Social factors drive vocal exchanges in red-capped mangabeys (Cercocebus torquatus).

Of all the calls made by non-human primates, the function of short-distance contact calls has largely remained to be determined. These calls are the most frequent in the repertoire and are most often exchanged between individuals in a non-random way. To our knowledge, no study has ever examined how vocal exchanges are structured in red-capped mangabeys (Cercocebus torquatus), a semi-terrestrial monkey living in the African forest with a complex semi-tolerant/semi-despotic social system. Our goal was to assess the organization of contact call exchanges in this species and their relationship with individual and social factors such as age, affinity, and hierarchy. Therefore, we observed several captive groups of red-capped mangabeys and collected data on vocal behavior, as well as grooming, agonistic behavior, and spatial proximity. We defined a vocal exchange in this species as a series of contact calls made by two or more individuals within a maximum inter-caller interval of 2 s. At the individual level, the higher the individual's hierarchical rank, the less they initiated exchanges. Furthermore, the most socially integrated individuals had a longer average response time than the less integrated ones. At the dyadic level, preferred exchange partners were individuals often observed near one other or individuals most distant in age. Also, the further apart two individuals were in the dominance hierarchy, the shorter the response time. Our results support both the social bonding hypothesis and a modulating key role of the dominance hierarchy on the social use of contact calls, which is in line with the social style of this species.

Golden-bellied mangabeys (Cercocebus chrysogaster) exhibit a larger home range and longer travel distances than those of bonobos (Pan paniscus) at LuiKotale, Democratic Republic of the Congo.

Primate ranging behavior is associated with numerous social and ecological correlates. Interspecific comparisons of ranging behavior can therefore provide insight into the socio-ecological conditions that characterize a species' niche within its community. We provide the first description of ranging behavior in golden-bellied mangabeys (Cercocebus chrysogaster), using sympatric bonobos (Pan paniscus) as a comparison. Over 6 months, we recorded GPS tracks at 1- and 5-min intervals from one habituated golden-bellied mangabey group and two habituated bonobo communities at LuiKotale, central Democratic Republic of the Congo. We compared estimates of home range size, time spent at different elevations, and hourly travel distances between species. We modeled daily travel distances against total monthly rainfall to investigate seasonal variation in daily ranging. The golden-bellied mangabey home range was similarly sized or larger than each of the two bonobo communities at LuiKotale across estimation methods. Mangabeys visited more of their range per day and spent more time in terra firma forest and less time in swamps than bonobos. Mangabeys traveled significantly farther per day and during midday hours than bonobos, but travel distances did not relate to monthly rainfall in either species. Golden-bellied mangabeys exhibited wide daily ranging behavior that more closely resembled that of sympatric bonobos than other Cercocebus species. Large homes ranges in mangabeys are likely influenced by food availability in terra firma forest, especially as groups appear to travel long distances between fruit trees and terrestrial food patches. Maximizing daytime activity may help mangabeys avoid competition from heterospecifics and indicates temporal niche partitioning in this primate community.

Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form.

Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1-2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = âˆ¼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.

Intentional gestural communication amongst red-capped mangabeys (Cercocebus torquatus).

Apes, human's closest living relatives, are renowned for their intentional and highly flexible use of gestural communication. In stark contrast, evidence for flexible and intentional gestural communication in monkeys is scarce. Here, we investigated the intentionality and flexibility of spontaneous gesture use in red-capped mangabeys (Cercocebus torquatus). We applied established methods used in ape gesture research to analyse whether the body acts produced by a total of 17 individuals living in three different groups in captivity qualified as intentionally produced gesture instances. Results showed that signallers showed all hallmarks of intentionality during the production of 20 out of a total of 21 different types of body acts. These were only produced in the presence of other individuals, and the monkeys showed audience checking, sensitivity to the attentional states of recipients, adjustment of signal modality, and response waiting relative to their production. Moreover, in case of communication failure, the monkeys showed goal persistence, and regarding the production contexts they showed some signs of means-ends dissociation. Therefore, these monkeys are capable of flexible and intentional gestural communication and use this to communicate with conspecifics. Our results corroborate recent findings showing that intentional gestural communication was already present in the monkey lineage of catarrhine primates. We discuss our results in light of the comparative approach towards human language evolution and highlight our finding that these monkeys also showed flexible and intentional use of four 'free' manual gesture types.

Maximum longevity and juvenile mortality in zoo-housed mangabeys.

