 9, and 13-15, the signal was also at the centromeric position. This is in agreement with recent and complete molecular sequence analysis of human chromosomes 8 and some acrocentric ones. Thus, the hypothesis regarding a link between LINE-1 and centromeres as well as a link with rearrangements are discussed. Indeed, data analysis leads us to support a link between LINE-1 and inter- and intrachromosomal rearrangements, as well as a link between LINE-1 and structural functions at centromeres in primates.

Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Recently Integrated Alu Elements in Capuchin Monkeys: A Resource for Cebus/Sapajus Genomics.

Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus. Further, all tufted capuchins were assigned to a single species, Cebus apella, despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus, with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins (Cebus imitator; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.

Major histocompatibility complex class II DR and DQ evolution and variation in wild capuchin monkey species (Cebinae).

The major histocompatibility complex (MHC) is an important gene complex contributing to adaptive immunity. Studies of platyrrhine MHC have focused on identifying experimental models of immune system function in the equivalent Human Leukocyte Antigen (HLA). These genes have thus been explored primarily in captive platyrrhine individuals from research colonies. However, investigations of standing MHC variation and evolution in wild populations are essential to understanding its role in immunity, sociality and ecology. Capuchins are a promising model group exhibiting the greatest habitat diversity, widest diet breadth and arguably the most social complexity among platyrrhines, together likely resulting in varied immunological challenges. We use high-throughput sequencing to characterize polymorphism in four Class II DR and DQ exons for the first time in seven capuchin species. We find evidence for at least three copies for DQ genes and at least five for DRB, with possible additional unrecovered diversity. Our data also reveal common genotypes that are inherited across our most widely sampled population, Cebus imitator in Sector Santa Rosa, Costa Rica. Notably, phylogenetic analyses reveal that platyrrhine DQA sequences form a monophyletic group to the exclusion of all Catarrhini sequences examined. This result is inconsistent with the trans-species hypothesis for MHC evolution across infraorders in Primates and provides further evidence for the independent origin of current MHC genetic diversity in Platyrrhini. Identical allele sharing across cebid species, and more rarely genera, however, does underscore the complexity of MHC gene evolution and the need for more comprehensive assessments of allelic diversity and genome structure.

Assessment of genetic variability in captive capuchin monkeys (Primates: Cebidae).

Capuchin monkeys (genera Cebus and Sapajus) show a wide range distribution, from Honduras to Argentina. The aim of this work was to evaluate the genetic and phenotypic variability of captive specimens putatively belonging to S. cay (SCY) and S. nigritus (SNI) at their southernmost distribution limit. Forty-four individuals held in five captive centers from Argentina were analyzed based on external morphology, karyology and DNA sequences of mitochondrial control region (mtDNA-CR). Three morphotypes associated with their probable geographical origin in SCY and a single morphotype in SNI were found. For SCY we could associate each morphotype with the most frequent karyotype. SNI showed a single phenotype and a homogenous karyotype. Heterochromatin showed geographical patterns within species. A 515-bp mtDNA-CR fragment was sequenced, defining fourteen haplotypes at 59 polymorphic sites. A network constructed with our 14 haplotypes and other 77 from S. apella, S. macrocephalus, S. cay and S. nigritus from bibliography revealed some phylogeographic signals. Our SCY and SNI samples rendered four groups that differed in multiple mutational steps, with SCY being more similar to S. apella than to S. macrocephalus. Also, we identified two genetic divergent SCY groups: samples from NOA and from NEA with high mitochondrial diversity. Our results highlight the relevance of using complementary genetic tools throughout the distribution ranges of SCY and SNI for a better assessment of their diversity.

The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS.

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity.

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.

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).

Association between Genomic Instability and Evolutionary Chromosomal Rearrangements in Neotropical Primates.

