Old World Monkey Species Research Articles

Replication potentials of HIV-1/HSIV in PBMCs from northern pig-tailed macaque (Macaca leonina).

The northern pig-tailed macaque (Macaca leonina) has been identified as an independent species of Old World monkey, and we previously found that PBMCs from M. leonina were susceptible to human immunodeficiency virus type 1 (HIV-1), which may be due to the absence of a TRIM5 protein restricting HIV-1 replication. Here we investigated the infection potentials of six laboratory adapted HIV-1 strains and three primary HIV-1 isolates in PBMCs from M. leonina. The results indicate that these strains are characterized by various but low replication levels, and among which, HIV-1NL4-3 shows the highest replication ability. Based on the abundant evidence of species-specific interactions between restriction factors APOBEC3 and HIV/SIV-derived Vif protein, we subsequently examined the replication potentials of vif-substituted HIV-1 (HSIV) in M. leonina PBMCs. Notably, HSIV-vifmac and stHIV-1SV chimeras, two HIV-1NL4-3-derived viruses encoding the viral infectivity factor (Vif) protein from SIVmac239, replicated robustly in cells from M. leonina, which suggests that HSIV could effectively antagonize the antiviral activity of APOBEC3 proteins expressed in cells of M. leonina. Therefore, our data demonstrate that M. leonina has the potential to be developed into a promising animal model for human AIDS.

One Good Turn Deserves Another: Combat versus Other Functions of Acrobatic Maneuvers in the Play Fighting of Vervet Monkeys (Chlorocebus aethiops)

During play fighting, animals make a variety of movements, some of which seem unrelated to the ongoing actions of the partner. Among such movements are the jumps and rotations reported in many species of Old World monkeys. In the present study, videotaped sequences of jumps and rotations performed by juvenile vervet monkeys were analyzed. Using the Eshkol-Wachman Movement Notation (EWMN) the sequences were described frame-by-frame revealing that about 82% of the jumps and rotations were correlated with the movements performed by the partner, consistent with the view that these movements are used as tactics of attack and defense. The majority of the remaining 18% occurred in contexts in which the performer solicited playful attacks from the partner. A small number of the rest were performed in a manner consistent with the movements being imposed by the performer to increase the difficulty in contacting the partner. The same distribution was present in both captive and free-living monkeys. Thus the analyses show that while most jumps were combat-related, these movements can occur in a variety of functional contexts.

Persistent human hepatitis B virus infection in cynomolgus monkeys: A novel animal model in the search for a cure?

Persistent human hepatitis B virus infection in cynomolgus monkeys: A novel animal model in the search for a cure?

Manual laterality for pointing gestures compared to grasping actions in guenons and mangabeys

In both humans and apes, the production of communicative gestures appears to be controlled by cerebral structures in the left hemisphere that would be distinct from those involved in noncommunicative actions. Whether communicative gestures also rely on specific lateralized systems in monkeys remains unclear. We assessed manual laterality for requesting gestures, i.e. pointing, and for grasping actions in two species of Old World monkeys, Campbell's monkeys, Cercopithecus campbelli, and red-capped mangabeys, Cercocebus torquatus, using the Bishop QHP task. The food items were placed at five positions in front of the monkeys and they were located at out-of-reach, far or close distance from the monkeys, to induce pointing gestures and grasping actions requiring full or low arm extensions, respectively. The mangabeys that exhibited the greatest skills for pointing referentially were more right-handed for pointing gestures than for grasping actions. We propose that in Old World monkeys, as in humans and apes, the production of intentional and referential gestures may rely on the activation of specific regions of the left hemisphere specialized in the processing of communicative signals. Subjects from both species preferred to use the hand that was closest to the item for grasping actions requiring low arm extension whereas they used the contralateral hand for grasping actions requiring full arm extension and pointing gestures. These results are discussed in relation to hypotheses on postural control and arboreality.