Little is known about the biology of grey-cheeked and black crested mangabeys (Lophocebus albigena and Lophocebus aterrimus, respectively). As these primates face threats in the wild, well-monitored zoo-housed populations with up to date registries are becoming increasingly valuable to acquire species knowledge and to support conservation efforts. We used international studbooks to extract demographic and genetic information on 519 mangabeys to investigate how life history and parent-related variables influence maximum longevity and juvenile mortality. Generalized linear mixed models, as well as survival analyses, were applied. Results showed that females lived significantly longer than males, which is not uncommon in primates. Furthermore, our results indicated that the maximum longevity is lower for individuals living in European zoos versus individuals from North American zoos, which may be due to a combination of environmental differences and potential founder effects. We also show that the maternal maximum longevity is positively related to the maximum longevity of the offspring, which may be explained by the inheritance of "good genes". However, the age of the mother at the moment of birth was negatively related to the maximum longevity of the offspring, which contradicts literature that states that, in primates, more experienced and thus older mothers will raise their offspring better than less experienced mothers. Instead, it is more likely that an "optimal age range" exists for breeding mothers. Our study provides insights into the population biology of captive mangabeys and may be helpful for identifying future research priorities to optimize primate health and welfare directly ex situ, and indirectly in situ.

Estimating the population size of the Sanje mangabey (Cercocebus sanjei) using acoustic distance sampling.

The Sanje mangabey (Cercocebus sanjei) is endemic to the Udzungwa Mountains, Tanzania, and is classified as Endangered due to its putatively declining population size, habitat degradation and fragmentation. Previous population size estimates have ranged from 1,350 to 3,500 individuals, with the last direct survey being conducted 15 years before the present study. Previous estimates are now thought to have underestimated the population due to a limited knowledge of group and habitat size, nonsystematic approaches and the use of visual methods that are not suitable for surveying the Sanje mangabey with its semi-terrestrial and elusive behaviors. We used an acoustic survey method with observers recording the distinctive "whoop-gobble" vocalization produced by mangabeys and point transect distance sampling to model a detection function and estimate abundance. Twenty-eight surveys were conducted throughout the two forests where Sanje mangabeys are found: Mwanihana forest in the Udzungwa Mountains National Park (n = 13), and the Uzungwa Scarp Nature Reserve (n = 15). Group density was found to be significantly lower in the relatively unprotected Uzungwa Scarp forest (0.15 groups/km2 ; 95% CI: 0.08-0.27) compared to the well-protected Mwanihana forest (0.29 groups/km2 ; 95% CI: 0.19-0.43; p = .03). We estimate that there are 1,712 (95% CI: 1,141-2,567) individuals in Mwanihana and 1,455 (95% CI: 783-2,702) in the Uzungwa Scarp, resulting in a total population size of 3,167 (95% CI: 2,181-4,596) individuals. The difference in group density between sites is likely a result of the differing protection status and levels of enforcement between the forests, suggesting that protection of the Uzungwa Scarp should be increased to encourage recovery of the population, and reduce the threat of degradation and hunting. Our results contribute to the reassessment of the species' IUCN Red List status and informing management and conservation action planning.

Maternal Care in Free-Ranging Arboreal Grey-Cheeked Mangabeys (Lophocebus albigena johnstoni) in Kibale National Park, Uganda.

Maternal styles have been intensively studied in a variety of terrestrial species of primates, but far less in arboreal species. However, to have a balanced view of the evolution of maternal care, it is necessary to investigate this behaviour in the context of habitat. Here, we investigate whether the mother's parity, age and dominance rank, as well as the infant's age and sex, influence maternal care and mother-infant proximity in arboreal grey-cheeked mangabeys (Lophocebus albigena). We observed 13 mother-infant dyads in four free-ranging groups for 6 months. Our main finding is that maternal care is a dynamic process affected by a mix of mothers' and infants' characteristics. We found that first-time mothers spent more time watching their infants than multiparous mothers, who carried, groomed and protected their infants more often. We also found that low-ranking mothers prevented their infants from leaving them more often than did high-ranking mothers. Moreover, mothers adjusted their care as infants became older. They groomed and protected female infants more than male infants, behaviours common in female-bonded species. Our study shows the ever-changing dynamics of maternal care related to infant age and highlights the role of the mother's parity and rank in this process.

Group movements in response to competitors' calls indicate conflicts of interest between male and female grey-cheeked mangabeys.

