Intergroup encounters in pair-living primates: Comparative analysis and a case study of pair-living and monogamous owl monkeys (Aotus azarae) of Argentina.

The function of intergroup encounters (IGEs) may differ substantially among species of different group sizes and social organizations. Research in group-living primates has shown that the behavioral responses during IGEs can vary widely from affiliative to neutral or aggressive interactions; still, little is known about IGEs in pair-living taxa. We conducted a systematic literature review to find relevant studies on the functions of IGEs in pair-living nonhuman primates that could inform analyses of IGE data (n = 242 IGEs, 21 groups and 10 solitary individuals, 1997-2020) from wild owl monkeys, a pair-living, monogamous primate with extensive biparental care. We identified 1315 studies published between 1965 and 2021; only 13 of them (n = 10 species) contained raw data on the number of IGEs. Our review of those studies showed that IGEs are common, but highly variable in their nature and characteristics in pair-living primates. To examine the non-mutually exclusive hypotheses of resource-, and mate defense, and infanticide avoidance we analyzed data from the Owl Monkey Project 27-year long database to build first an a priori model set. To incorporate prior knowledge from the literature review, we conducted our analyses as a consecutive series of binomial logistic regressions. All IGEs including all biologically relevant parameters (N = 156) were codified into three different behavioral categories (Reaction, Agonism, and Physical Aggression). The analysis showed that owl monkeys regularly engaged in IGEs, most of which were agonistic. They showed more reaction when infants were present, but reactions were less physically aggressive when infants and pregnant females were involved. Overall, our results lend more support for the infant and mate defense hypotheses than they do for the resource defense one.

Gastrointestinal tract pathology of the owl monkey (Aotus spp.).

Owl monkeys are small nocturnal new world primates in the genus Aotus that are most used in biomedical research for malaria. Cardiomyopathy and nephropathy are well-described common diseases contributing to their morbidity and mortality; less is known about lesions affecting the gastrointestinal tract. Records from a 14-year period (2008-2022) at the Keeling Center for Comparative Medicine and Research were queried to identify instances of spontaneous gastrointestinal disease that directly contributed to the cause of death from the 235 adult owl monkeys submitted for necropsy. Of the 235, 10.6% (25/235) had gastrointestinal disease listed as a significant factor that contributed to morbidity and mortality. Diagnoses included candidiasis (3/25), gastric bloat (4/25), and intestinal incarceration and ischemia secondary (11/25), which included intussusception (4/25), mesenteric rent (3/25), strangulating lipoma (2/25), intestinal torsion (1/25), and an inguinal hernia (1/25). Intestinal adenocarcinomas affecting the jejunum (4/25) were the most common neoplasia diagnosis. Oral squamous cell carcinoma (1/25) and intestinal lymphoma (2/25) were also diagnosed. This report provides evidence of spontaneous lesions in the species that contribute to morbidity and mortality.

Growth and microanatomy of the paranasal sinuses in two species of New World monkeys.

Paranasal sinuses of living apes and humans grow with positive allometry, suggesting a novel mechanism for bone enlargement. Here, we examine the paranasal sinuses of the owl monkey (Aotus spp.) and a tamarin (Saguinus midas) across postnatal development. The prediction that paranasal sinuses grow disproportionately faster than the main nasal chamber is tested. We used diffusible iodine-based contrast-enhanced computed tomography and histology to study sinuses in eight Aotus and three tamarins ranging from newborn to adult ages. Sinuses were segmented at the mucosa-air cavity interface and measured in volume. All sinuses were lined by a ciliated respiratory epithelium, except for the ethmoid air cells in Aotus, which are lined in part by olfactory epithelium. An age comparison indicates that only the maxillary sinus and ethmoid air cells are present in newborns, and two additional sinuses (invading the orbitosphenoid and the frontal bone), do not appear until late infancy or later. Comparing newborns and adults, the main nasal airway is 10 times larger in the adult Aotus and ~ 6.5 times larger in adult Saguinus. In contrast, the maxillary sinus far exceeds this magnitude of difference: 24 times larger in the adult Aotus and 46 times larger in adult Saguinus. The frontal sinuses add significantly to total paranasal space volume in both species, but this growth is likely delayed until juvenile age. Results suggest ethmoid air cells expand the least. These results support our prediction that most paranasal sinuses have a distinctly higher growth rate compared to the main nasal chamber.

