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Abstract Although recent advances in genomics have enabled the high-resolution study of whole genomes, our understanding of one of the key evolutionary processes, mutation, still remains limited. In primates specifically, studies have largely focused on humans and their closest evolutionary relatives, the great apes, as well as a handful of species of biomedical or conservation interest. Yet, as mutation rates vary across genomic regions, individuals, and species, a greater understanding of the underlying evolutionary dynamics at play will ultimately be illuminated by not only additional sampling across the order but also by a greater depth of sampling within species. To address these needs, we here present the first population-scale genomic resources for the coppery titi monkey (Plecturocebus cupreus)—a platyrrhine of considerable biomedical interest for both social behavior and neurobiology. Deep whole-genome sequencing of 15 parent–offspring trios, together with a computational de novo mutation detection pipeline based on pan-genome graphs, has provided a detailed picture of the sex-averaged mutation rate—0.63 × 10−8 (95% CI: 0.43 × 10−8–0.90 × 10−8) per site per generation—as well as the effects of both sex and parental age on underlying rates, demonstrating a significant paternal age effect. Coppery titi monkey males exhibit long reproductive lifespans, afforded by long-term pair bonding in the species' monogamous mating system, and our results have demonstrated that individuals reproducing later in life exhibit one of the strongest male mutation biases observed in any non-human primate studied to date. Taken together, this study thus provides an important piece of the puzzle for better comprehending the mutational landscape across primates.

We examined photic and ecological factors related to initiation of feeding by four sympatric primates in the rain forest of Amazonian Ecuador. With rare exceptions, morning activities of all taxa began only after the onset of nautical twilight, which occurred 47-48 min before sunrise. The larger spider and woolly monkeys, Ateles belzebuth and Lagothrix lagotricha poeppigii, left their sleeping trees before sunrise about half the time, while the smaller sakis and titi monkeys, Pithecia aequatorialis and Plecturocebus (formerly Callicebus) discolor, did not emerge until sunrise or later. None of the four taxa routinely began feeding before sunrise. Pithecia began feeding a median 2.17 h after sunrise, at least 0.8 h later than the median feeding times of the other three taxa. The early movement of Ateles and Lagothrix, and late initiation of feeding by Pithecia are consistent with temporal niche partitioning. Among most New World primate species, all males and many females, have dichromatic color vision, with only two cone photopigments, while some females are trichromats with three cone photopigments. Current evidence indicates that the dichromats have a foraging advantage in dim light, which could facilitate utilization of twilight periods and contribute to temporal niche partitioning. However, in our study, dichromatic males did not differentially exploit the dim light of twilight, and times of first feeding bouts of female Ateles and Lagothrix were similar to those of males. First feeding bouts followed a seasonal pattern, occurring latest in May-August, when ripe fruit abundance and ambient temperature were both relatively low. The most frugivorous taxon, Ateles, exhibited the greatest seasonality, initiating feeding 1.4 h later in May-August than in January-April. This pattern may imply a strategy of conserving energy when ripe fruit is scarcer, but starting earlier to compete successfully when fruit is more abundant. Lower temperatures were associated with later feeding of Ateles (by 26 min / °C) and perhaps Pithecia, but not Lagothrix or Plecturocebus. The potential for modification of temporal activity patterns and temporal niche partitioning by relatively small changes in temperature should be considered when predicting the effects of climate change.

Primates play an important role in ecosystem functioning and offer critical insights into human evolution, biology, behavior, and emerging infectious diseases. There are 26 primate species in the Atlantic Forests of South America, 19 of them endemic. We compiled a dataset of 5,472 georeferenced locations of 26 native and 1 introduced primate species, as hybrids in the genera Callithrix and Alouatta. The dataset includes 700 primate communities, 8,121 single species occurrences and 714 estimates of primate population sizes, covering most natural forest types of the tropical and subtropical Atlantic Forest of Brazil, Paraguay and Argentina and some other biomes. On average, primate communities of the Atlantic Forest harbor 2 ± 1 species (range = 1–6). However, about 40% of primate communities contain only one species. Alouatta guariba (N = 2,188 records) and Sapajus nigritus (N = 1,127) were the species with the most records. Callicebus barbarabrownae (N = 35), Leontopithecus caissara (N = 38), and Sapajus libidinosus (N = 41) were the species with the least records. Recorded primate densities varied from 0.004 individuals/km² (Alouatta guariba at Fragmento do Bugre, Paraná, Brazil) to 400 individuals/km² (Alouatta caraya in Santiago, Rio Grande do Sul, Brazil). Our dataset reflects disparity between the numerous primate census conducted in the Atlantic Forest, in contrast to the scarcity of estimates of population sizes and densities. With these data, researchers can develop different macroecological and regional level studies, focusing on communities, populations, species co-occurrence and distribution patterns. Moreover, the data can also be used to assess the consequences of fragmentation, defaunation, and disease outbreaks on different ecological processes, such as trophic cascades, species invasion or extinction, and community dynamics. There are no copyright restrictions. Please cite this Data Paper when the data are used in publications. We also request that researchers and teachers inform us of how they are using the data.

Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris (Cacajao) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari, C. calvus, by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.

There have been recent disagreements as to how many taxa of titi monkeys, genus Callicebus , occur in the region between the Purus and Madeira rivers in western Brazilian Amazonia. Three parapatric taxa were proposed for the area: Callicebus caligatus , Callicebus stephennashi , and Callicebus dubius , but the latter has recently been considered a synonym of C. caligatus , even though both form monophyletic groups and are morphologically distinct. We analyzed the geographic variation in the pelage of Callicebus occurring between the Madeira and Purus rivers and concluded that the phenotypes attributed to C. caligatus and C. dubius are not individual morphs, but rather well-marked and geographically restricted varieties. For this reason, we classify Callicebus caligatus as a polytypic species with two subspecies: Callicebus caligatus caligatus and Callicebus caligatus dubius . This classification is corroborated by molecular evidence as well. The morphological and distributional data indicate that Callicebus stephennashi is a hybrid form of C. c. caligatus and C. c. dubius , due to the presence of intermediate characters. Therefore, until more precise locality records are provided and further evidence is presented, we consider Callicebus stephennashi to be a homonym of the two parental forms.

There is little systematic assessment of how total health expenditure is distributed across diseases and comorbidities. The objective of this study was to use statistical methods to disaggregate all publicly funded health expenditure by disease and comorbidities in order to answer three research questions: (1) What is health expenditure by disease phase for noncommunicable diseases (NCDs) in New Zealand? (2) Is the cost of having two NCDs more or less than that expected given the independent costs of each NCD? (3) How is total health spending disaggregated by NCDs across age and by sex? We used linked data for all adult New Zealanders for publicly funded events, including hospitalisation, outpatient, pharmaceutical, laboratory testing, and primary care from 1 July 2007 to 30 June 2014. These data include 18.9 million person-years and $26.4 billion in spending (US$ 2016). We used case definition algorithms to identify if a person had any of six NCDs (cancer, cardiovascular disease [CVD], diabetes, musculoskeletal, neurological, and a chronic lung/liver/kidney [LLK] disease). Indicator variables were used to identify the presence of any of the 15 possible comorbidity pairings of these six NCDs. Regression was used to estimate excess annual health expenditure per person. Cause deletion methods were used to estimate total population expenditure by disease. A majority (59%) of health expenditure was attributable to NCDs. Expenditure due to diseases was generally highest in the year of diagnosis and year of death. A person having two diseases simultaneously generally had greater health expenditure than the expected sum of having the diseases separately, for all 15 comorbidity pairs except the CVD-cancer pair. For example, a 60-64-year-old female with none of the six NCDs had $633 per annum expenditure. If she had both CVD and chronic LLK, additional expenditure for CVD separately was $6,443/$839/$9,225 for the first year of diagnosis/prevalent years/last year of life if dying of CVD; additional expenditure for chronic LLK separately was $6,443/$1,291/$9,051; and the additional comorbidity expenditure of having both CVD and LLK was $2,456 (95% confidence interval [CI] $2,238-$2,674). The pattern was similar for males (e.g., additional comorbidity expenditure for a 60-64-year-old male with CVD and chronic LLK was $2,498 [95% CI $2,264-$2,632]). In addition to this, the excess comorbidity costs for a person with two diseases was greater at younger ages, e.g., excess expenditure for 45-49-year-old males with CVD and chronic LLK was 10 times higher than for 75-79-year-old males and six times higher for females. At the population level, 23.8% of total health expenditure was attributable to higher costs of having one of the 15 comorbidity pairs over and above the six NCDs separately; of the remaining expenditure, CVD accounted for 18.7%, followed by musculoskeletal (16.2%), neurological (14.4%), cancer (14.1%), chronic LLK disease (7.4%), and diabetes (5.5%). Major limitations included incomplete linkage to all costed events (although these were largely non-NCD events) and missing private expenditure. The costs of having two NCDs simultaneously is typically superadditive, and more so for younger adults. Neurological and musculoskeletal diseases contributed the largest health system costs, in accord with burden of disease studies finding that they contribute large morbidity. Just as burden of disease methodology has advanced the understanding of disease burden, there is a need to create disease-based costing studies that facilitate the disaggregation of health budgets at a national level.

