Whole genomes of Amazonian uakari monkeys reveal complex connectivity and fast differentiation driven by high environmental dynamism.

Despite showing the greatest primate diversity on the planet, genomic studies on Amazonian primates show very little representation in the literature. With 48 geolocalized high coverage whole genomes from wild uakari monkeys, we present the first population-level study on platyrrhines using whole genome data. In a very restricted range of the Amazon rainforest, eight uakari species (Cacajao genus) have been described and categorized into the bald and black uakari groups, based on phenotypic and ecological differences. Despite a slight habitat overlap, we show that posterior to their split 0.92 Mya, bald and black uakaris have remained independent, without gene flow. Nowadays, these two groups present distinct genetic diversity and group-specific variation linked to pathogens. We propose differing hydrology patterns and effectiveness of geographic barriers have modulated the intra-group connectivity and structure of bald and black uakari populations. With this work we have explored the effects of the Amazon rainforest's dynamism on wild primates' genetics and increased the representation of platyrrhine genomes, thus opening the door to future research on the complexity and diversity of primate genomics.

Identification of constrained sequence elements across 239 primate genomes.

Noncoding DNA is central to our understanding of human gene regulation and complex diseases1,2, and measuring the evolutionary sequence constraint can establish the functional relevance of putative regulatory elements in the human genome3-9. Identifying the genomic elements that have become constrained specifically in primates has been hampered by the faster evolution of noncoding DNA compared to protein-coding DNA10, the relatively short timescales separating primate species11, and the previously limited availability of whole-genome sequences12. Here we construct a whole-genome alignment of 239 species, representing nearly half of all extant species in the primate order. Using this resource, we identified human regulatory elements that are under selective constraint across primates and other mammals at a 5% false discovery rate. We detected 111,318 DNase I hypersensitivity sites and 267,410 transcription factor binding sites that are constrained specifically in primates but not across other placental mammals and validate their cis-regulatory effects on gene expression. These regulatory elements are enriched for human genetic variants that affect gene expression and complex traits and diseases. Our results highlight the important role of recent evolution in regulatory sequence elements differentiating primates, including humans, from other placental mammals.

A global catalog of whole-genome diversity from 233 primate species.

The rich diversity of morphology and behavior displayed across primate species provides an informative context in which to study the impact of genomic diversity on fundamental biological processes. Analysis of that diversity provides insight into long-standing questions in evolutionary and conservation biology and is urgent given severe threats these species are facing. Here, we present high-coverage whole-genome data from 233 primate species representing 86% of genera and all 16 families. This dataset was used, together with fossil calibration, to create a nuclear DNA phylogeny and to reassess evolutionary divergence times among primate clades. We found within-species genetic diversity across families and geographic regions to be associated with climate and sociality, but not with extinction risk. Furthermore, mutation rates differ across species, potentially influenced by effective population sizes. Lastly, we identified extensive recurrence of missense mutations previously thought to be human specific. This study will open a wide range of research avenues for future primate genomic research.

The landscape of tolerated genetic variation in humans and primates.

Personalized genome sequencing has revealed millions of genetic differences between individuals, but our understanding of their clinical relevance remains largely incomplete. To systematically decipher the effects of human genetic variants, we obtained whole-genome sequencing data for 809 individuals from 233 primate species and identified 4.3 million common protein-altering variants with orthologs in humans. We show that these variants can be inferred to have nondeleterious effects in humans based on their presence at high allele frequencies in other primate populations. We use this resource to classify 6% of all possible human protein-altering variants as likely benign and impute the pathogenicity of the remaining 94% of variants with deep learning, achieving state-of-the-art accuracy for diagnosing pathogenic variants in patients with genetic diseases.

The landscape of tolerated genetic variation in humans and primates.

