[Show abstract][Hide abstract] ABSTRACT: Kin selection theory provides a strong theoretical framework to explain the evolution of altruism and cooperative behaviour among genetically related individuals. However, the proximate mechanisms underlying kin discrimination, a necessary process to express kin-related behaviour, remain poorly known. In particular, no study has yet unambiguously disentangled mechanisms based on learned familiarity from true phenotype matching in kin discrimination based on vocal signals. Here we show that in addition to genetic background, social accommodation also shapes individual voices in an Old World monkey (Mandrillus sphinx), even though primate vocalizations were thought to be innate and little flexible. Nonetheless, social shaping of voice parameters does not impair kin discrimination through phenotype-matching of unknown relatives, revealing unexpected discriminatory versatility despite signal complexity. Accurate signal production and perception, therefore, provide a basis for kin identification and kin-biased behaviour in an Old World primate.
[Show abstract][Hide abstract] ABSTRACT: Mandrill is a vulnerable Old World primate living in the rain-forests of central Africa. This species is currently facing two major human encroachments: habitat destruction and bush-meat trade. The total population size remains unknown in the wild, but it is suspected to have recently declined. We developed and characterized 24 new polymorphic microsatellite markers from the next-generation sequencing data using 66 individuals from a wild population. The number of alleles per locus ranged from 2 to 9 and the observed heterozygosity from 0.12 to 0.92. Conveniently, the developed markers did not amplify human DNA avoiding cross-species contamination. These microsatellites will be especially useful for studies based on sensible DNA, including population genetics analyses to studies in behavioral ecology.
[Show abstract][Hide abstract] ABSTRACT: High social rank is expected to incur fitness costs under unstable social conditions. A disruption of the oxidative balance may underlie such effects, but how markers of oxidative stress vary in relation to social rank and stability is unknown. We examined in mandrills whether the mating season characterized by social instability between males (but not between females) affected their oxidative balance differently according to their social rank. Outside the mating season, high-ranking males showed the lowest levels of oxidative damage, while during the mating season, they were the only males to experience increased oxidative damage. In contrast, in females, the mating season increased oxidative stress for all of them, irrespective of their social rank. These results support the hypothesis that the coupling between social rank and social stability is responsible for differential costs in terms of oxidative stress, which may explain inter-individual differences in susceptibility to socially-induced health issues.
[Show abstract][Hide abstract] ABSTRACT: Tooth wear in primates is caused by aging and ecological factors. However, comparative data that would allow us to delineate the contribution of each of these factors are lacking. Here, we contrast age-dependent molar tooth wear by scoring percent of dentine exposure (PDE) in two wild African primate populations from Gabonese forest and Kenyan savanna habitats. We found that forest-dwelling mandrills exhibited significantly higher PDE with age than savanna yellow baboons. Mandrills mainly feed on large tough food items, such as hard-shell fruits, and inhabit an ecosystem with a high presence of mineral quartz. By contrast, baboons consume large amounts of exogenous grit that adheres to underground storage organs but the proportion of quartz in the soils where baboons live is low. Our results support the hypothesis that not only age but also physical food properties and soil composition, particularly quartz richness, are factors that significantly impact tooth wear. We further propose that the accelerated dental wear in mandrills resulting in flatter molars with old age may represent an adaptation to process hard food items present in their environment.
PLoS ONE 04/2014; 9(4):e94938. DOI:10.1371/journal.pone.0094938 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The aggression animals receive from conspecifics varies between individuals across their lifetime. As poignantly evidenced by infanticide, for example, aggression can have dramatic fitness consequences. Nevertheless, we understand little about the sources of variation in received aggression, particularly in females. Using a female-dominant species renowned for aggressivity in both sexes, we tested for potential social, demographic, and genetic patterns in the frequency with which animals were wounded by conspecifics. Our study included 243 captive, ring-tailed lemurs (Lemur catta), followed from infancy to adulthood over a 35-year time span. We extracted injury, social, and life-history information from colony records and calculated neutral heterozygosity for a subset of animals, as an estimate of genetic diversity. Focusing on victims rather than aggressors, we used General Linear Models to explain bite-wound patterns at different life stages. In infancy, maternal age best predicted wounds received, as infants born to young mothers were the most frequent infanticide victims. In adulthood, sex best predicted wounds received, as males were three times more likely than females to be seriously injured. No relation emerged between wounds received and the other variables studied. Beyond the generally expected costs of adult male intrasexual aggression, we suggest possible additive costs associated with female-dominant societies - those suffered by young mothers engaged in aggressive disputes and those suffered by adult males aggressively targeted by both sexes. We propose that infanticide in lemurs may be a costly by-product of aggressively mediated, female social dominance. Accordingly, the benefits of female behavioral 'masculinization' accrued to females through priority of access to resources, may be partially offset by early costs in reproductive success. Understanding the factors that influence lifetime patterns of conspecific wounding is critical to evaluating the fitness costs associated with social living; however, these costs may vary substantially between societies.