A MODULAR FRAMEWORK CHARACTERIZES MICRO- AND MACROEVOLUTION OF OLD WORLD MONKEY DENTITIONS

The study of modularity can provide a foundation for integrating development into studies of phenotypic evolution. The dentition is an ideal phenotype for this as it is developmentally relatively simple, adaptively highly significant, and evolutionarily tractable through the fossil record. Here, we use phenotypic variation in the dentition to test a hypothesis about genetic modularity. Quantitative genetic analysis of size variation in the baboon dentition indicates a genetic modular framework corresponding to tooth type categories. We analyzed covariation within the dentitions of six species of Old World monkeys (OWMs) to assess the macroevolutionary extent of this framework: first by estimating variance-covariance matrices of linear tooth size, and second by performing a geometric morphometric (GM) analysis of tooth row shape. For both size and shape, we observe across OWMs a framework of anterior and postcanine modules, as well as submodularity between the molars and premolars. Our results of modularity by tooth type suggest that adult variation in the OWM dentition is influenced by early developmental processes such as odontogenesis and jaw patterning. This study presents a comparison of genotypic modules to phenotypic modules, which can be used to better understand their action across evolutionary time scales.

Visual Recognition of Age Class and Preference for Infantile Features: Implications for Species-Specific vs Universal Cognitive Traits in Primates

Despite not knowing the exact age of individuals, humans can estimate their rough age using age-related physical features. Nonhuman primates show some age-related physical features; however, the cognitive traits underlying their recognition of age class have not been revealed. Here, we tested the ability of two species of Old World monkey, Japanese macaques (JM) and Campbell's monkeys (CM), to spontaneously discriminate age classes using visual paired comparison (VPC) tasks based on the two distinct categories of infant and adult images. First, VPCs were conducted in JM subjects using conspecific JM stimuli. When analyzing the side of the first look, JM subjects significantly looked more often at novel images. Based on analyses of total looking durations, JM subjects looked at a novel infant image longer than they looked at a familiar adult image, suggesting the ability to spontaneously discriminate between the two age classes and a preference for infant over adult images. Next, VPCs were tested in CM subjects using heterospecific JM stimuli. CM subjects showed no difference in the side of their first look, but looked at infant JM images longer than they looked at adult images; the fact that CMs were totally naïve to JMs suggested that the attractiveness of infant images transcends species differences. This is the first report of visual age class recognition and a preference for infant over adult images in nonhuman primates. Our results suggest not only species-specific processing for age class recognition but also the evolutionary origins of the instinctive human perception of baby cuteness schema, proposed by the ethologist Konrad Lorenz.

Geographical, genetic and functional diversity of antiretroviral host factor TRIMCyp in cynomolgus macaque (Macaca fascicularis)

The antiretroviral factor tripartite motif protein 5 (TRIM5) gene-derived isoform (TRIMCyp) has been found in at least three species of Old World monkey: rhesus (Macaca mulatta), pig-tailed (Macaca nemestrina) and cynomolgus (Macaca fascicularis) macaques. Although the frequency of TRIMCyp has been well studied in rhesus and pig-tailed macaques, the frequency and prevalence of TRIMCyp in cynomolgus macaques remain to be definitively elucidated. Here, the geographical and genetic diversity of TRIM5α/TRIMCyp in cynomolgus macaques was studied in comparison with their anti-lentiviral activity. It was found that the frequency of TRIMCyp in a population in the Philippines was significantly higher than those in Indonesian and Malaysian populations. Major and minor haplotypes of cynomolgus macaque TRIMCyp with single nucleotide polymorphisms in the cyclophilin A domain were also found. The functional significance of the polymorphism in TRIMCyp was examined, and it was demonstrated that the major haplotype of TRIMCyp suppressed human immunodeficiency virus type 1 (HIV-1) but not HIV-2, whilst the minor haplotype of TRIMCyp suppressed HIV-2 but not HIV-1. The major haplotype of TRIMCyp did not restrict a monkey-tropic HIV-1 clone, NL-DT5R, which contains a capsid with the simian immunodeficiency virus-derived loop between α-helices 4 and 5 and the entire vif gene. These results indicate that polymorphisms of TRIMCyp affect its anti-lentiviral activity. Overall, the results of this study will help our understanding of the genetic background of cynomolgus macaque TRIMCyp, as well as the host factors composing species barriers of primate lentiviruses.

