Phylogeny, molecular dating and zoogeographic history of the titi monkeys (Callicebus, Pitheciidae) of eastern Brazil

The titi monkeys belong to a genus of New World primates endemic to South America, which were recently reclassified in three genera (Cheracebus, Plecturocebus and Callicebus). The genus Callicebus, which currently includes five species, is endemic to eastern Brazil, occurring in the Caatinga, Savanna, and Atlantic Forest biomes. In the present study, we investigated the validity of these species and inferred their phylogenetic relationships, divergence times, and biogeographic patterns based on the molecular analysis of a concatenated sequence of 11 mitochondrial and nuclear DNA markers, derived from 13 specimens. We ran Maximum Likelihood (ML) and Bayesian Inference (BI) analyses, and estimated genetic distances, divergence times. Ancestral areas were estimated on BioGeoBears. Our results suggest that at about twelve million years ago, the ancestor of all titi monkeys inhabited a wide area that extended from the Amazon forest to the South of the Atlantic forest. A first vicariant event originated Cheracebus in the West of the Amazon and the ancestor of Callicebus and Plectorocebus which, later were separated by a second one. The diversification of Callicebus occurred during the Plio-Pleistocene (beginning at 5 Ma) probably influenced by climatic fluctuations and geological events. Therefore, the results of the present work confirmed the existence of five species that currently inhabit forested areas under increasing threat from human activities. Thus, a reliable diagnosis of the taxonomic status of species living in endangered environments is extremely important for the development of conservation measures

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 provide 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 interspersed in a widespread clade with no evidence for monophyly for any of these three 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

An Integrative Analysis Uncovers a New, Pseudo-Cryptic Species of Amazonian Marmoset (Primates: Callitrichidae: \u3cem\u3eMico\u3c/em\u3e) from the Arc of Deforestation

Amazonia has the richest primate fauna in the world. Nonetheless, the diversity and distribution of Amazonian primates remain little known and the scarcity of baseline data challenges their conservation. These challenges are especially acute in the Amazonian arc of deforestation, the 2500 km long southern edge of the Amazonian biome that is rapidly being deforested and converted to agricultural and pastoral landscapes. Amazonian marmosets of the genus Mico are little known endemics of this region and therefore a priority for research and conservation efforts. However, even nascent conservation efforts are hampered by taxonomic uncertainties in this group, such as the existence of a potentially new species from the Juruena–Teles Pires interfluve hidden within the M. emiliae epithet. Here we test if these marmosets belong to a distinct species using new morphological, phylogenomic, and geographic distribution data analysed within an integrative taxonomic framework. We discovered a new, pseudo-cryptic Mico species hidden within the epithet M. emiliae, here described and named after Horacio Schneider, the pioneer of molecular phylogenetics of Neotropical primates. We also clarify the distribution, evolutionary and morphological relationships of four other Mico species, bridging Linnean, Wallacean, and Darwinian shortfalls in the conservation of primates in the Amazonian arc of deforestation

Taxonomic review of Saguinus mystax (Spix, 1823) (Primates, Callitrichidae), and description of a new species

Although the Amazon has the greatest diversity of primates, there are still taxonomic uncertainties for many taxa, such as the species of the Saguinus mystax group. The most geographically broadly distributed and phenotypically diverse species in this group is S. mystax, and its phenotypic diversity has been recognized as three subspecies—S. mystax mystax, S. mystax pileatus and S. mystax pluto—with non-overlapping geographic distributions. In this sense, we carried out an extensive field survey in their distribution areas and used a framework of taxonomic hypothesis testing of genomic data combined with an integrative taxonomic decision-making framework to carry out a taxonomic revision of S. mystax. Our tests supported the existence of three lineages/species. The first species corresponds to Saguinus mystax mystax from the left bank of the Juruá River, which was raised to the species level, and we also discovered and described animals from the Juruá–Tefé interfluve previously attributed to S. mystax mystax as a new species. The subspecies S. m. pileatus and S. m. pluto are recognized as a single species, under a new nomenclatural combination. However, given their phenotypic distinction and allopatric distribution, they potentially are a manifestation of an early stage of speciation, and therefore we maintain their subspecific designations