PLoS ONE 12/2013; 8(12):e82830. DOI:10.1371/journal.pone.0082830 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: The evolution of paternal care is rare in promiscuous mammals, where it is hampered by low paternity confidence. However, recent evidence indicates that juveniles whose fathers are present experience accelerated maturation in promiscuous baboon societies. The mechanisms mediating these paternal effects remain unclear. Here, we investigated whether father–offspring associations might facilitate offspring access to resources in wild desert baboons (Papio ursinus). We combined paternity analyses and behavioral observations of juveniles that had started feeding autonomously to show that (1) offspring associate more often with their genetic father than with any other male, and actively manage such associations, (2) offspring associate more closely with their father when another adult male is in sight, and when their mother is out of sight, (3) father–offspring associations are more frequent when juveniles are feeding (relative to other activities), and these associations enable juveniles to access richer food patches, and (4) father–offspring associations are stronger among subordinate males and their offspring. Taken together, these findings indicate that fathers may buffer the social and ecological environment faced by their offspring. In addition to mitigating risks of attacks by predators or conspecifics, paternal presence improves offspring access to food in wild baboons, highlighting a new mechanism through which fathers may impact offspring fitness in promiscuous primate societies.
[Show abstract][Hide abstract] ABSTRACT: Multimale–multifemale primate groups are ideal models to study the impact of kinship on the evolution of sociality. Indeed, the frequent combination of female philopatry and male reproductive skew produces social systems where both maternal and paternal kin are co‐resident. Several primates are known to bias their behavior toward both maternal and paternal kin. Moreover, allocation of affiliation toward paternal kin has been shown to depend on the availability in maternal kin: Female baboons invest more in paternal kin after the loss of preferred maternal kin. Here, we examined how affiliation co‐varies across kin classes in juvenile mandrills (Mandrillus sphinx), an Old World primate living in a multimale–multifemale society. While affiliation levels observed with the mother and with maternal half‐sibs co‐varied positively, especially in young females, we found that levels of affiliation among paternal half‐sibs correlated negatively with levels of affiliation among individuals from the same matriline (distant kin), possibly as a result of kin availability. In addition, in social species, social bonds between individuals have been linked to differentiated fitness consequences: More socially integrated individuals generally enjoy higher fitness. We therefore also tested whether affiliation during early life impacts fitness. We showed that the global amount of affiliation during juvenescence translated into possible reproductive benefits: Females who were more socially integrated gave birth on average a year before females that were less socially integrated. However, age at first reproduction was not predicted by the amount of affiliation exchanged with any particular kin class. These results add to the growing body of evidence demonstrating differential investment in bonding and possible social adjustments among different kin categories and emphasizing once more the adaptive value of sociality.
[Show abstract][Hide abstract] ABSTRACT: 1. Sophisticated and sensitive technologies now allow separation, quantification and chemical characterization of numerous compounds that play roles in chemical communication, chemical defence and aggression, in interactions between conspecific or heterospecific individuals. In the particular subfield of mammalian chemical communication, these rapid technological advances, combined with a frequent lack of technical background, have led to important errors in both chemical characterization of molecules and interpretation of their roles as chemical mediators of communication. 2. The aim of this article is to highlight some of these methodological and analytical pitfalls and to provide a basis for better understanding of chemical mediation of communication in mammals. We compiled the recent literature treating molecules found in mammalian secretions and having putative roles in communication. A selection of 41 published studies dealing with 33 mammal species revealed reports of 857 different molecules. Based on the five main metabolic pathways responsible for the biosynthesis of most known secondary metabolites, we propose nine general biochemical rules that will help researchers to avoid errors of chemical characterization and to aid in interpreting the possible functional role of identified molecules as chemical mediators of mammal communication. 3. Following these nine rules, we show that published studies include reports of molecules that are incorrectly or ambiguously named, molecules of exclusively non-natural origin, molecules produced by other organisms but not directly by mammals, and molecules of biological origin and possibly produced by mammals. Only the last two of these classes could conceivably play roles as mediators of mammalian communication. We discuss the potential roles of these compounds as reported in the publications we reviewed. 4. Our recommendations concerning technical, analytical and statistical aspects of the identification of compounds and interpretation of their roles should help chemical ecologists ask the appropriate questions about the accuracy of their identifications of molecules, the biological relevance of molecules they do identify and the possible functional roles of these molecules in mammalian communication.