Evolutionary patterns of killer cell Ig-like receptor genes in Old World monkeys

Killer cell Ig-like receptors (KIRs) modulate the cytotoxic effects of Natural Killer cells. KIR genes are encoded in the Leucocyte Receptor Complex and are characterized by their high haplotypic diversity and polymorphism. The KIR system has been studied in only three species of Old World monkeys, the rhesus macaque, the cynomolgus macaque, and the sabaeus monkey, displaying a complexity rivaling that of hominids (human and apes). Here we analyzed bacterial artificial chromosome draft sequences spanning the KIR haplotype of three other Old World monkeys, the vervet monkey ( Chlorocebus aethiops), the olive baboon ( Papio anubis) and the colobus monkey (Colobus guereza). A total of 25 KIR gene models were identified in these species, predicted to encode receptors with 1, 2, and 3 extracellular Ig domains, all of them with long cytoplasmic domains having two putative ITIMs, although three had a positively charged residue in the transmembrane domain. Sequence and phylogenetic analyses showed that most Old World monkeys shared five classes of KIR loci: i) KIR2DL5/3DL20 in the most centromeric region, followed by ii) the single Ig domain-encoding locus KIR1D, iii) the pseudogene KIR2DP, iv) the conserved KIR2DL4, and v) the highly diversified KIR3DL/H loci in the telomeric half of the cluster. An exception to this pattern was the KIR haplotype of the colobus monkey that lacked the KIR1D, KIR2DP, and KIR2DL4 loci of the central region of the cluster. Thus, Old World monkeys display a broad spectrum of KIR haplotype variation that has been generated upon an ancestral haplotype architecture by gene duplication, gene deletion, and non-homologous recombination.

Chemical characterization of oligosaccharides in the milk of six species of New and Old world monkeys

Human and great ape milks contain a diverse array of milk oligosaccharides, but little is known about the milk oligosaccharides of other primates, and how they differ among taxa. Neutral and acidic oligosaccharides were isolated from the milk of three species of Old World or catarrhine monkeys (Cercopithecidae: rhesus macaque (Macaca mulatta), toque macaque (Macaca sinica) and Hamadryas baboon (Papio hamadryas)) and three of New World or platyrrhine monkeys (Cebidae: tufted capuchin (Cebus apella) and Bolivian squirrel monkey (Saimiri boliviensis); Atelidae: mantled howler (Alouatta palliata)). The milks of these species contained 6–8% total sugar, most of which was lactose: the estimated ratio of oligosaccharides to lactose in Old World monkeys (1:4 to 1:6) was greater than in New World monkeys (1:12 to 1:23). The chemical structures of the oligosaccharides were determined mainly by 1H-NMR spectroscopy. Oligosaccharides containing the type II unit (Gal(β1-4)GlcNAc) were found in the milk of the rhesus macaque, toque macaque, Hamadryas baboon and tufted capuchin, but oligosaccharides containing the type I unit (Gal(β1-3)GlcNAc), which have been found in human and many great ape milks, were absent from the milk of all species studied. Oligosaccharides containing Lewis x (Gal(β1-4)[Fuc(α1-3)]GlcNAc) and 3-fucosyl lactose (3-FL, Gal(β1-4)[Fuc(α1-3)]Glc) were found in the milk of the three cercopithecid monkey species, while 2-fucosyl lactose (5'-FL, Fuc(α1-2)Gal(β1-4)Glc) was absent from all species studied. All of these milks contained acidic oligosaccharides that had N-acetylneuraminic acid as part of their structures, but did not contain oligosaccharides that had N-glycolylneuraminic acid, in contrast to the milk or colostrum of great apes which contain both types of acidic oligosaccharides. Two GalNAc-containing oligosaccharides, lactose 3′-O-sulfate and lacto-N-novopentaose I (Gal(β1-3)[Gal(β1-4)GlcNAc(β1-6)]Gal(β1-4)Glc) were found only in the milk of rhesus macaque, hamadryas baboon and tufted capuchin, respectively. Further research is needed to determine the extent to which the milk oligosaccharide patterns observed among these taxa represent wider phylogenetic trends among primates and how much variation occurs among individuals or species.Electronic supplementary materialThe online version of this article (doi:10.1007/s10719-010-9315-0) contains supplementary material, which is available to authorized users.