During the last decades, the mammalian genome has been proposed to have regions prone to breakage and reorganization concentrated in certain chromosomal bands that seem to correspond to evolutionary breakpoints. These bands are likely to be involved in chromosome fragility or instability. In Primates, some biomarkers of genetic damage may be associated with various degrees of genomic instability. Here, we investigated the usefulness of Sister Chromatid Exchange as a biomarker of potential sites of frequent chromosome breakage and rearrangement in Alouatta caraya, Ateles chamek, Ateles paniscus, and Cebus cay. These Neotropical species have particular genomic and chromosomal features allowing the analysis of genomic instability for comparative purposes. We determined the frequency of spontaneous induction of Sister Chromatid Exchanges and assessed the relationship between these and structural rearrangements implicated in the evolution of the primates of interest. Overall, A. caraya and C. cay presented a low proportion of statistically significant unstable bands, suggesting fairly stable genomes and the existence of some kind of protection against endogenous damage. In contrast, Ateles showed a highly significant proportion of unstable bands; these were mainly found in the rearranged regions, which is consistent with the numerous genomic reorganizations that might have occurred during the evolution of this genus.

A phylogenomic perspective on the robust capuchin monkey (Sapajus) radiation: First evidence for extensive population admixture across South America.

Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provided support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidinosus as sister species; however, S. apella, S. macrocephalus, and S. cay individuals were recovered in two geographic clades, from northeastern and southwestern Amazon, rather than clustering by currently defined morphospecies. STRUCTURE analysis of population clustering revealed widespread admixture among Sapajus populations within the Amazon and even into the Cerrado and Atlantic Forest. Difficulty in assigning species by morphology may be a result of widespread population admixture facilitated through frequent movement across major rivers and even ecosystems by robust capuchin monkeys.

Evidence of a Conserved Molecular Response to Selection for Increased Brain Size in Primates.

The adaptive significance of human brain evolution has been frequently studied through comparisons with other primates. However, the evolution of increased brain size is not restricted to the human lineage but is a general characteristic of primate evolution. Whether or not these independent episodes of increased brain size share a common genetic basis is unclear. We sequenced and de novo assembled the transcriptome from the neocortical tissue of the most highly encephalized nonhuman primate, the tufted capuchin monkey (Cebus apella). Using this novel data set, we conducted a genome-wide analysis of orthologous brain-expressed protein coding genes to identify evidence of conserved gene-phenotype associations and species-specific adaptations during three independent episodes of brain size increase. We identify a greater number of genes associated with either total brain mass or relative brain size across these six species than show species-specific accelerated rates of evolution in individual large-brained lineages. We test the robustness of these associations in an expanded data set of 13 species, through permutation tests and by analyzing how genome-wide patterns of substitution co-vary with brain size. Many of the genes targeted by selection during brain expansion have glutamatergic functions or roles in cell cycle dynamics. We also identify accelerated evolution in a number of individual capuchin genes whose human orthologs are associated with human neuropsychiatric disorders. These findings demonstrate the value of phenotypically informed genome analyses, and suggest at least some aspects of human brain evolution have occurred through conserved gene-phenotype associations. Understanding these commonalities is essential for distinguishing human-specific selection events from general trends in brain evolution.

Chapparvoviruses occur in at least three vertebrate classes and have a broad biogeographic distribution.

Chapparvoviruses are a highly divergent group of parvoviruses (family Parvoviridae) that have recently been identified via metagenomic sampling of animal faeces. Here, we report the sequences of six novel chapparvoviruses identified through both metagenomic sampling of bat tissues and in silico screening of published vertebrate genome assemblies. The novel chapparvoviruses share several distinctive genomic features and group together as a robustly supported monophyletic clade in phylogenetic trees. Our data indicate that chapparvoviruses have a broad host range in vertebrates and a global distribution.

Inbreeding avoidance and female mate choice shape reproductive skew in capuchin monkeys (Cebus capucinus imitator).