Sterile protection against P. vivax malaria by repeated blood stage infection in the Aotus monkey model.

The malaria parasite Plasmodium vivax remains a major global public health challenge, and no vaccine is approved for use in humans. Here, we assessed whether P. vivax strain-transcendent immunity can be achieved by repeated infection in Aotus monkeys. Sterile immunity was achieved after two homologous infections, whereas subsequent heterologous challenge provided only partial protection. IgG levels based on P. vivax lysate ELISA and protein microarray increased with repeated infections and correlated with the level of homologous protection. Parasite transcriptional profiles provided no evidence of major antigenic switching upon homologous or heterologous challenge. However, we observed significant sequence diversity and transcriptional differences in the P. vivax core gene repertoire between the two strains used in the study, suggesting that partial protection upon heterologous challenge is due to molecular differences between strains rather than immune evasion by antigenic switching. Our study demonstrates that sterile immunity against P. vivax can be achieved by repeated homologous blood stage infection in Aotus monkeys, thus providing a benchmark to test the efficacy of candidate blood stage P. vivax malaria vaccines.

Molecular data aids pinworm diagnosis in night monkeys (Aotus spp., Primates: Aotidae) with the resurrection of a Trypanoxyuris species (Nematoda: Oxyuridae).

Neotropical primates (Platyrrhines) are commonly parasitized by pinworm nematodes of the genus Trypanoxyuris Vevers, 1923. The taxonomic identity of Trypanoxyuris sampled in night monkeys (Aotus Iliger) has been rather controversial. Two species have been described, namely T. microon (Linstow, 1907) and T. interlabiata (Sandosham, 1950). The latter was synonymized with T. microon considering that the observed morphological differences corresponded to different developmental stages of the nematode rather than to differences between both species. Here, we used an integrative taxonomy approach, based on morphological and molecular data along with host identity, in order to assess the validity of both species. Our results evidenced that these different morphotypes correspond to different and reciprocally monophyletic groups; thus, we propose the resurrection of T. interlabiata. We redescribe both pinworm species using specimens sampled in Aotus monkeys from Colombia and discuss the advantages of combining molecular and morphological data to uncover pinworm diversity, and to understand the potential forces determining the diversification process in pinworms from platyrrhine primates.

Aotus nancymaae model predicts human immune response to the placental malaria vaccine candidate VAR2CSA.

Placental malaria vaccines (PMVs) are being developed to prevent severe sequelae of placental malaria (PM) in pregnant women and their offspring. The leading candidate vaccine antigen VAR2CSA mediates parasite binding to placental receptor chondroitin sulfate A (CSA). Despite promising results in small animal studies, recent human trials of the first two PMV candidates (PAMVAC and PRIMVAC) generated limited cross-reactivity and cross-inhibitory activity to heterologous parasites. Here we immunized Aotus nancymaae monkeys with three PMV candidates (PAMVAC, PRIMVAC and ID1-ID2a_M1010) adjuvanted with Alhydrogel, and exploited the model to investigate boosting of functional vaccine responses during PM episodes as well as with nanoparticle antigens. PMV candidates induced high levels of antigen-specific IgG with significant cross-reactivity across PMV antigens by enzyme-linked immunosorbent assay. Conversely, PMV antibodies recognized native VAR2CSA and blocked CSA adhesion of only homologous parasites and not of heterologous parasites. PM episodes did not significantly boost VAR2CSA antibody levels or serum functional activity; nanoparticle and monomer antigens alike boosted serum reactivity but not functional activities. Overall, PMV candidates induced functional antibodies with limited heterologous activity in Aotus monkeys, similar to responses reported in humans. The Aotus model appears suitable for preclinical downselection of PMV candidates and assessment of antibody boosting by PM episodes.

The importance of auditory, olfactory, and visual cues for insect foraging in owl monkeys (Aotus nancymaae).