Long-distance vocalizations mediate spacing patterns by allowing groups to choose whether to draw close enough to a neighbor to initiate a short-range interaction. It is unclear, however, whether the patterning of calls and the resulting movements are invariant or change in response to social and ecological variables. In this study, we compare the impact of long-distance calls on neighboring groups' movements in two populations of grey-cheeked mangabeys (Lophocebus albigena) in Uganda, which differed widely in group density and food availability. We monitored movement responses of target groups to both naturally occurring and experimentally simulated "whoop-gobble" vocalizations of neighboring adult males to test whether responses indicated mate and food defense. When defending access to fertile females, males might coerce group members to move away from neighboring males; when defending fitness-limiting food resources, however, groups might approach and attempt to evict neighbors. Controlling for pre-call movement prior to the vocalization, we found no difference in group responses between the low- and high-density populations, and little support for either form of defense. Mangabey groups generally continued moving in their original direction, albeit at a slower pace, and deviations from this pattern were predictable: they avoided nearby callers but approached distant callers; they approached if the caller was in the area where home ranges overlapped; and approached when their own group contained multiple peak-estrous females. The effect of multiple fertile females potentially indicates a breakdown of male control as a result of within-group intrasexual mating competition, and greater-than-expected female control over travel movements. As suspected, grey-cheeked mangabeys use neighbors' long-distance calls to maintain a spatial buffer between groups but changes in group movements indicate a conflict between male and female interests.

Gastrointestinal protists and helminths of habituated agile mangabeys (Cercocebus agilis) at Bai Hokou, Central African Republic.

Infectious diseases including those caused by parasites can be a major threat to the conservation of endangered species. There is thus a great need for studies describing parasite infections of these species in the wild. Here we present data on parasite diversity in an agile mangabey (Cercocebus agilis) group in Bai Hokou, Dzanga-Sangha Protected Areas (DSPA), Central African Republic. We coproscopically analyzed 140 mangabey fecal samples by concentration techniques (flotation and sedimentation). Agile mangabeys hosted a broad diversity of protistan parasites/commensals, namely amoebas (Entamoeba spp., Iodamoeba buetschlli), a Buxtonella-like ciliate and several parasitic helminths: strongylid and spirurid nematodes, Primasubulura sp., Enterobius sp., and Trichuris sp. Importantly, some of the detected parasite taxa might be of potential zoonotic importance, such as Entamoeba spp. and the helminths Enterobius sp., Trichuris sp., and strongylid nematodes. Detailed morphological examination of ciliate cysts found in mangabeys and comparison with cysts of Balantioides coli from domestic pigs showed no distinguishing structures, although significant differences in cyst size were recorded. Scanning or transmission electron microscopy combined with molecular taxonomy methods are needed to properly identify these ciliates. Further studies using molecular epidemiology are warranted to better understand cross-species transmission and the zoonotic potential of parasites in sympatric non-human primates and humans cohabiting DSPA.

Decision-making under risk of gain in young children and mangabey monkeys.

In contrast to human adults, risk proneness in the gain domain is usually observed in both young children and non-human primates. It is currently unclear what mechanism might be underlying such economic preferences. We investigated decision-making under risk of gain in toddlers and monkeys. The choices of 2.5-year-old children and red-capped mangabeys (Cercocebus torquatus torquatus) were examined in a gambling task for food reward in which participants have to choose between two options, a secure option and a risky option. In contrast to monkeys, toddlers showed a strong preference for the risky option over the safe option. In order to test the hypothesis that risky choices in participants reflect inhibitory control difficulties, toddlers and mangabeys were presented in Experiment 2 with a situation analogous to that used in Experiment 1 except for the fact that the opaque cover under which was placed the secure option was replaced by a transparent cover. In this second experiment, toddlers continued to show a preference for the risky option over the safe option. In contrast, mangabeys showed a preference for the safe option over the risky option in Trial 1 but they shifted their economic preferences in Trial 2. We argue that decision-making strategies under risk of gain in both toddlers and mangabeys (a) do not reflect poor behavioral control and (b) are not reducible to perception-action couplings.

First molecular identification of Buxtonella ciliates from captive-bred mangabeys (Cercocebus torquatus) from China.