Cercopithecine Herpesvirus 1 Risk in a Child Bitten by a Bonnet Macaque Monkey

Background: Exotic animal importation and trade has the potential to expose the public to a variety of injuries and diseases not endemic to the United States. Bonnet Macaque monkeys are a fairly common primate illegally held in captivity. These monkeys become aggressive as they age past 2 years and are known to carry asymptomatic Cercopithecine herpesvirus 1 infection. Objective: This case is presented to illustrate the point that simple wound management alone may not only be insufficient but could be fatal in certain exotic animal bites and that the emergency physician should consult with authorities familiar with exotic animals when treating a patient with an exotic animal bite. Case Report: We present the case of a 2-year-old child that was bitten by his neighbor's pet Bonnet Macaque monkey. This species of Old World monkey carries the Cercopithecine herpesvirus 1 (simian B virus) 73–100% of the time. This infection in humans can lead to an encephalitis that has a 70% mortality rate. Consultation with animal authorities led to the proper treatment, which included routine wound care, rabies prophylaxis, irrigation with sodium hypochlorite solution, and treatment with antiviral medication. Conclusion: Simple wound management alone may not be enough in patients bitten by exotic animals. Consultation with local zoo officials, veterinary medical schools, or the Centers for Disease Control and Prevention is recommended in these cases.

Sequence length polymorphisms within primate amelogenin and amelogenin‐like genes: usefulness in sex determination

Sequence length polymorphisms between the amelogenin (AMELX) and the amelogenin-like (AMELY) genes both within and between several mammalian species have been identified and utilized for sex determination, species identification, and to elucidate evolutionary relationships. Sex determination via polymerase chain reaction (PCR) assays of the AMELX and AMELY genes has been successful in greater apes, prosimians, and two species of old world monkeys. To date, no sex determination PCR assay using AMELX and AMELY has been developed for new world monkeys. In this study, we present partial AMELX and AMELY sequences for five old world monkey species (Mandrillus sphinx, Macaca nemestrina, Macaca fuscata, Macaca mulatta, and Macaca fascicularis) along with primer sets that can be used for sex determination of these five species. In addition, we compare the sequences we generated with other primate AMELX and AMELY sequences available on GenBank and discuss sequence length polymorphisms and their usefulness in sex determination within primates. The mandrill and four species of macaque all share two similar deletion regions with each other, the human, and the chimpanzee in the region sequenced. These two deletion regions are 176-181 and 8 nucleotides in length. In analyzing existing primate sequences on GenBank, we also discovered that a separate six-nucleotide polymorphism located approximately 300 nucleotides upstream of the 177 nucleotide polymorphism in sequences of humans and chimps was also present in two species of new world monkeys (Saimiri boliviensis and Saimiri sciureus). We designed primers that incorporate this polymorphism, creating the first AMELX and AMELY PCR primer set that has been used successfully to generate two bands in a new world monkey species.

Glycan stem-cell markers are specifically expressed by spermatogonia in the adult non-human primate testis