Nocturnal mammals have unique sensory adaptations to facilitate foraging at night. Owl monkeys (Aotus spp.) are pair-living nocturnal platyrrhines adept at capturing insect prey under low-light conditions. Owl monkeys use acoustic and chemical cues in intraspecific communication and use olfaction to detect fruit as they forage. We conducted an experiment to determine which cues (auditory, olfactory, and visual) Aotus nancymaae rely upon when foraging for insects. We scored the behavior of 23 captive owl monkeys during a series of trials in which monkeys were provided sensory boxes with insect cues either present (experimental box) or absent (control box). Each cue was tested alone and in combination with all other cues (multimodal cues). We used generalized linear mixed models to determine which cues elicited the greatest behavioral response. Owl monkeys approached and spent more time near experimental boxes than control boxes. Male owl monkeys were quicker than their female partners to approach the sensory boxes, suggesting that males may be less neophobic than females. The owl monkeys exhibited behaviors associated with olfaction and foraging (e.g., sneezing, trilling) during trials with multimodal cues and when only olfactory cues were present. When only visual or auditory cues were present, owl monkeys exhibited fewer foraging-related behaviors. After approaching a sensory box, however, they often touched boxes containing visual cues. A. nancymaae may rely on olfactory cues at night to detect a food source from several meters away and then rely more on visual cues once they are closer to the food source. Their use of sensory cues during insect foraging differs from nocturnal strepsirrhines, possibly reflecting physiological constraints associated with phylogeny, given that owl monkeys evolved nocturnality secondarily from a more recent diurnal ancestor.

SELECTED OPHTHALMIC TESTS AND OCULAR DIMENSIONS IN RELATION TO ACTIVITY PATTERN IN THREE NEOTROPICAL NONHUMAN PRIMATES: BLACK-TUFTED MARMOSET (CALLITHRIX PENICILLATA), GUIANAN SQUIRREL MONKEY (SAIMIRI SCIUREUS), AND AZARA'S NIGHT MONKEY (AOTUS AZARAE INFULATUS).

The goals of this study were to compare ocular morphology, determine the reference intervals of selected ophthalmic tests, ocular measurements, intraocular pressure, and tear production, and to establish possible relationships in the visual ecology of three different Neotropical nonhuman primates (NHP). Nineteen black-tufted marmosets (Callithrix penicillate), 24 Guianan squirrel monkeys (Saimiri sciureus), and 24 night monkeys (Aotus azarae infulatus) were included in the study. Schirmer tear test, ocular dimensions, ocular ultrasonography, intraocular pressure, central corneal thickness, and corneal touch threshold were determined. The ratio of the average corneal diameters and axial diameters (CD/AGL) were established. No significant difference was noted between males and females, nor left and right eyes, for all three species for all measurements (P > 0.05). CD/AGL ratio was significantly higher (P < 0.0001) in night monkeys (a nocturnal species) as compared to black-tufted marmoset and Guianan squirrel monkeys (two diurnal species). The reference intervals will aid veterinary ophthalmologists to more accurately diagnose pathological changes in the eyes of these species. In addition, ocular dimension comparison will allow other NHP species to be evaluated and examined in relationship to behavioral traits (nocturnal versus diurnal).

Adiponectin levels in captive Owl Monkeys (Aotus sp.).

The mean serum value of adiponectin in captive Aotus sp. is 541.99 ng/mL ± 73.05. There is no influence of sex or age, but there is a moderate positive correlation between body weight and adiponectin levels in males.

Cuterebra baeri Infecting Grey-Legged Night Monkeys (Aotus griseimembra) and Red Howler Monkeys (Alouatta seniculus) in Colombia.

Myiases are parasitic infections caused by the larval stages of some fly species. In American nonhuman primates (NHP), three bot fly species causing cutaneous myiasis have been reported: Cuterebra baeri, Cochliomyia hominivorax, and Dermatobia hominis. Studies on myiasis in NHP are scarce and mainly based on morphologic identification of larvae, while molecular approaches have been barely used. This study aimed to molecularly identify bot flies parasitizing two NHP species living sympatrically in central Colombia. Bot fly larvae were collected from two grey-legged night monkeys (Aotus griseimembra) and from a howler monkey (Alouatta seniculus). Larvae were measured and photographed for morphologic evaluation; subsequent molecular characterizations of a partial region of the cytochrome c oxidase subunit 1 mitochondrial gene were performed. Sequence analysis allowed the identification of all specimens as Cuterebra baeri, enabling confirmation of this species parasitizing Alouatta seniculus and Aotus griseimembra in Colombia.