Buxtonella species are large cyst-forming ciliates that infect ruminants and monkeys, and are morphologically similar to Balantidium coli ciliates that infect pigs, humans, monkeys, and other animals. In this study, we isolated spherical cysts of ciliates that were similar to those of Balantidium and Buxtonella species within collared mangabeys (Cercocebus torquatus) from the Wangcheng Zoo of Luoyang in the Henan Province of central China. The cysts were further identified and designated as belonging to the Buxtonella monkey genotype based on molecular analyses of 18S rRNA, 5.8S rRNA, and ITS1-5.8S rRNA-ITS2 genetic markers. To our knowledge, this is the first report of Buxtonella monkey genotype within monkeys in China. These results will help clarify the classification of species of cyst-forming ciliate infections in monkeys.

Consequences of a male takeover on mating skew in wild Sanje mangabeys.

Among primate species living in multimale-multifemale groups, the number of receptive females may determine the rank of the lowest male that copulates (priority of access model, or PoA [Altmann SA. 1962. A field study of the sociobiology of rhesus monkeys, Macaca mulatta. Annals of the New York Academy of Sciences 102:338-435]). Factors, such as temporary instability in the hierarchy and female behavior can, however, affect high-ranking males' ability to monopolize females, reducing mating skew and causing the hierarchy to depart from predictions of PoA. Here, I use behavioral data collected over a 22-month period on a wild group of Sanje mangabeys (Cercocebus sanjei) to examine the effect of a takeover by two immigrating males who became α and ß in the hierarchy, and of female behavior on male mating skew. Data on male agonistic interactions were collected on nine males using ad libitum observations, while information on male mating success (i.e., daily proportion of ejaculatory copulations with the focal female) was collected through focal follows of 12 sexually receptive females. Before the takeover, the hierarchy was stable and highly skewed, with the α-male monopolizing up to 75% of copulations. At this time, however, mating skew did not follow the predictions of PoA. During the takeover, from the time one of the newly immigrant males replaced the α until the second immigrant male became the new ß, the stability of the hierarchy dropped significantly and mating was no longer skewed. Accordingly, the top two ranking males at that time (i.e., the new α and former ß) accounted for only 33% of copulations. After the takeover, rank stability increased, and mating skew followed the PoA. Female mating solicitations also had a significant positive effect on male mating success, and may have contributed to the deviation from the PoA. This study demonstrates that temporary rank instability decreases high-ranking males' ability to monopolize copulations, causing a departure from the predictions of the PoA. Am. J. Primatol. 79:e22532, 2017. © 2016 Wiley Periodicals, Inc.

Changes in physiological stress and behaviour in semi-free-ranging red-capped mangabeys (Cercocebus torquatus) following antiparasitic treatment.

Parasites are ubiquitous in wildlife populations, but physiological and behavioural responses of hosts to infection are difficult to measure. We experimentally treated semi-free-ranging red-capped mangabeys (Cercocebus torquatus) in Nigeria with antiparasitic drugs and examined subsequent changes in glucocorticoid production and individual behaviour. Because both parasites and stress impact energy balance and health, we measured (i) behavioural time re-allocation via activity budgets, (ii) social relationships (e.g. social connectivity and dominance hierarchy stability) and (iii) body condition. We collected triplicate faecal samples (n = 441) from 49 individuals prior to and following treatment. Cortisol levels fluctuated in parallel with parasite abundance. Elevations in cortisol, but not parasitism, were related to reduced body condition. Behaviour also shifted according to infection status, with uninfected individuals spending more time foraging and less time resting and vigilant compared with when they were infected. Time spent feeding, travelling or socializing did not differ between pre- and post-treatment time periods. Group cohesion, but not dominance stability, changed following treatment, suggesting parasite-induced social avoidance. Together, these findings show a coordinated response to infection that promotes host tolerance through stress and energy conservation, reduces transmission risk and increases protection when infected hosts are vulnerable.

Characterization of the interactions between SIVrcm Vpx and red-capped mangabey SAMHD1.