Reproductive skew in multimale groups may be determined by the need for alpha males to offer reproductive opportunities as staying incentives to subordinate males (concessions), by the relative fighting ability of the alpha male (tug-of-war) or by how easily females can be monopolized (priority-of-access). These models have rarely been investigated in species with exceptionally long male tenures, such as white-faced capuchins, where female mate choice for novel unrelated males may be important in shaping reproductive skew. We investigated reproductive skew in white-faced capuchins at Sector Santa Rosa, Costa Rica, using 20 years of demographic, behavioural and genetic data. Infant survival and alpha male reproductive success were highest in small multimale groups, which suggests that the presence of subordinate males can be beneficial to the alpha male, in line with the concession model's assumptions. None of the skew models predicted the observed degree of reproductive sharing, and the probability of an alpha male producing offspring was not affected by his relatedness to subordinate males, whether he resided with older subordinate males, whether he was prime aged, the number of males or females in the group or the number of infants conceived within the same month. Instead, the alpha male's probability of producing offspring decreased when he was the sire of the mother, was weak and lacked a well-established position and had a longer tenure. Because our data best supported the inbreeding avoidance hypothesis and female choice for strong novel mates, these hypotheses should be taken into account in future skew models.

Transferability of microsatellites for studies on the social behavior of the tufted capuchin monkey (genus Sapajus).

Because of relevant results that indicated that molecular techniques can provide increased knowledge of animal social systems, they usually complement observational field studies. Despite the great utility of microsatellites, they are not available for all species. Gathering genetic information using microsatellites that were originally designed for other species is a time-saving procedure. The aim of this study was to test the transferability of microsatellites and their usefulness in studies of social behavior of black capuchin monkeys (Sapajus nigritus). We noninvasively sampled adult and subadult black capuchins of three wild groups in southeastern Brazil. Seventeen microsatellites, which were previously designed for and successfully amplified in multiple Neotropical primate species, were tested. Nine of the 17 microsatellite loci tested produced an average of 6.22 alleles (range 2-12) per locus. The allelic richness and the expected heterozygosity for all loci was 5.93 and 0.70, respectively. The combined non-exclusion probability for one candidate parent across all loci was 0.01. The nine microsatellite loci optimized in this study have a great potential for application in studies of social structure and dispersal patterns in S. nigritus populations and in other Neotropical primate species.

Color discrimination in the tufted capuchin monkey, Sapajus spp.

The present study evaluated the efficacy of an adapted version of the Mollon-Reffin test for the behavioral investigation of color vision in capuchin monkeys. Ten tufted capuchin monkeys (Sapajus spp., formerly referred to as Cebus apella) had their DNA analyzed and were characterized as the following: one trichromat female, seven deuteranope dichromats (six males and one female), and two protanope males, one of which was identified as an "ML protanope." For their behavioral characterization, all of the subjects were tested at three regions of the Commission International de l'Eclairage (CIE) 1976 u'v' diagram, with each test consisting of 20 chromatic variation vectors that were radially distributed around the chromaticity point set as the test background. The phenotypes inferred from the behavioral data were in complete agreement with those predicted from the genetic analysis, with the threshold distribution clearly differentiating between trichromats and dichromats and the estimated confusion lines characteristically converging for deuteranopes and the "classic" protanope. The discrimination pattern of the ML protanope was intermediate between protan and deutan, with confusion lines horizontally oriented and parallel to each other. The observed phenotypic differentiation confirmed the efficacy of the Mollon-Reffin test paradigm as a useful tool for evaluating color discrimination in nonhuman primates. Especially noteworthy was the demonstration of behavioral segregation between the "classic" and "ML" protanopes, suggesting identifiable behavioral consequences of even slight variations in the spectral sensitivity of M/L photopigments in dichromats.

Molecular relationships and classification of several tufted capuchin lineages (Cebus apella, Cebus xanthosternos and Cebus nigritus, Cebidae), by means of mitochondrial cytochrome oxidase II gene sequences.

