Primate Simplexviruses Differ in Tropism for Macaque Cells.

Primate simplexviruses are closely related neurotropic herpesviruses, which are largely apathogenic in their respective host species. However, cross-species transmission of Macacine alphaherpesvirus 1 (McHV1, also termed herpes B virus) from rhesus macaques to humans can cause fatal encephalomyelitis. In contrast, closely related viruses, such as Cercopithecine alphaherpesvirus 2 (CeHV2, also termed simian agent 8) or Papiine alphaherpesvirus 2 (PaHV2, also termed herpesvirus papio 2), have not been linked to human disease and are believed to be largely apathogenic in humans. Here, we investigated whether McHV1, PaHV2 and CeHV2 differ in their capacity to infect human and non-human primate (NHP) cells. For comparison, we included the human simplexviruses HSV1 and HSV2 in our analyses. All five viruses replicated efficiently in cell lines of human and African green monkey origin, and McHV1 and PaHV2 also showed robust replication in rhesus macaque cell lines. In contrast, the replication of CeHV2 and particularly HSV1 and HSV2 in cell lines of rhesus macaque origin were reduced or inefficient. Similarly, McHV1, but not CeHV2, efficiently infected rhesus macaque brain organoids. These results point towards the previously unappreciated partial resistance of certain rhesus macaque cells to HSV1/HSV2/CeHV2 infection and reveal similarities between the cell tropism of McHV1 and PaHV2 that might be relevant for risk assessment.

Low rank and primiparity increase fecal glucocorticoid metabolites across gestation in wild geladas.

Integrative behavioral ecology requires accurate and non-invasive measures of hormone mediators for the study of wild animal populations. Biologically sensitive assay systems for the measurement of hormones and their metabolites need to be validated for the species and sample medium (e.g. urine, feces, saliva) of interest. Where more than one assay is available for hormone (metabolite) measurement, antibody selection is useful in identifying the assay that tracks changes in an individuals endocrine activity best, i.e., the most biologically sensitive assay. This is particularly important when measuring how glucocorticoids (GCs) respond to the subtle, additive effects of acute stressors during a predictable metabolic challenge, such as gestation. Here, we validate a group-specific enzyme immunoassay, measuring immunoreactive 11ß-hydroxyetiocholanolone, for use in a wild primate, geladas (Theropithecus gelada). This group-specific assay produced values correlated with those from a previously validated double-antibody, corticosterone 125I radioimmunoassay. However, the results with the group-specific assay showed a stronger response to an ACTH challenge and identified greater variation in gelada immunoreactive fecal glucocorticoid metabolites (iGCMs) compared with the corticosterone assay, indicating a higher biological sensitivity for assessing adrenocortical activity. We then used the group-specific assay to: (1) determine the normative pattern of iGCM levels across gelada gestation, and (2) identify the ecological, social, and individual factors that influence GC output for pregnant females. Using a general additive mixed model, we found that higher iGCM levels were associated with low rank (compared to high rank) and first time mothers (compared to multiparous mothers). This study highlights the importance of assay selection and the efficacy of group-specific assays for hormonal research in non-invasively collected samples. Additionally, in geladas, our results identify some of the factors that increase GC output over and above the already-elevated GC concentrations associated with gestation. In the burgeoning field of maternal stress, these factors can be examined to identify the effects that GC elevations may have on offspring development.

A Fosmid-Based System for the Generation of Recombinant Cercopithecine Alphaherpesvirus 2 Encoding Reporter Genes.

The transmission of Macacine alphaherpesvirus 1 (McHV-1) from macaques, the natural host, to humans causes encephalitis. In contrast, human infection with Cercopithecine alphaherpesvirus 2 (CeHV-2), a closely related alphaherpesvirus from African vervet monkeys and baboons, has not been reported and it is believed that CeHV-2 is apathogenic in humans. The reasons for the differential neurovirulence of McHV-1 and CeHV-2 have not been explored on a molecular level, in part due to the absence of systems for the production of recombinant viruses. Here, we report the generation of a fosmid-based system for rescue of recombinant CeHV-2. Moreover, we show that, in this system, recombineering can be used to equip CeHV-2 with reporter genes. The recombinant CeHV-2 viruses replicated with the same efficiency as uncloned, wt virus and allowed the identification of cell lines that are highly susceptible to CeHV-2 infection. Collectively, we report a system that allows rescue and genetic modification of CeHV-2 and likely other alphaherpesviruses. This system should aid future analysis of CeHV-2 biology.

Convergence of human and Old World monkey gut microbiomes demonstrates the importance of human ecology over phylogeny.