Effects of local habitat variation on the behavioral ecology of two sympatric groups of brown howler monkey (alouatta clamitans)

Although the brown howler monkey (Alouatta clamitans) is a relatively well-studied Neotropical primate, its behavioral and dietary flexibility at the intra-population level remains poorly documented. This study presents data collected on the behavior and ecology of two closely located groups of brown howlers during the same period at the RPPN Feliciano Miguel Abdala in southeastern Brazil. One group occupied a primary valley habitat, henceforth the Valley Group (VG), and the other group occupied a regenerating hillside habitat, the Hill Group (HG). We hypothesized differences in the behavior and ecological parameters between these sympatric groups due to the predicted harsher conditions on the hillside, compared to the valley. We measured several habitat parameters within the home range of both groups and collected data on the activity budget, diet and day range lengths, from August to November 2005, between dawn and dusk. In total, behavioral data were collected for 26 (318 h) and 28 (308 h) sampling days for VG and HG, respectively. As we predicted, HG spent significantly more time feeding and consumed less fruit and more leaves than VG, consistent with our finding that the hillside habitat was of lower quality. However, HG also spent less time resting and more time travelling than VG, suggesting that the monkeys had to expend more time and energy to obtain high-energy foods, such as fruits and flowers that were more widely spaced in their hill habitat. Our results revealed that different locations in this forest vary in quality and raise the question of how different groups secure their home ranges. Fine-grained comparisons such as this are important to prioritize conservation and management areas within a reserve

Ancient DNA of the Pygmy Marmoset Type Specimen \u3cem\u3eCebuella pygmaea\u3c/em\u3e (Spix, 1823) Resolves a Taxonomic Conundrum

The pygmy marmoset, the smallest of the anthropoid primates, has a broad distribution in Western Amazonia. Recent studies using molecular and morphological data have identified two distinct species separated by the Napo and Solimões-Amazonas rivers. However, reconciling this new biological evidence with current taxonomy, i.e., two subspecies, Cebuella pygmaea pygmaea (Spix, 1823) and Cebuella pygmaea niveiventris (Lönnberg, 1940), was problematic given the uncertainty as to whether Spix’s pygmy marmoset (Cebuella pygmaea pygmaea) was collected north or south of the Napo and Solimões-Amazonas rivers, making it unclear to which of the two newly revealed species the name pygmaea would apply. Here, we present the first molecular data from Spix’s type specimen of Cebuella pygmaea, as well as novel mitochondrial genomes from modern pygmy marmosets sampled near the type locality (Tabatinga) on both sides of the river. With these data, we can confirm the correct names of the two species identified, i.e., C. pygmaea for animals north of the Napo and Solimões-Amazonas rivers and C. niveiventris for animals south of these two rivers. Phylogenetic analyses of the novel genetic data placed into the context of cytochrome b gene sequences from across the range of pygmy marmosets further led us to re-evaluate the geographical distribution for the two Cebuella species. We dated the split of these two species to 2.54 million years ago. We discuss additional, more recent, subdivisions within each lineage, as well as potential contact zones between the two species in the headwaters of these rivers

The role of competition in structuring primate communities under different productivity regimes in the Amazon

The factors responsible for the formation of Amazonian primate communities are not well understood. Here we investigated the influence of interspecific competition in the assembly of these communities, specifically whether they follow an assembly rule known as "favored states". According to this rule, interspecific competition influences final species composition, resulting in functional groups that are equally represented in the community.We compiled presence-absence data for primate species at 39 Amazonian sites in Brazil, contrasting two regions with distinct productivity regimes: the eutrophic Juruá River basin and the oligotrophic Negro River basin. We tested two hypotheses: that interspecific competition is a mechanism that influences the structure of Amazonian primate communities, and that competition has had a greater influence on the structure of primate communities in regions with low productivity, where resources are more limited. We used null models to test the statistical significance of the results, and found a non-random pattern compatible with the favored states rule in the two regions. Our findings suggest that interspecific competition is an important force driving primate community assembly regardless of productivity regimes