[Show abstract][Hide abstract] ABSTRACT: Mating behavior has profound consequences for two phenomena--individual reproductive success and the maintenance of species boundaries--that contribute to evolutionary processes. Studies of mating behavior in relation to individual reproductive success are common in many species, but studies of mating behavior in relation to genetic variation and species boundaries are less commonly conducted in socially complex species. Here we leveraged extensive observations of a wild yellow baboon (Papio cynocephalus) population that has experienced recent gene flow from a close sister taxon, the anubis baboon (Papio anubis), to examine how admixture-related genetic background affects mating behavior. We identified novel effects of genetic background on mating patterns, including an advantage accruing to anubis-like males and assortative mating among both yellow-like and anubis-like pairs. These genetic effects acted alongside social dominance rank, inbreeding avoidance, and age to produce highly nonrandom mating patterns. Our results suggest that this population may be undergoing admixture-related evolutionary change, driven in part by nonrandom mating. However, the strength of the genetic effect is mediated by behavioral plasticity and social interactions, emphasizing the strong influence of social context on mating behavior in socially complex species.
The American Naturalist 07/2012; 180(1):113-29. DOI:10.1086/665993 · 4.45 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Behaviour and genetic structure are intimately related: mating patterns and patterns of movement between groups or populations influence the movement of genetic variation across the landscape and from one generation to the next. In hybrid zones, the behaviour of the hybridizing taxa can also impact the incidence and outcome of hybridization events. Hybridization between yellow baboons and anubis baboons has been well documented in the Amboseli basin of Kenya, where more anubis-like individuals tend to experience maturational and reproductive advantages. However, it is unknown whether these advantages are reflected in the genetic structure of populations surrounding this area. Here, we used microsatellite genotype data to evaluate the structure and composition of baboon populations in southern Kenya. Our results indicate that, unlike for mitochondrial DNA, microsatellite-based measures of genetic structure concord with phenotypically based taxonomic distinctions and that the currently active hybrid zone is relatively narrow. Isolation with migration analysis revealed asymmetric gene flow in this region from anubis populations into yellow populations, in support of the anubis-biased phenotypic advantages observed in Amboseli. Populations that are primarily yellow but that receive anubis gene flow exhibit higher levels of genetic diversity than yellow populations far from the introgression front. Our results support previous work that indicates a long history of hybridization and introgression among East African baboons. Specifically, it suggests that anubis baboons are in the process of gradual range expansion into the range of yellow baboons, a pattern potentially explained by behavioural and life history advantages that correlate with anubis ancestry.
[Show abstract][Hide abstract] ABSTRACT: Multicomponent signals consist of several traits that are perceived as a whole. Although many animals rely on multicomponent signals to communicate, the selective pressures shaping these signals are still poorly understood. Previous work has mainly investigated the evolution of multicomponent signals by studying each trait individually, which may not accurately reflect the selective pressures exerted by the holistic perception of signal receivers. Here, we study the design of the multicoloured face of an Old World primate, the mandrill (Mandrillus sphinx), in relation to two aspects of signalling that are expected to be selected by receivers: conspicuousness and information. Using reflectance data on the blue and red colours of the faces of 34 males and a new method of hue vectorisation in a perceptual space of colour vision, we show that the blue hue maximises contrasts to both the red hue and the foliage background colouration, thereby increasing the conspicuousness of the whole display. We further show that although blue saturation, red saturation and the contrast between blue and red colours are all correlated with dominance, dominance is most accurately indicated by the blue-red contrast. Taken together our results suggest that the evolution of blue and red facial colours in male mandrills are not independent and are likely driven by the holistic perception of conspecifics. In this view, we propose that the multicoloured face of mandrills acts as a multicomponent signal. Last, we show that information accuracy increases with the conspicuousness of the whole display, indicating that both aspects of signalling can evolve in concert.