The morphological systematics of the tufted capuchins is confusing. In an attempt to clarify the complex systematics and phylogeography of this taxon, we provide a first molecular analysis. We obtained mitochondrial cytochrome oxidase II (mtCOII) gene sequences from 49 tufted capuchins that had exact geographic origins from diverse lineages in Colombia, Peru, Bolivia, French Guyana, Brazil, Argentina and Paraguay and that belonged to clearly recognized morphological taxa. This project had 4 main findings: (1) we determined 2 established and related taxa in the northern Amazon River area, which we named C. a. apella and C. a. fatuellus. C. a. apella is distributed from French Guyana until, at least, the Negro River in the northern Brazilian Amazon, whereas C. a. fatuellus is distributed throughout the Colombian Eastern Llanos and the northern Colombian Amazon. We also determined 2 other southern C. apella taxa, which we named C. a. macrodon and C. a. cay. C. a. macrodon has a western and southern Amazon distribution, while C. a. cay has a more southern distribution outside the Amazon basin. (2) In the upper Amazon basin, there is a unique lineage (C. a. macrocephalus) with 1 widely distributed haplotype. The 4 morphological subspecies (C. a. maranonis, C. a. macrocephalus, C. a. peruanus, C. a. pallidus), and maybe a fifth unknown subspecies, described in this area were molecularly undifferentiated at least for the mitochondrial gene analyzed. (3) Our molecular analysis determined that 1 individual of C. robustus fell into the lineage of C. a. macrocephalus. Therefore, this form does not receive any specific name. (4) The animals classified a priori as C. nigritus and C. xanthosternos (because of their morphological phenotypes and by their geographical origins) were clearly differentiated from the other specimens analyzed with the molecular marker employed. Therefore, we consider that these 2 lineages could be assigned the status of full species following the biological species definition. (5) In 2001, Groves described 4 tufted capuchin species (C. apella, C. libidinosus, C. nigritus and C. xanthosternos), while Silva Jr. determined 7 species (C. apella, C. macrocephalus, C. libidinosus, C. cay, C. nigritus, C. robustus and C. xanthosternos). The tests of Swofford-Olsen-Waddell-Hillis, of Shimodaira and Hasegawa and of Templeton did not fit with either of these two classificatory schemes, although Groves' scheme was better with regard to our data than that of Silva Jr. (6) All the temporal splits among the tufted capuchin taxa studied were estimated to have occurred during the last phase of the Pleistocene by using the ρ statistic applied to the median joining haplotype network.

Monomorphic region of the serotonin transporter promoter gene in New World monkeys.

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior-related disorders. Among non-human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin-related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene-linked polymorphic region (5-HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5-HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms.

Cebus phylogenetic relationships: a preliminary reassessment of the diversity of the untufted capuchin monkeys.

The untufted, or gracile, capuchin monkeys are currently classified in four species, Cebus albifrons, C. capucinus, C. olivaceus, and C. kaapori, with all but C. kaapori having numerous described subspecies. The taxonomy is controversial and their geographic distributions are poorly known. Cebus albifrons is unusual in its disjunct distribution, with a western and central Amazonian range, a separate range in the northern Andes in Colombia, and isolated populations in Trinidad and west of the Andes in Ecuador and northern Peru. Here we examine previous morphological and molecular hypotheses of the taxonomy and phylogeny of Cebus. We construct a time-calibrated phylogeny based upon mitochondrial DNA sequences from 50 Cebus samples from across their range. Our data indicate that untufted capuchins underwent a radiation at about 2 Ma, and quickly diversified in both the Andes and the Amazon. We provide a provisional reassessment for the taxonomy of untufted capuchins in the Amazon, the Llanos, the Andes, Trinidad, and Central America, splitting currently paraphyletic taxa into several species, including: at least two Amazonian species (C. yuracus and C. unicolor); a species from the Guiana Shield (most likely the same as Humboldt's C. albifrons); two northern Andean species, C. versicolor, C. cesarae; C. brunneus (with trinitatis a junior synonym) on the Venezuelan coast, and C. adustus in the region of Lake Maracaibo; C. capucinus in northwestern Ecuador and Colombia, and Panama; C. imitator in Central America; C. olivaceus and C. castaneus occupying a large part of the Guiana Shield; and C. kaapori in the eastern Amazon, south of the Rio Amazonas. More intensive and extensive geographic sampling is needed, including that for some subspecies not represented here. Taxa from the southwestern Amazon (yuracus, cuscinus, and unicolor) and the phylogenetic position of Humboldt's Simia albifrons from the Orinoco remain particularly poorly defined.