Framework of the Alu Subfamily Evolution in the Platyrrhine Three-Family Clade of Cebidae, Callithrichidae, and Aotidae.

The history of Alu retroposons has been choreographed by the systematic accumulation of inherited diagnostic nucleotide substitutions to form discrete subfamilies, each having a distinct nucleotide consensus sequence. The oldest subfamily, AluJ, gave rise to AluS after the split between Strepsirrhini and what would become Catarrhini and Platyrrhini. The AluS lineage gave rise to AluY in catarrhines and to AluTa in platyrrhines. Platyrrhine Alu subfamilies Ta7, Ta10, and Ta15 were assigned names based on a standardized nomenclature. However, with the subsequent intensification of whole genome sequencing (WGS), large scale analyses to characterize Alu subfamilies using the program COSEG identified entire lineages of subfamilies simultaneously. The first platyrrhine genome with WGS, the common marmoset (Callithrix jacchus; [caljac3]), resulted in Alu subfamily names sf0 to sf94 in an arbitrary order. Although easily resolved by alignment of the consensus sequences, this naming convention can become increasingly confusing as more genomes are independently analyzed. In this study, we reported Alu subfamily characterization for the platyrrhine three-family clade of Cebidae, Callithrichidae, and Aotidae. We investigated one species/genome from each recognized family of Callithrichidae and Aotidae and of both subfamilies (Cebinae and Saimiriinae) of the family Cebidae. Furthermore, we constructed a comprehensive network of Alu subfamily evolution within the three-family clade of platyrrhines to provide a working framework for future research. Alu expansion in the three-family clade has been dominated by AluTa15 and its derivatives.

Asymmetric dimethyl arginine in captive owl monkeys (Aotus sp).

Only four of 40 animals had measurable asymmetric dimethyl arginine (ADMA) levels. The young primate had the lowest value (53.4 ng/ml) when compared with the two adults (218.8 ± 9.3 ng/ml) and the elderly one (320.5 ng/ml). The ADMA levels in this study may relate to the echocardiographic abnormalities found, and possible hypertensive individuals.

Cortical adaptation of the night monkey to a nocturnal niche environment: a comparative non-invasive T1w/T2w myelin study.

Night monkeys (Aotus) are the only genus of monkeys within the Simian lineage that successfully occupy a nocturnal environmental niche. Their behavior is supported by their sensory organs' distinctive morphological features; however, little is known about their evolutionary adaptations in sensory regions of the cerebral cortex. Here, we investigate this question by exploring the cortical organization of night monkeys using high-resolution in-vivo brain MRI and comparative cortical-surface T1w/T2w myeloarchitectonic mapping. Our results show that the night monkey cerebral cortex has a qualitatively similar but quantitatively different pattern of cortical myelin compared to the diurnal macaque and marmoset monkeys. T1w/T2w myelin and its gradient allowed us to parcellate high myelin areas, including the middle temporal complex (MT +) and auditory cortex, and a low-myelin area, Brodmann area 7 (BA7) in the three species, despite species differences in cortical convolutions. Relative to the total cortical-surface area, those of MT + and the auditory cortex are significantly larger in night monkeys than diurnal monkeys, whereas area BA7 occupies a similar fraction of the cortical sheet in all three species. We propose that the selective expansion of sensory areas dedicated to visual motion and auditory processing in night monkeys may reflect cortical adaptations to a nocturnal environment.

Stereo electronic principles for selecting fully-protective, chemically-synthesised malaria vaccines.