Personalized genome sequencing has revealed millions of genetic differences between individuals, but our understanding of their clinical relevance remains largely incomplete. To systematically decipher the effects of human genetic variants, we obtained whole genome sequencing data for 809 individuals from 233 primate species, and identified 4.3 million common protein-altering variants with orthologs in human. We show that these variants can be inferred to have non-deleterious effects in human based on their presence at high allele frequencies in other primate populations. We use this resource to classify 6% of all possible human protein-altering variants as likely benign and impute the pathogenicity of the remaining 94% of variants with deep learning, achieving state-of-the-art accuracy for diagnosing pathogenic variants in patients with genetic diseases. One Sentence Summary: Deep learning classifier trained on 4.3 million common primate missense variants predicts variant pathogenicity in humans.

Male genital organs of the black-crowned dwarf marmoset (Callibella humilis).

This study provides the first morphological description of the male genital organs of black-crowned dwarf marmoset (Callibella humilis). Internal and external genital organs were similar to other species of non-human primates. However, some shape and size differences were noted. The penile shaft was laterally flattened and comprised of two corpus cavernosus. These were split by a septum up to the level of the glans and then merged to form a single structure. The glans penis had small, keratinized spicules arising from epidermal or dermal projections. The small, fully ossified and well-mineralized penile bone, located at the distal end of the penis, consisted of a bone matrix surrounded by sparse osteoblasts and well-developed internal osteocytes. The penile urethra was lined with columnar pseudostratified epithelium, with areas of simple cuboidal epithelium. The testes were small relative to the body compared to other primate species. The findings of this work may support comparative studies of primate reproductive ecology.

Morphological description of male genital organs of Marca's marmoset (Mico marcai).

Morphological characterisation of the genital organs of primates may bring significant contributions to the understanding of different reproductive behaviours and support new conservation strategies. However, relevant or detailed descriptions of genital morphology of several primate species are still lacking. This study describes the gross and microscopic anatomy of the internal and external genitalia of Marca's marmoset (Mico marcai). The same organs described in other primate species were identified here, but some anatomical particularities were detected, such as absence of a dartos tunic, presence of a vas deferens ampulla, absence of spongious erectile tissue in the pelvic urethra, separation of prostate gland lobes by a longitudinal sulcus and lack of septation in the corpus cavernosus and spongiosus at the level of the shaft and free portion of the penis. Keratinised type 1 spicules arising from epidermal or dermal projections were found in the free portion of the penis. Microscopic analysis revealed a small bone (baculum) consisting of peripheral compact bone and a central, non-ossified area filled with vascular tissue at the distal end of this portion of the penis. Results of this study may support further comparative studies of primates' reproductive ecology.

New insights into the distribution and conservation status of the Golden-White Tassel-Ear Marmoset Mico chrysoleucos (Primates, Callitrichidae).

Among the 13 Mico species recognized by the IUCN Red List of Threatened Species, six are listed as "Data Deficient". The geographic range of most of the Mico species has been estimated from only a few records. We report new localities and the geographic extension of Mico chrysoleucos. In addition, we confirmed the presence of the species in two distinct protected areas. We modeled the habitat suitability of M. chrysoleucos using the maximum entropy method and including new records obtained by the authors in the state of Amazonas, Brazil. From the total area of occurrence calculated for the species, 22.8% is covered by protected areas and indigenous lands. The annual mean deforestation rate estimated between 2000 and 2015 was 2.95%, and the total area deforested by 2015 was 3354 km2 or 8.6% of the total distribution limits of the species. The habitat lost between 2000 and 2015 was 3.2% (1131 km2) of the total potential distribution, while the habitat loss area legally protected was 31 km2, and the habitat loss in settlements was equal to 691 km2. Our results extend the geographic distribution of the species about 100 km farther south, with the Maracanã River being a possible geographic barrier for the species. The significantly low rate of habitat loss inside protected areas and indigenous land, when compared to unprotected areas, points out the importance of these areas to M. chrysoleucos conservation. The species is relatively wide-ranging, legally protected, and resilient to regional anthropic threats. However, the hydroelectric schemes and the improvement of the road system in southern Amazonia pose an imminent threat to the species.