SAMHD1 (SAM domain- and HD domain-containing protein 1) inhibits HIV-1 infection of myeloid cells and resting CD4+ T-cells. Two lineages of primate lentiviruses, the sooty mangabey SIV (simian immunodeficiency virus) (SIVsm)/macaque SIV (SIVmac)/HIV-2 lineage and the red-capped mangabey SIV (SIVrcm) lineage, carry a SAMHD1 antagonist called Vpx. Vpx recognizes SAMHD1 and recruits a ubiquitin E3 ligase complex that is composed of CUL4 (Cullin4), DDB1 (damaged DNA-binding protein 1) and a member of the DCAF (DDB1/CUL4-associated factor) family called DCAF1. This E3 ligase complex polyubiquitinates SAMHD1, which leads to proteasomal degradation of SAMHD1. As opposed to the well-characterized interaction of SIVmac Vpx with human SAMHD1 and DCAF1, SIVrcm Vpx adopts a different mode of interaction with SAMHD1 of red-capped mangabeys. In the present study, we have characterized the interactions that are essential for SIVrcm Vpx-mediated degradation of rcmSAMHD1 (red-capped mangabey SAMHD1). Using mutagenesis and molecular modelling, we have determined the key role of the W23LHR26 peptide of SIVrcm Vpx in recognizing rcmSAMHD1. The amino acids Phe15, Leu36, Phe52, Arg55 and Arg56 at the N-terminal domain (NtD) of rcmSAMHD1 are involved in interaction with Vpxrcm (red-capped mangabey Vpx). The molecular model of rcmSAMHD1-NtD, Vpxrcm and C-terminal domain (CtD) of DCAF1 (DCAF1-CtD) complex reveals further that rcmSAMHD1-NtD and Vpxrcm utilize an interaction interface that is different from that used by human SAMHD1-CtD and Vpxsm. These findings provide further insights into the different modes of interaction between Vpx and SAMHD1 as the result of the 'arms race' of virus and host cell.

Call rates of mothers change with maternal experience and with infant characteristics in free-ranging gray-cheeked mangabeys.

Studies have shown that becoming a mother triggers important social changes within females, according to both social experience and infant characteristics, showing different maternal concerns. But how this impacts call usage has been far less studied. Based on 6 months of observations of five free-ranging groups of gray-cheeked mangabeys, we investigated variations in the production of three call types (contact, excitement, and alarm calls) in 29 females of different ages, dominance ranks, and infant rearing experiences: 15 females with infants of different ages and sexes, and 14 females without infants. We found that in females with infants-both maternal and infant characteristics influenced call production in a call type-dependent way. Females produced contact calls at a higher rate during the first month of infant age and after weaning when infants start to move away. Mothers of daughters produced more contact calls than mothers of sons. More excitement calls were recorded for first-time and young mothers and for females with young infants, while alarm call rates were not influenced by any of these factors. Increased mother-infant spatial separation enhanced only contact and excitement call rates. Finally, we found that females with infants vocalized much more than females without infants. Our results contribute to the current debate about the social factors responsible for the flexibility of call usage in nonhuman primates and open new lines for research on mothering behavior in forest-dwelling species. Am. J. Primatol. 78:983-991, 2016. © 2016 Wiley Periodicals, Inc.

How Many for Lunch Today? Seasonal Fission-Fusion Dynamics as a Feeding Strategy in Wild Red-Capped Mangabeys (Cercocebus torquatus).

For group-living primates, social organization hinges upon multiple factors, including group size, group cohesion, and the group's age and sex composition. Fission-fusion dynamics reduce the risks of living in a large group, which can include feeding competition related to the seasonality of resources. Here we report on the group dynamics (i.e. formation of parties) of a population of red-capped mangabeys (Cercocebus torquatus) located in Sentier Nature forest, South Loango National Park, Gabon, and examine the role of fruit availability in episodes of fission-fusion and shifting range use during the peak fruiting season of 2014. To assess fission-fusion dynamics, we obtained data on party type (i.e. number, size and age-sex composition), the effect of availability of fruit from 4 tree species on the home range and habitat used by parties, and the periodicity of these processes. The results show that red-capped mangabeys displayed seasonal fission-fusion dynamics related to fruit availability during the season under study.

Down-modulation of primate lentiviral receptors by Nef proteins of simian immunodeficiency virus (SIV) of chimpanzees (SIVcpz) and related SIVs: implication for the evolutionary event at the emergence of SIVcpz.

It has been estimated that human immunodeficiency virus type 1 originated from the zoonotic transmission of simian immunodeficiency virus (SIV) of chimpanzees, SIVcpz, and that SIVcpz emerged by the recombination of two lineages of SIVs in Old World monkeys (SIVgsn/mon/mus in guenons and SIVrcm in red-capped mangabeys) and SIVcpz Nef is most closely related to SIVrcm Nef. These observations suggest that SIVrcm Nef had an advantage over SIVgsn/mon/mus during the evolution of SIVcpz in chimpanzees, although this advantage remains uncertain. Nef is a multifunctional protein which downregulates CD4 and coreceptor proteins from the surface of infected cells, presumably to limit superinfection. To assess the possibility that SIVrcm Nef was selected by its superior ability to downregulate viral entry receptors in chimpanzees, we compared its ability to down-modulate viral receptor proteins from humans, chimpanzees and red-capped mangabeys with Nef proteins from eight other different strains of SIVs. Surprisingly, the ability of SIVrcm Nef to downregulate CCR5, CCR2B and CXCR6 was comparable to or lower than SIVgsn/mon/mus Nef, indicating that ability to down-modulate chemokine receptors was not the selective pressure. However, SIVrcm Nef significantly downregulates chimpanzee CD4 over SIVgsn/mon/mus Nefs. Our findings suggest the possibility that the selection of SIVrcm Nef by ancestral SIVcpz is due to its superior capacity to down-modulate chimpanzees CD4 rather than coreceptor proteins.