PLoS ONE 12/2011; 6(12):e29117. DOI:10.1371/journal.pone.0029117 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: To enhance the fitness benefits of social and sexual interaction, animals should be able to decipher information about the genetic makeup of conspecifics. The use of relative criteria to estimate genetic relatedness could facilitate nepotism or inbreeding avoidance, and the use of absolute criteria to estimate genetic quality could help identify the fittest competitor or the best mate. For animals to process trade-offs between relatedness and quality, however, both relative and absolute genetic information must be concurrently available and detectable by conspecifics. Although there is increasing evidence to suggest that animals make genetically informed decisions about their partners, and may even process trade-offs, we understand relatively little about the sensory mechanisms informing these decisions. In previous analyses of the olfactory signals of ringtailed lemurs, Lemur catta, we showed that both scrotal and labial secretions seasonally encode chemical information about (1) pairwise genetic relatedness, within and between the sexes, and (2) individual heterozygosity. Here, using a signaller–receiver paradigm, we conducted behavioural bioassays to test whether male and female lemurs are sensitive to these olfactory sources of genetic information in unfamiliar conspecifics. As the lemurs discriminated conspecific glandular secretions by pairwise relatedness and individual heterozygosity, volatile olfactory signals can be used by both sexes to concurrently process relative and absolute genetic information about conspecifics. Beyond supporting an olfactory mechanism of kin discrimination and mate choice in a primate, we suggest that animals could use olfactory processing to trade off between selection for the most compatible partner versus the most genetically diverse partner.
[Show abstract][Hide abstract] ABSTRACT: Sexual selection theory predicts that potential mates or competitors signal their quality to conspecifics. Whereas evidence of honest visual or vocal signals in males abounds, evidence of honest signalling via scent or by females is scarce. We previously showed that scent marks in male lemurs seasonally encode information about individual heterozygosity - a reliable predictor of immunocompetence and survivorship. As female lemurs dominate males, compete over resources, and produce sexually differentiated scent marks that likely evolved via direct selection, here we tested whether females also advertise genetic quality via olfactory cues. During the breeding season specifically, individual heterozygosity correlated negatively with the diversity of fatty acids (FAs) expressed in labial secretions and positively with the diversity of heavy FA esters. As odour-gene relationships predictive of health and survivorship emerged during a period critical to mate choice and female competition, we posit that genital scent marks function as honest olfactory ornaments in females.
[Show abstract][Hide abstract] ABSTRACT: Although many primates exhibit striking coloration, including brightly colored pelage and bare areas of skin, our understanding
of the function and evolution of these traits pales in the face of knowledge about color in other taxa. However, recent years
have seen an increase in the number of studies of individual variation in primate color and evidence is accumulating that
these traits can act as important signals to conspecifics. Mandrills are arguably the most colorful of all primates. Here,
we review what we have discovered about the signal function of coloration in male and female mandrills from our long-term
studies of a semi-free-ranging colony in Franceville, Gabon and test the predictions of the Hamilton-Zuk hypothesis—that bright
coloration is condition dependent, and that only individuals of superior quality will be able to express color fully—in this
species. We compare measures of facial coloration in both sexes with parasite load (using fecal analysis over 1 annual cycle),
immune status (hematological parameters), neutral genetic diversity (microsatellite heterozygosity), and major histocompatability
(MHC) genotype to examine whether red coloration acts as an honest signal of individual quality in mandrills. We found that
red coloration was unrelated to parasitism and hematological parameters. Red was also unrelated to genome-wide heterozygosity
and MHC diversity, although specific MHC genotypes were significantly related to red. The healthy, provisioned nature of the
colony and problems associated with observational, correlational studies restrict interpretation of our data, and it would
be premature to draw conclusions as to whether color signals individual quality in mandrills. We conclude with some suggestions
for future studies on the signal content of color in mandrills and other primates.