The glycan cell surface molecules, stage-specific embryonic antigen (SSEA)-1, -3 and -4 and tumor-rejection antigen (TRA)-1-60 and -1-81, are expressed in specific combinations by undifferentiated pluripotent cells, i.e. embryonic stem cells, induced pluripotent stem cells, embryonal carcinoma cells, primordial germ cells and embryonic germ cells. Upon differentiation of the cells, these markers vanish. Recently, it has been shown that also neonatal and adult mouse testes contain pluripotent cells. Here, we aimed at identifying in situ possibly pluripotent cells in the adult primate testis. Monoclonal antibodies raised against the glyco-epitopes SSEA-1, -3 and -4 and TRA-1-60 and -1-81, respectively, were tested to detect cells expressing the antigens, by immunohistochemistry on Bouin's-fixed and paraffin-embedded adult primate testes. Man, the new-world monkey, Callithrix jacchus (common marmoset), and the old-world monkey species, Macaca mulatta (Rhesus macaque) and Macaca silenus (Lion-tailed macaque), were included. The percentage of SSEA-4-positive cells in three adult marmoset testes was determined using flow cytometry. Spermatogonia in the testes of C. jacchus were labeled by SSEA-4, TRA-1-60 and -1-81-antibodies. In the macaques, spermatogonia were detected by SSEA-4 and TRA-1-81-antibodies. TRA-1-61 did not bind to macaque spermatogonia. Also, SSEA-1 and -3 did not bind to spermatogonia in any species. In human testes, we never obtained any clear staining. The total percentage of SSEA-4-positive cells in marmoset testes was 8.6 +/- 1.61%. SSEA-4 and TRA-1-81-antibodies may be very well suited for the identification and isolation of spermatogonia, and possibly also germline stem cells, in the non-human primate testis.

The Gene of Retroviral Origin Syncytin 1 is Specific to Hominoids and is Inactive in Old World Monkeys

Syncytin 1 is one of the best known examples of recent acquisition of a new gene from an endogenous retrovirus (HERV) in the human genome and has been implicated in placental physiology. Within primates, Syncytin 1 is conserved in all hominoids but has not been characterized in Old World monkeys (OWMs). In this study, we investigated the status of Syncytin 1 in 14 hominoid and OWM species. We show that although the HERV-W provirus responsible for the origin of this gene was present in the genome of the most recent common ancestor of hominoids and OWMs, Syncytin 1 is inactive in OWMs. In addition, we were able to determine that the evolution of Syncytin 1 in hominoids involved an accumulation of amino acid changes and showed signatures of both positive and purifying selection. Our results indicate that Syncytin 1 is indeed a hominoid-specific gene and illustrate the complex and dynamic process associated with the origin of new genes.

The evolution of female copulation calls in primates: a review and a new model

Female copulation calls are mating-associated vocalizations that occur in some species of Old World monkeys and apes. We argue that copulation calls have two immediate functions: to encourage mating attempts by other males and to increase mate guarding by the consort male. We hypothesize that female copulation calls have evolved under the selective pressures of risk of infanticide and sperm competition. When male mate guarding is effective, copulation calls allow females to concentrate paternity in dominant males and benefit from their protection against the risk of infanticide. When mate guarding is ineffective, copulation calls may bring genetic benefits to females through facilitation of sperm competition. We present a quantitative model in which interspecific variation in females' promiscuity predicts their tendency to use copulation calls in conjunction with mating. The model predicts that in species with little female promiscuity, copulation calls should be rare and exhibited only in association with mating with dominant males. In species in which females are highly promiscuous, copulation calls should be frequent and unrelated to male dominance rank. The limited data available to test the model support its main predictions as well as the predicted relation between copulation calls and male dominance rank.

Molecular evolution of growth hormone gene family in old world monkeys and hominoids

Growth hormone is a classic molecule in the study of the molecular clock hypothesis as it exhibits a relatively constant rate of evolution in most mammalian orders except primates and artiodactyls, where dramatically enhanced rate of evolution (25–50-fold) has been reported. The rapid evolution of primate growth hormone occurred after the divergence of tarsiers and simians, but before the separation of old world monkeys (OWM) from new world monkeys (NWM). Interestingly, this event of rapid sequence evolution coincided with multiple duplications of the growth hormone gene, suggesting gene duplication as a possible cause of the accelerated sequence evolution. Here we determined 21 different GH-like sequences from four species of OWM and hominoids. Combining with published sequences from OWM and hominoids, our analysis demonstrates that multiple gene duplications and several gene conversion events both occurred in the evolutionary history of this gene family in OWM/hominoids. The episode of recent duplications of CSH-like genes in gibbon is accompanied with rapid sequence evolution likely resulting from relaxation of purifying selection. GHN genes in both hominoids and OWM are under strong purifying selection. In contrast, CSH genes in both lineages are probably not. GHV genes in OWM and hominoids evolved at different evolutionary rates and underwent different selective constraints. Our results disclosed the complex history of the primate growth hormone gene family and raised intriguing questions on the consequences of these evolutionary events.