High rates of infection with novel enterovirus variants in wild populations of mandrills and other old world monkey species.

UNLABELLED: Enteroviruses (EVs) are a genetically and antigenically diverse group of viruses infecting humans. A mostly distinct set of EV variants have additionally been documented to infect wild apes and several, primarily captive, Old World monkey (OWM) species. To investigate the prevalence and genetic characteristics of EVs infecting OWMs in the wild, fecal samples from mandrills (Mandrillus sphinx) and other species collected in remote regions of southern Cameroon were screened for EV RNA. Remarkably high rates of EV positivity were detected in M. sphinx (100 of 102 screened), Cercocebus torquatus (7/7), and Cercopithecus cephus (2/4), with high viral loads indicative of active infection. Genetic characterization in VP4/VP2 and VP1 regions allowed EV variants to be assigned to simian species H (EV-H) and EV-J (including one or more new types), while seven matched simian EV-B variants, SA5 and EV110 (chimpanzee). Sequences from the remaining 70 formed a new genetic group distinct in VP4/2 and VP1 region from all currently recognized human or simian EV species. Complete genome sequences were obtained from three to determine their species assignment. In common with EV-J and the EV-A A13 isolate, new group sequences were chimeric, being most closely related to EV-A in capsid genes and to EV-B in the nonstructural gene region. Further recombination events created different groupings in 5' and 3' untranslated regions. While clearly a distinct EV group, the hybrid nature of new variants prevented their unambiguous classification as either members of a new species or as divergent members of EV-A using current International Committee on Taxonomy of Viruses (ICTV) assignment criteria. IMPORTANCE: This study is the first large-scale investigation of the frequency of infection and diversity of enteroviruses (EVs) infecting monkeys (primarily mandrills) in the wild. Our findings demonstrate extremely high frequencies of active infection (95%) among mandrills and other Old World monkey species inhabiting remote regions of Cameroon without human contact. EV variants detected were distinct from those infecting human populations, comprising members of enterovirus species B, J, and H and a large novel group of viruses most closely related to species A in the P1 region. The viral sequences obtained contribute substantially to our growing understanding of the genetic diversity of EVs and the existence of interspecies chimerism that characterizes the novel variants in the current study, as well as in previously characterized species A and J viruses infecting monkeys. The latter findings will contribute to future development of consensus criteria for species assignments in enteroviruses and other picornavirus genera.

Unraveling the effect of genomic structural changes in the rhesus macaque - implications for the adaptive role of inversions.

BACKGROUND: By reshuffling genomes, structural genomic reorganizations provide genetic variation on which natural selection can work. Understanding the mechanisms underlying this process has been a long-standing question in evolutionary biology. In this context, our purpose in this study is to characterize the genomic regions involved in structural rearrangements between human and macaque genomes and determine their influence on meiotic recombination as a way to explore the adaptive role of genome shuffling in mammalian evolution. RESULTS: We first constructed a highly refined map of the structural rearrangements and evolutionary breakpoint regions in the human and rhesus macaque genomes based on orthologous genes and whole-genome sequence alignments. Using two different algorithms, we refined the genomic position of known rearrangements previously reported by cytogenetic approaches and described new putative micro-rearrangements (inversions and indels) in both genomes. A detailed analysis of the rhesus macaque genome showed that evolutionary breakpoints are in gene-rich regions, being enriched in GO terms related to immune system. We also identified defense-response genes within a chromosome inversion fixed in the macaque lineage, underlying the relevance of structural genomic changes in evolutionary and/or adaptation processes. Moreover, by combining in silico and experimental approaches, we studied the recombination pattern of specific chromosomes that have suffered rearrangements between human and macaque lineages. CONCLUSIONS: Our data suggest that adaptive alleles - in this case, genes involved in the immune response - might have been favored by genome rearrangements in the macaque lineage.