Major histocompatibility class II molecule-peptide-T-cell receptor (MHCII-p-TCR) complex-mediated antigen presentation for a minimal subunit-based, multi-epitope, multistage, chemically-synthesised antimalarial vaccine is essential for inducing an appropriate immune response. Deep understanding of this MHCII-p-TCR complex's stereo-electronic characteristics is fundamental for vaccine development. This review encapsulates the main principles for achieving such epitopes' perfect fit into MHC-II human (HLADRß̞1*) or Aotus (Aona DR) molecules. The enormous relevance of several amino acids' physico-chemical characteristics is analysed in-depth, as is data regarding a 26.5 ± 2.5Å distance between the farthest atoms fitting into HLA-DRß1* structures' Pockets 1 to 9, the role of polyproline II-like (PPIIL) structures having their O and N backbone atoms orientated for establishing H-bonds with specific HLA-DRß1*-peptide binding region (PBR) residues. The importance of residues having specific charge and orientation towards the TCR for inducing appropriate immune activation, amino acids' role and that of structures interfering with PPIIL formation and other principles are demonstrated which have to be taken into account when designing immune, protection-inducing peptide structures (IMPIPS) against diseases scourging humankind, malaria being one of them.

Owl Monkey Alu Insertion Polymorphisms and Aotus Phylogenetics.

Owl monkeys (genus Aotus), or "night monkeys" are platyrrhine primates in the Aotidae family. Early taxonomy only recognized one species, Aotus trivirgatus, until 1983, when Hershkovitz proposed nine unique species designations, classified into red-necked and gray-necked species groups based predominately on pelage coloration. Recent studies questioned this conventional separation of the genus and proposed designations based on the geographical location of wild populations. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. A scaffold-level genome assembly for one Aotus species, Aotus nancymaae [Anan_2.0], facilitated large-scale ascertainment of nearly 2000 young lineage-specific Alu insertions. This study provides candidate oligonucleotides for locus-specific PCR assays for over 1350 of these elements. For 314 Alu elements across four taxa with multiple specimens, PCR analyses identified 159 insertion polymorphisms, including 21 grouping A. nancymaae and Aotus azarae (red-necked species) as sister taxa, with Aotus vociferans and A. trivirgatus (gray-necked) being more basal. DNA sequencing identified five novel Alu elements from three different taxa. The Alu datasets reported in this study will assist in species identification and provide a valuable resource for Aotus phylogenetics, population genetics and conservation strategies when applied to wild populations.

Lipid profile, apolipoproteins A-1 and B in owl monkeys (Aotus infulatus) in captivity.

BACKGROUND: Owl monkeys (Aotus infulatus) are frequently affected by heart diseases and, as in humans, dyslipidemia is one of the predisposing factors for adverse cardiovascular events. In view of this, the study of the lipid profile and plasma apolipoproteins can contribute to the clinical management of this neotropical primate species. METHODS: Lipid profile as well as A-1 and B apolipoprotein values were analyzed in 60 owl monkeys, studying their relationship with body biometry and the presence of cardiac alterations. RESULTS: Animals suspected of having heart disease did not show significant differences (p < .05) in terms of biometry or in relation to lipid profile and apolipoproteins A-1 and B values; however, higher values of LDL and ApoB and ApoB/ApoA-1 were observed in this group. CONCLUSIONS: This study is the first to describe the lipid profile and apolipoprotein values in owl monkeys, and further work will be needed to better elucidate the worthiness of LDL, ApoB, and the ApoB/ApoA-1 ratio in this primate species.

Pathways to paternal care in primates.

Natural selection will favor male care when males have limited alternative mating opportunities, can invest in their own offspring, and when care enhances males' fitness. These conditions are easiest to fulfill in pair-bonded species, but neither male care nor stable "breeding bonds" that facilitate it are limited to pair-bonded species. We review evidence of paternal care and extended breeding bonds in owl monkeys, baboons, Assamese macaques, mountain gorillas, and chimpanzees. The data, which span social/mating systems and ecologies, suggest that there are multiple pathways by which conditions conducive to male care can arise. This diversity highlights the difficulty of making inferences about the emergence of male care in early hominins based on single traits visible in the fossil record. We discuss what types of data are most needed and the questions yet to be answered about the evolution of male care and extended breeding bonds in the primate order.

Plasmodium falciparum in Aotus nancymaae: A New Model for Placental Malaria.