Serum Leptin in Nonpregnant and Pregnant Women and in Old and New World Nonhuman Primates

Leptin is a hormone that is produced during mammalian pregnancy in the placental trophoblast and other tissues, including! fetal and maternal adipocytes. Synthesis of the polypeptide and the presence of its specific receptors throughout the human maternal fetoplacental unit suggest direct effects on conceptus growth and development. However, both the physiologic roles of leptin and the mechanisms regulating leptin synthesis in human pregnancy differ from those in laboratory and domestic species, necessitating the development of non-human primate research models. Therefore, we compared serum leptin concentrations in nonpregnant and pregnant women with those in both old world nonhuman primates (i.e., baboon, rhesus monkey, cynomolgus monkey) and new world nonhuman primates (i.e., squirrel monkey, titi monkey). As expected, maternal leptin levels were elevated in human and baboon pregnancies (P < 0.05 and P < 0.001, respectively). Levels in both species of old world monkeys were also greatly enhanced (P < 0.001). Although maternal serum concentrations were slightly elevated compared to nonpregnant levels in both species of new world monkeys, overall concentrations were dramatically lower than for either old world primates or humans. Results provide comparisons of serum leptin concentrations in pregnant and nonpregnant humans and baboons with those in both old and new world monkeys and further characterize these nonhuman primates as models for the investigation of leptin dynamics in pregnancy.

Vpu-mediated CD4 down-regulation and degradation is conserved among highly divergent SIV cpz strains

Human immunodeficiency virus type 1 (HIV-1) along with simian immunodeficiency viruses from chimpanzees (SIV cpz) and three species of Old World monkeys from the genus Cercopithecus have been shown to encode a Vpu protein. To date, the functional characterization of Vpu has been limited to a small number of subtype B and more recently subtype C Vpu proteins. Using a recently developed VpuEGFP reporter system, we have shown that the subtype B and C Vpus are capable of preventing CD4 from being expressed on the cell surface. Using the same reporter system, we report here on the expression and functional analysis of Vpu protein from four SIV cpz isolates (CAM13, ANT, TAN1, and GAB1). All four SIV Vpu fusion proteins were efficiently expressed and prevented CD4 expression on the cell surface and induced CD4 degradation. This was surprising as three of the SIV cpz Vpu fusion proteins had only one canonical casein kinase II (CK-II) site (CAM13, ANT, TAN1) while previous studies with laboratory adapted HXB2 had indicated that both CK-II sites were required for CD4 degradation. Both ANT and TAN1 Vpu sequences encoded five consecutive negatively charged amino acids residues following the only CKII site ( SAIEEDEE for ANT; SGVEEDEE for TAN1). We thus explored the possibility that this stretch of negatively charged amino acids might substitute for the lack of second CK-II site. Substitution of the aspartic acid at position 61 and glutamic acid at position 63 in the SIV cpz ANT Vpu within with lysine residues abolished the ability of this protein to down-modulate cell surface expression of CD4. Similarly, change of a serine to an alanine residue following the single consensus CK-II site of the CAM13 Vpu ( SGNESDGGEEE) abolished CD4-down-regulation, suggesting that this serine was phosphorylated in the absence of a canonical CK-II site. Our results indicate that the serine was required, suggesting that this serine was phosphorylated by CK-II or possibly another cellular kinase. Taken together, these results show for the first time that Vpu proteins from SIV cpz isolates, although quite diverse in sequence and predicted secondary structure from the HIV-1 subtype B protein, are capable of down-regulating CD4, which is one of the major functions of the HIV-1 protein.