Geographic comparison of plant genera used in frugivory among the pitheciids Cacajao, Callicebus, Chiropotes, and Pithecia.

Pitheciids are known for their frugivorous diets, but there has been no broad-scale comparison of fruit genera used by these primates that range across five geographic regions in South America. We compiled 31 fruit lists from data collected from 18 species (three Cacajao, six Callicebus, five Chiropotes, and four Pithecia) at 26 study sites in six countries. Together, these lists contained 455 plant genera from 96 families. We predicted that 1) closely related Chiropotes and Cacajao would demonstrate the greatest similarity in fruit lists; 2) pitheciids living in closer geographic proximity would have greater similarities in fruit lists; and 3) fruit genus richness would be lower in lists from forest fragments than continuous forests. Fruit genus richness was greatest for the composite Chiropotes list, even though Pithecia had the greatest overall sampling effort. We also found that the Callicebus composite fruit list had lower similarity scores in comparison with the composite food lists of the other three genera (both within and between geographic areas). Chiropotes and Pithecia showed strongest similarities in fruit lists, followed by sister taxa Chiropotes and Cacajao. Overall, pitheciids in closer proximity had more similarities in their fruit list, and this pattern was evident in the fruit lists for both Callicebus and Chiropotes. There was no difference in the number of fruit genera used by pitheciids in habitat fragments and continuous forest. Our findings demonstrate that pitheciids use a variety of fruit genera, but phylogenetic and geographic patterns in fruit use are not consistent across all pitheciid genera. This study represents the most extensive examination of pitheciid fruit consumption to date, but future research is needed to investigate the extent to which the trends in fruit genus richness noted here are attributable to habitat differences among study sites, differences in feeding ecology, or a combination of both.

Extension of the geographic range of Ateles chamek (Primates, Atelidae): evidence of river-barrier crossing by an amazonian primate.

The black-faced black spider monkey (Ateles chamek) is endangered because of hunting and habitat loss. There are many gaps in our understanding of its geographic distribution. The Ucayali-Solimões-Amazon fluvial complex is currently recognized as the northern boundary of the species' range, although published reports have indicated that it occurs north of the Rio Solimões. In this study we investigate published records, generate new field records, and assess the current information concerning the northern boundary of this species' range. We conducted the study at the Mamirauá Sustainable Development Reserve in the central Brazilian Amazon, an area of 1,124,000 ha that consists entirely of Amazonian flooded forest (várzea). We collected data on the occurrence of the species from museum specimens and through field surveys, including interviews with local residents, direct observations, and the collection of new museum specimens. We confirmed the presence of A. chamek at 17 locations in the reserve, one of which was an island formed by a river bend cut-off that would have effectively taken any resident spider to the (new) north bank of the Solimões. We therefore conclude that fluvial dynamics were involved in creating the conditions for the dispersal and colonization of the species on the northern bank of the Rio Solimões. The data we present extends the known distribution of the species and increases its representation in protected areas.

Evaluation of the fecal steroid concentrations in Alouatta belzebul (Primates, Atelidae) in the National Forest of Tapirape-Aquiri in Pará, Brazil.

BACKGROUND: The studies on fecal steroid metabolites published with free-living primates are limited mainly by the difficulty in obtaining samples. METHODS: A radioimmunoassay was used to measure the fecal steroid concentrations in Alouatta belzebul in the National Forest of Tapirape-Aquiri in Brazil. RESULTS AND CONCLUSIONS: Androgens were significantly higher for the adult males from the Area of Influence (AI-I group) when compared to those from the Control Area (CA group) (P < 0.05). Progestin and estrogen concentrations were higher in the females from the CA group than in those from the AI-I for both the adult females and females with offspring; however, P < 0.05 was only observed in the concentrations of fecal progestins from the adult females. The physiological differences between the AI-I and CA groups suggest that the cause was a sum of factors, such as an exposure to sound waves, feeding habits, daily activity patterns, and the habituation of the animals.