Plasmodium falciparum-infected erythrocytes that display the variant surface antigen VAR2CSA bind chondroitin sulfate A (CSA) to sequester in placental intervillous spaces, causing severe sequelae for mother and offspring. Here, we establish a placental malaria (PM) monkey model. Pregnant Aotus infected with CSA-binding P. falciparum CS2 parasites during the third trimester developed pronounced sequestration of late-stage parasites in placental intervillous spaces that express VAR2CSA and bind specifically to CSA. Similar to immune multigravid women, a monkey infected with P. falciparum CS2 parasites over successive pregnancies acquired antibodies against VAR2CSA, with potent functional activity that was boosted upon subsequent pregnancy infections. Aotus also developed functional antibodies after multiple acute PM episodes and subsequent VAR2CSA immunization. In summary, P. falciparum infections in pregnant Aotus monkeys recapitulate all the prominent features of human PM infection and immunity, and this model can be useful for basic mechanistic studies and preclinical studies to qualify candidate PM vaccines. Clinical Trials Registration: NCT02471378.

Out of the shadows: Multilocus systematics and biogeography of night monkeys suggest a Central Amazonian origin and a very recent widespread southeastward expansion in South America.

Night monkeys (Aotus, Cebidae) are a widely distributed genus of Neotropical primates with a poorly understood taxonomy and biogeography. The number of species in the genus varies from one to nine, depending on the author, and there are at least 18 known karyotypes, varying from 2n = 46 to 2n = 58. Historically, night monkeys are divided into two species groups: red- and grey-necked groups from south and north of the Amazon-Solimões River, respectively. Here, we used 10 nuclear and 10 mitochondrial molecular markers from a wide taxonomic and geographic sample to infer phylogeny, divergence times, and biogeography of the genus. For phylogenetic reconstruction we used Maximum Likelihood (ML) and Bayesian Inferences (BI). Biogeographic models were generated using the 'BioGeoBEARS' software. We found support for nine taxa of Aotus and rejected the existence of monophyletic "red necked" and "grey necked" species groups. We suggest a taxonomic reclassification of the genus, which is better represented by two clades named northern group, which contains Aotus miconax, A. nancymae, A. trivirgatus, A. vociferans, A. lemurinus, A. griseimembra, A. zonalis, and A. brumbacki, and southern group, which contains A. nigriceps, A. boliviensis, A. infulatus, and A. azarae. The results suggest that the most recent common ancestor of all species of Aotus arose in the central Amazon basin in the Early Pliocene. The evolutionary history of night monkeys was guided by dispersal, vicariance and founder events. The end of the Andean uplift and the subsequent changes in the Amazon landscape, as well as the Amazon-Solimões and Tapajós rivers may have played an important role in the origin and diversification of Aotus, respectively. However, most of the Amazonian rivers seem not to have been geographical barriers to dispersal of night monkeys. The herein named southern group is fruit of a very recent diversification guided by dispersal, crossing the Tapajós, Xingú, Tocantins, and Guapore rivers and reaching the Cerrado in the last 1.6 My.

Detection of early myocardial cell death in owl monkeys (Aotus nancymai) using complement component C9 immunohistochemistry in formalin-fixed paraffin-embedded heart tissues: A retrospective study.

BACKGROUND: Owl monkeys are commonly used in biomedical research which is affected by the high incidence of cardiomyopathy in this species. Occasionally, owl monkeys with no clinical signs of heart disease are found dead and at necropsy show no, or very mild, cardiomyopathy. A possible explanation for sudden death is acute myocardial infarction; however, early myocardial changes may be difficult to assess by conventional stains and light microscopy. METHODS: Complement component C9 immunohistochemistry was performed in paraffin-embedded heart tissue samples from owl monkeys who died suddenly, or were euthanized due to sickness, to determine whether these animals suffered from acute myocardial infarcts. RESULTS AND CONCLUSION: C9 deposits were found in the myocardium of 19 out of 20 (95%) animals. The findings in this study suggest owl monkeys suffer from acute myocardial infarcts, and complement component C9 immunohistochemistry may be a useful diagnostic tool.