BACKGROUND: Comparative data from non-human primates provide insight into the processes that shaped the evolution of the human gut microbiome and highlight microbiome traits that differentiate humans from other primates. Here, in an effort to improve our understanding of the human microbiome, we compare gut microbiome composition and functional potential in 14 populations of humans from ten nations and 18 species of wild, non-human primates. RESULTS: Contrary to expectations from host phylogenetics, we find that human gut microbiome composition and functional potential are more similar to those of cercopithecines, a subfamily of Old World monkey, particularly baboons, than to those of African apes. Additionally, our data reveal more inter-individual variation in gut microbiome functional potential within the human species than across other primate species, suggesting that the human gut microbiome may exhibit more plasticity in response to environmental variation compared to that of other primates. CONCLUSIONS: Given similarities of ancestral human habitats and dietary strategies to those of baboons, these findings suggest that convergent ecologies shaped the gut microbiomes of both humans and cercopithecines, perhaps through environmental exposure to microbes, diet, and/or associated physiological adaptations. Increased inter-individual variation in the human microbiome may be associated with human dietary diversity or the ability of humans to inhabit novel environments. Overall, these findings show that diet, ecology, and physiological adaptations are more important than host-microbe co-diversification in shaping the human microbiome, providing a key foundation for comparative analyses of the role of the microbiome in human biology and health.

Male-inflicted wounds have opposite effects on hair cortisol for captive male and female rhesus macaques (Macaca mulatta) following new group formation.

Sexual dimorphism in body size, aggression, and dispersal patterns may affect the degree to which males and females perceive aggression from either sex as stressful. Whereas male macaques typically disperse to new groups at maturity, thus encountering many unfamiliar individuals of both sexes, females are philopatric, usually only encountering unfamiliar males who transfer into their natal groups. In rare circumstances, however, group fusions can expose both males and females to many novel individuals, which often increases aggression. Here, we use a captive new group formation of rhesus macaques (Macaca mulatta) as a model of social instability during fusions and examine differences in male and female chronic stress responses to male-pattern and female-pattern trauma (i.e., trauma inflicted by males or by females, respectively). We found that male- but not female-pattern traumas predicted hair cortisol concentrations during the first 9 months after new group formation, but in opposite ways for males and females. A greater number of male-pattern traumas was linked to elevated hair cortisol concentrations in females but slightly lower hair cortisol concentrations in males. We suggest that the apparent importance of male-pattern trauma, but not female-pattern-trauma, in predicting higher hair cortisol concentrations in females can be attributed to the more acutely intense but less persistent nature of male aggression toward females.

GPS-identified vulnerabilities of savannah-woodland primates to leopard predation and their implications for early hominins.

Predation is thought to have been a key selection pressure in primate evolution, especially in the savannah-woodland habitats where several early hominin species lived. However, predator-primate prey relationships are still poorly understood because human presence often deters predators, limiting our ability to quantify the impact of predation. Synchronized high-resolution tracking of leopards (Panthera pardus), vervets (Chlorocebus pygerythrus), and olive baboons (Papio anubis) during a 14-month study in Kenya revealed that increased vulnerability to leopard predation was not associated with higher encounter rates, smaller body size, smaller group size, or greater distance from refuges, contrary to long-standing inferences. Instead, the initiation, rate, timing, and duration of encounters, outcome of approaches, and predation events showed only a diel pattern of differential vulnerability. In the absence of human observers, vervets were more vulnerable during the day, whereas baboons were more vulnerable at night, but overall neither species was more vulnerable than the other. As our results show that leopards avoided baboons during the day and hunted them at night, we suggest that the same pattern would have applied to hominins-because they were even larger than baboons and bipedal, resulting in similarly offensive capability on the ground during the day but poorer agility in the trees at night, especially as they became committed bipeds. Drawing from hominid behavior and archaeopaleontological and ethnographic evidence, we hypothesize that ground-sleeping hominins initially dealt with this formidable threat by using stone tools to modify Acacia branches into 'bomas', thorny enclosures that provided nighttime shelter. The ability of hominins to create their own nightly refuges on the ground wherever Acacia spp. were available would have allowed them to range more widely, a crucial step in furthering the spread of hominins across Africa and beyond.

Understanding Primate Herpesviruses.

Viruses related to the herpes simplex viruses of humans are present in all nonhuman primate (NHP) species tested and cross species transmission has been documented. The herpesvirus present in macaques, Herpes B virus (BV) rarely causes disease in its natural macaque host. However, when transmitted to a nonnative host, BV has occasionally caused severe and even fatal disease if not treated immediately. Here we present a comprehensive review of the taxonomy, molecular biology, physiology, epidemiology, diagnosis and treatment of BV. We also summarizes what is known about related herpesviruses of other NHP species and the zoonotic potential of these viruses.

The vocal repertoire of Tibetan macaques (Macaca thibetana): A quantitative classification.