Urban expansion is a global driver of wildlife decline, with cities encroaching into forested areas, leading among other things to habitat loss and fragmentation. This can result in remnant forest patches becoming isolated within anthropogenic mosaics, trapping wildlife unable to move beyond the urban areas. The city of Moyobamba, capital of Peru’s San Martin region, population has increased rapidly since 1970 and is currently estimated at ~ 90,000 people. Moyobamba’s urban forest patches are home to the endemic and Critically Endangered San Martin titi monkey ( Plecturocebus oenanthe ). We conducted an 18-month survey of primates in 23 urban forest patches to determine the presence of P. oenanthe , evaluate the patch-specific variables influencing its presence, and estimate its population size and density in the remaining green areas of Moyobamba city. Plecturocebus oenanthe was present in 17 patches and was never detected outside of patches. Using triangulation we estimate 26 groups of P. oenanthe in Moyobamba, with an average occupied-patch density of 26.9/km 2 . The number of groups per patch was positively correlated with patch area ( p  = 0.023) and distance between patches ( p  = 0.0004), whereas presence and density were not correlated with any other landscape metrics, patch size, or habitat structure. Our results demonstrate that urban forests can support important populations of primates, particularly endemic and threatened species. Therefore, remnant forest patches and green corridors should be prioritized in urban planning strategies to ensure long-term wildlife persistence in rapidly developing landscapes.

All primate species produce vocalizations for complex communication, conveying a wide range of information, regulating social interactions, coordinating activities, and serving as antipredator strategies. Together, these vocalizations form a species' vocal repertoire. However, despite their widespread presence and ecological significance, the vocal repertoires of less than 15% of primate taxa have been documented to date. The purpose of this study was to quantitatively characterize the vocal repertoire and behavior of a wild population of Ucayali bald or red uakaris ( Cacajao ucayalii ), a rare Amazonian platyrrhine primate. We analyzed and categorized 1,155 red uakari vocalizations using a combination of machine-learning-based random forest analyses, bioacoustic analysis, and field observations. We identified and described 12 acoustically distinct call types, two of which were not previously reported ( High-chick and Shriek ). The Hic was the most common vocalization, both in context and frequency of use. Some calls were specific to age, sex, or context, while others occurred across a range of situations. The vocal repertoire exhibited properties of both graded and discrete calls, depending on the call type and its apparent function. The uakaris’ tail plays a key role in the species’ acoustic-visual multimodal communication, as evidenced by the frequent combination of different call types and tail wagging, probably to draw attention from other group members and emphasize the transmission of information. The bioacoustic characterization of the Ucayali bald uakari's vocal repertoire provides a groundwork for potential acoustic monitoring of this species and the potential use of uakari monkeys as models for studying multimodal communication in primates.

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 dichromatic 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.

Deforestation and fragmentation of tropical rainforests are increasingly creating forest edges and corresponding edge effects. Furthermore, primary forest is increasingly being replaced by secondary forest. The presence of high population densities of titi monkeys in fragmented and secondary forests suggests that they are capable of adapting to such habitat alterations. The aim of our study was to examine the ability of the red titi monkey ( Callicebus cupreus ) to adapt to forest edges and secondary forest. We compared home-range use, activity budgets, and diet composition in two groups of monkeys: one in primary forest and the other in primary forest with a long edge bordering secondary forest. The latter group avoided the secondary forest and used the edge in proportion to its availability. Groups did not differ in activity budgets but did show slight differences in diet composition. Taken together, our results suggest that there are no major effects of forest edges and secondary forest on red titi monkeys; however, given the relatively short study period, generalizations should be avoided until more comparative data become available. Furthermore, the age or successional stage of the secondary forest must be taken into consideration when drawing conclusions about its suitability as a primate habitat.