Medium/Long wavelength sensitive opsin diversity in Pitheciidae

New World primates feature a complex colour vision system. Most species have polymorphic colour vision where males have a dichromatic colour perception and females can be either ichromatic or trichromatic. The adaptive value of high allelic diversity of opsins, a light sensitive protein, found in primates’ eyes remains unknown. Studies revealing the allelic diversity are important as they shed light on our understanding of the adaptive value of differences in the colouration of species and their ecologies. Here we investigate the allelic types found in Pitheciidae, an understudied New World primate family, revealing the diversity of medium/long wavelength sensitive opsins both in cryptic and conspicuous species of this primate family. We found five alleles in Cacajao, six in Callicebinae (i.e. Plecturocebus, Cheracebus, and Callicebus), four in Chiropotes, and three in Pithecia, some of them reported for the first time. Both cryptic and conspicuous species in this group presented high allelic diversity

205 newly assembled mitogenomes provide mixed evidence for rivers as drivers of speciation for Amazonian primates

Mitochondrial DNA remains a cornerstone for molecular ecology, especially for study species from which high-quality tissue samples cannot be easily obtained. Methods using mitochondrial markers are usually reliant on reference databases, but these are often incomplete. Furthermore, available mitochondrial genomes often lack crucial metadata, such as sampling location, limiting their utility for many analyses. Here, we assembled 205 new mitochondrial genomes for platyrrhine primates, most from the Amazon and with known sampling locations. We present a dated mitogenomic phylogeny based on these samples along with additional published platyrrhine mitogenomes, and use this to assess support for the long-standing riverine barrier hypothesis (RBH), which proposes that river formation was a major driver of speciation in Amazonian primates. Along the Amazon, Negro, and Madeira rivers, we found mixed support for the RBH. While we identified divergences that coincide with a river barrier, only some occur synchronously and also overlap with the proposed dates of river formation. The most compelling evidence is for the Amazon river potentially driving speciation within bearded saki monkeys (Chiropotes spp.) and within the smallest extant platyrrhines, the marmosets and tamarins. However, we also found that even large rivers do not appear to be barriers for some primates, including howler monkeys (Alouatta spp.), uakaris (Cacajao spp.), sakis (Pithecia spp.), and robust capuchins (Sapajus spp.). Our results support a more nuanced, clade-specific effect of riverine barriers and suggest that other evolutionary mechanisms, besides the RBH and allopatric speciation, may have played an important role in the diversification of platyrrhines

Barriers to chimpanzee gene flow at the south-east edge of their distribution.

Populations on the edge of a species' distribution may represent an important source of adaptive diversity, yet these populations tend to be more fragmented and are more likely to be geographically isolated. Lack of genetic exchanges between such populations, due to barriers to animal movement, can not only compromise adaptive potential but also lead to the fixation of deleterious alleles. The south-eastern edge of chimpanzee distribution is particularly fragmented, and conflicting hypotheses have been proposed about population connectivity and viability. To address this uncertainty, we generated both mitochondrial and MiSeq-based microsatellite genotypes for 290 individuals ranging across western Tanzania. While shared mitochondrial haplotypes confirmed historical gene flow, our microsatellite analyses revealed two distinct clusters, suggesting two populations currently isolated from one another. However, we found evidence of high levels of gene flow maintained within each of these clusters, one of which covers an 18,000 km2 ecosystem. Landscape genetic analyses confirmed the presence of barriers to gene flow with rivers and bare habitats highly restricting chimpanzee movement. Our study demonstrates how advances in sequencing technologies, combined with the development of landscape genetics approaches, can resolve ambiguities in the genetic history of critical populations and better inform conservation efforts of endangered species