Maintenance of above-branch balance during primate arboreal quadrupedalism: Coordinated use of forearm rotators and tail motion

Animals that live and travel in trees display a variety of morphological and behavioral adaptations to help them maintain balance on narrow flexible supports. Among these adaptations are long tails that can be used as counterweights, and freely mobile limbs in order to reach discontinuous supports. Here we describe two additional ways in which these features can contribute to balance during arboreal locomotion. Electromyographic (EMG) recordings of the forearm rotators pronator quadratus and supinator during over-ground and above-branch quadrupedal locomotion in five species of Old World monkeys revealed their contribution to shifting the weight of the body to help change the direction of travel and maintain balance on a branch. In addition, we observed a coordinated mechanism consisting of a sweeping tail rotation toward the direction of imbalance, to impart an angular momentum to the body that assists in the restoration of balance. While all five primate species utilized forearm rotators to shift their bodies toward one side or the other during quadrupedal walking along a branch, the tail-whip mechanism was most frequently used by the largest and most terrestrial species. We suggest that their large size and/or terrestrial habits have made them less adept at arboreal locomotion, and therefore most likely to utilize auxiliary balancing mechanisms. The usefulness of a long tail as a balancing aid during arboreal locomotion highlights the puzzling nature of the evolutionary loss of a tail in the ape and human lineage.

Honest signaling of intentions: the importance of performance risk, receiver response, and prior knowledge of opponents in the threat displays of mandrills

Honest signaling of intentions was initially rejected by evolutionary game theory because it was believed to be susceptible to cheating mutants. In theory, however, conditions may exist that enable this type of signaling to remain evolutionarily stable. Two such conditions have been proposed: (1) signaling may entail performance risks by making the sender vulnerable to attack ('vulnerability handicap' model), or (2) individuals may recognize one another, remember the outcome of past interactions, and interact repeatedly ('individual recognition' model). In this paper, I tested predictions deriving from both models by analyzing behavioural sequences involving threats in a species of Old World monkey (Mandrillus sphinx). The results were consistent with the individual recognition model. Subordinates (judged competitively inferior based on approach-avoid interactions) rarely elicited favorable responses with their threats, which were generally ignored. In addition, the honesty of dominants was frequently tested since subordinates responded favorably to dominants' threats less than half the time. When dominants experienced unfavorable responses to their threats they were significantly more likely to direct further aggression at the subordinate, thus demonstrating an honest commitment to the conflict. The results did not support the vulnerability handicap model since receiver retaliation against threats was essentially nonexistent. Though in partial support of the vulnerability handicap model (a) riskier threats were more effective, and (b) senders were less likely to perform the riskiest threats against more dominant individuals. In primates and other animals that live in long-term, stable groups, individual recognition may be especially important in maintaining honest signaling of intentions. Vulnerability handicaps, however, could also play a role in maintaining honesty in such species, but primarily during interactions between unfamiliar individuals that are transferring groups, or during dominance reversals.

Can simple rules account for the pattern of triadic interactions in juvenile and adult female sooty mangabeys?

Several experimental and observational studies have investigated the pattern of triadic relationships in primates to demonstrate knowledge of third-party relationships (i.e. an individual recognizes the relationship that exists between two others). To date, all studies have investigated the recognition of third-party relationships in adult animals. Thus, we do not know whether juveniles have knowledge of third-party rank relationships or whether they use a set of simple rules until they learn the rank relationships of all animals within a group. Here, we present the first data on triadic interactions involving juveniles in a rainforest primate, the sooty mangabey, Cercocebus torquatus atys. In a group of 120 individuals, we found that (1) if two groomers were approached by an individual ranking higher than both, the higher-ranking member of the grooming dyad was significantly more likely to stay than the lower-ranking one; (2) when an animal intervened in a conflict, juveniles and adult females were significantly more likely to support the higher-ranking contestant; and (3) juveniles and females solicited help in conflicts significantly more often from potential allies that outranked them and their target than from allies that ranked below them and/or the opponent. Our results suggest that the triadic interactions of juvenile sooty mangabeys resemble triadic interactions reported for adult members of other species of Old World monkeys, but that most of the observed behaviour patterns could be explained by a set of simple rules instead of invoking higher cognitive abilities.