International Journal of Primatology 12/2009; 30(6):825-844. DOI:10.1007/s10764-009-9371-0 · 1.99 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Like other vertebrates, primates recognize their relatives, primarily to minimize inbreeding, but also to facilitate nepotism. Although associative, social learning is typically credited for discrimination of familiar kin, discrimination of unfamiliar kin remains unexplained. As sex-biased dispersal in long-lived species cannot consistently prevent encounters between unfamiliar kin, inbreeding remains a threat and mechanisms to avoid it beg explanation. Using a molecular approach that combined analyses of biochemical and microsatellite markers in 17 female and 19 male ring-tailed lemurs (Lemur catta), we describe odor-gene covariance to establish the feasibility of olfactory-mediated kin recognition.
Despite derivation from different genital glands, labial and scrotal secretions shared about 170 of their respective 338 and 203 semiochemicals. In addition, these semiochemicals encoded information about genetic relatedness within and between the sexes. Although the sexes showed opposite seasonal patterns in signal complexity, the odor profiles of related individuals (whether same-sex or mixed-sex dyads) converged most strongly in the competitive breeding season. Thus, a strong, mutual olfactory signal of genetic relatedness appeared specifically when such information would be crucial for preventing inbreeding. That weaker signals of genetic relatedness might exist year round could provide a mechanism to explain nepotism between unfamiliar kin.
We suggest that signal convergence between the sexes may reflect strong selective pressures on kin recognition, whereas signal convergence within the sexes may arise as its by-product or function independently to prevent competition between unfamiliar relatives. The link between an individual's genome and its olfactory signals could be mediated by biosynthetic pathways producing polymorphic semiochemicals or by carrier proteins modifying the individual bouquet of olfactory cues. In conclusion, we unveil a possible olfactory mechanism of kin recognition that has specific relevance to understanding inbreeding avoidance and nepotistic behavior observed in free-ranging primates, and broader relevance to understanding the mechanisms of vertebrate olfactory communication.
[Show abstract][Hide abstract] ABSTRACT: Fecal glucocorticoid (fGC) concentrations are reliable, non-invasive indices of physiological stress that provide insight into an animal's energetic and social demands. To better characterize the long-term stressors in adult members of a female-dominant, seasonally breeding species - the ring-tailed lemur (Lemur catta) - we first validated fecal samples against serum samples and then examined the relationship between fGC concentrations and seasonal, social, demographic, genetic, and reproductive variables. Between 1999 and 2006, we collected 1386 fecal samples from 32 adult, semi-free-ranging animals of both sexes. In males and non-pregnant, non-lactating females, fGC concentrations were significantly elevated during the breeding season, specifically during periods surrounding known conceptions. Moreover, group composition (e.g., multi-male versus one-male) significantly predicted the fGC concentrations of males and females in all reproductive states. In particular, the social instability introduced by intra-male competition likely created a stressor for all animals. We found no relationship, however, between fGC and the sex, age, or heterozygosity of animals. In reproducing females, fGC concentrations were significantly greater during lactation than during the pre-breeding period. During pregnancy, fGC concentrations were elevated in mid-ranking dams, relative to dominant or subordinate dams, and significantly greater during the third trimester than during the first or second trimesters. Thus, in the absence of nutritional stressors, social dominance was a relatively poor predictor of fGC in this female-dominant species. Instead, the animals were maximally challenged by their social circumstances and reproductive events-males by competition for mating opportunities and females by late-term gestation and lactation.
Hormones and Behavior 10/2009; 57(1):76-85. DOI:10.1016/j.yhbeh.2009.09.016 · 4.51 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: We investigated reproduction in a semi-free-ranging population of a polygynous primate, the mandrill, in relation to genetic relatedness and male genetic characteristics, using neutral microsatellite and major histocompatibility complex (MHC) genotyping. We compared genetic dissimilarity to the mother and genetic characteristics of the sire with all other potential sires present at the conception of each offspring (193 offspring for microsatellite genetics, 180 for MHC). The probability that a given male sired increased as pedigree relatedness with the mother decreased, and overall genetic dissimilarity and MHC dissimilarity with the mother increased. Reproductive success also increased with male microsatellite heterozygosity and MHC diversity. These effects were apparent despite the strong influence of dominance rank on male reproductive success. The closed nature of our study population is comparable to human populations for which MHC-associated mate choice has been reported, suggesting that such mate choice may be especially important in relatively isolated populations with little migration to introduce genetic variation.