Vocal repertoires are basic and essential components for describing vocal communication in animals. Studying the entire suite of vocal signals aids investigations on the variation of acoustic structure across social contexts, comparisons on the complexity of communication systems across taxa, and in exploration of the evolutionary origins of species-specific vocalizations. Here, we describe the vocal repertoire of the largest species in the macaque genus, Macaca thibetana. We extracted thirty acoustic parameters from call recordings. Post hoc validation through quantitative analyses of the a priori repertoire classified eleven call types: coo, squawk, squeal, noisy scream, growl, bark, compound squeak, leap coo, weeping, modulated tonal scream, and pant. In comparison to the rest of the genus, Tibetan macaques uttered a wider array of vocalizations in the context of copulations. Previous reports did not include modulated tonal screams and pants during harassment of copulatory dyads. Furthermore, in comparison to the rest of the genus, Tibetan macaque females emit acoustically distinct copulation calls. The vocal repertoire of Tibetan macaques contributes to the literature on the emergence of species-specific calls in the genus Macaca with potential insights from social, reproductive, and ecological comparisons across species. Am. J. Primatol. 78:937-949, 2016. © 2016 Wiley Periodicals, Inc.

Endozoochorous seed dispersal by Japanese macaques (Macaca fuscata): Effects of temporal variation in ranging and seed characteristics on seed shadows.

Variation in seed shadows generated by frugivores is caused by daily, seasonal, and inter-annual variation in ranging, as well as inter-specific variability in gut passage times according to seed characteristics. We studied the extent to which seed weight, specific gravity, and daily (morning, afternoon, and evening) and inter-annual (2004 vs. 2005) variation in ranging affected seed shadows generated by wild Japanese macaques (Macaca fuscata) in northern Japan. The macaques ingested fleshy fruits of 11 species during the two year study period; Viburnum dilatatum (Caprifoliaceae: heavier seeds with higher specific gravity) and Rosa multiflora (Rosaceae: lighter seeds with lower specific gravity) were eaten frequently in both years. The travel distances of macaques after feeding on V. dilatatum and R. multiflora fruits were estimated by combining feeding locations and ranging patterns measured in the field with gut passage times of model seeds in captive animals. Median travel distances after fruit feeding were 431 (quantile range: 277-654) and 478 m (265-646), respectively, with a maximum of 1,261 m. Neither year nor time of day affected travel distances. The gut passage time of model V. dilatatum seeds was longer than that of model R. multiflora seed, but this did not affect dispersal distances. Seed shadows for both species over 2 years showed unimodal distribution (peak: 101-500 m) and more than 90%, 20%, and 3% of ingested seeds were estimated to be dispersed >100, >500, and >1000 m, respectively, the longest known distances among macaque species. R. multiflora seeds tended to be dispersed further in 2004 than 2005, but V. dilatatum seeds were not, implying that inter-annual variations in ranging pattern due to the distribution and abundance of nut fruiting could affect dispersal distance.

Coding potential of UL/b' from the initial source of rhesus cytomegalovirus Strain 68-1.

Rhesus cytomegalovirus (RhCMV) 68-1 is the prototypic strain of RhCMV that has been used for pathogenesis and vaccine development. We determined the complete sequence of the RhCMV 68-1 UL/b' region directly from the original urine from which RhCMV 68-1 was isolated in 1968, and compared it to other RhCMVs. The laboratory passaged RhCMV 68-1 has inversions, deletions, and stop codons in UL/b' that are absent in the original isolate and other low passage RhCMV isolates. Fourteen of the 17 open reading frames (ORFs) in 68-1 UL/b' in the original isolate share >95% amino acid identity with low passage RhCMV. The original isolate retains 6 ORFs that encode α-chemokine-like proteins, including RhUL146 and RhUL146b that share only 92% and 81% amino acid identity, respectively, with a contemporary low passage RhCMV isolate. Identification of the original RhCMV 68-1 UL/b' sequence is important for using RhCMV 68-1 in pathogenesis and vaccine studies.

Secondary sex ratio and maternal dominance rank among wild yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania.

The Trivers and Willard model predicts that offspring of dominant mothers will be biased toward males and offspring of subordinate mothers towards females, whereas a local-resource-competition hypothesis predicts the reverse. Available data bearing upon these alternative predictions are inconsistent. It has been suggested that the local-resource-competition hypothesis will predominate when resources are scarce, and the Trivers-Willard hypothesis when resources are abundant. The relationship between maternal dominance and secondary sex ratio for 214 offspring of 61 females was examined using four troops of wild yellow baboons living in Mikumi National Park, where the population was increasing in a resource-rich habitat. For all troops combined, no significant relationship was found between offspring sex ratio and maternal rank. The four troops separately showed inconsistent trends, and in no case did the relationship reach conventional levels of statistical significance. In contrast, the local resource-competition hypothesis was supported by a study of yellow baboons done with one troop and 80 offspring in Amboseli National Park, where a massive population decline had occurred. The contrasting Amboseli and Mikumi results may be due to differences in resource-competition at the two study sites, or to stochastic variation. © 1992 Wiley-Liss, Inc.