Marie J. E. Charpentier

Pathogen-Driven Selection and Worldwide HLA Class I Diversity

The human leukocyte antigen (HLA; known as MHC in other vertebrates) plays a central role in the recognition and presentation of antigens to the immune system and represents the most polymorphic gene cluster in the human genome [1]. Pathogen-driven balancing selection (PDBS) has been previously hypothesized to explain the remarkable polymorphism in the HLA complex, but there is, as yet, no direct support for this hypothesis [2 and 3]. A straightforward prediction coming out of the PDBS hypothesis is that populations from areas with high pathogen diversity should have increased HLA diversity in relation to their average genomic diversity. We tested this prediction by using HLA class I genetic diversity from 61 human populations. Our results show that human colonization history explains a substantial proportion of HLA genetic diversity worldwide. However, between-population variation at the HLA class I genes is also positively correlated with local pathogen richness (notably for the HLA B gene), thus providing support for the PDBS hypothesis. The proportion of variations explained by pathogen richness is higher for the HLA B gene than for the HLA A and HLA C genes. This is in good agreement with both previous immunological and genetic data suggesting that HLA B could be under a higher selective pressure from pathogens.

Senescence rates are determined by ranking on the fast-slow life-history continuum

Comparative analyses of survival senescence by using life tables have identified generalizations including the observation that mammals senesce faster than similar-sized birds. These generalizations have been challenged because of limitations of life-table approaches and the growing appreciation that senescence is more than an increasing probability of death. Without using life tables, we examine senescence rates in annual individual fitness using 20 individual-based data sets of terrestrial vertebrates with contrasting life histories and body size. We find that senescence is widespread in the wild and equally likely to occur in survival and reproduction. Additionally, mammals senesce faster than birds because they have a faster life history for a given body size. By allowing us to disentangle the effects of two major fitness components our methods allow an assessment of the robustness of the prevalent life-table approach. Focusing on one aspect of life history - survival or recruitment - can provide reliable information on overall senescence.

Smelling right: the scent of male lemurs advertises genetic quality and relatedness

Sexual selection theory predicts that competitors or potential mates signal their quality or relatedness to conspecifics. Researchers have focused on visual or auditory modes of signal transmission; however, the importance of olfactory indicators is gaining recognition. Using a primate model and a new integrative analytical approach, we provide the first evidence relating male olfactory cues to individual genome‐wide heterozygosity and to the genetic distance between individuals. The relationships between male semiochemical profiles and genetic characteristics are apparent only during the highly competitive and stressful breeding season. As heterozygosity accurately predicts health and survivorship in this population, we identify scrotal olfactory cues as honest indicators of male quality, with relevance possibly to both sexes. Beyond showing that semiochemicals could underlie kin recognition and nepotism, we provide a putative olfactory mechanism to guide male–male competition and female mate choice.

Mate guarding and paternity in mandrills: factors influencing alpha male monopoly

We used long-term data on mate guarding and paternity in mandrills, Mandrillus sphinx, (1) to examine cycle day and cycle selection by males; (2) to examine associations between male rank, periovulatory mate guarding and paternity outcome; (3) to test the predictions of the priority-of-access model; and (4) to investigate factors influencing the ability of alpha males to monopolize females. Males mate-guarded on periovulatory days more than on other receptive days, and during conceptive cycles more than during nonconceptive cycles. Both periovulatory mate guarding and paternity outcome correlated significantly with male rank. Alpha males accounted for 94% of periovulatory mate guarding and 69% of paternity, confirming the existence of extremely high reproductive skew in this highly sexually dimorphic species. The fit of the observed distributions of mate guarding and paternity to predictions from the priority-of-access model was good, but in both cases the alpha males accounted for a greater proportion of reproduction than predicted. Mate guarding was a good predictor of paternity, but consistently overestimated the reproductive success of the alpha male. Splitting data into group-years revealed that the percentage of mate guarding by the alpha male decreased with increasing numbers of adult males, and the percentage of paternity decreased with increasing numbers of reproductive males (all postpubertal males). Furthermore, mate guarding became less effective as the number of reproductive males increased. We attribute this to the fact that only males aged 8 years or more mate-guarded, but that all males aged at least 3.8 years may sneak copulations, reducing the effectiveness of mate guarding and therefore reducing paternity concentration in the alpha male.

Age at maturity in wild baboons: genetic, environmental and demographic influences

The timing of early life‐history events, such as sexual maturation and first reproduction, can greatly influence variation in individual fitness. In this study, we analysed possible sources of variation underlying different measures of age at social and physical maturation in wild baboons in the Amboseli basin, Kenya. The Amboseli baboons are a natural population primarily comprised of yellow baboons (Papio cynocephalus) that occasionally hybridize with anubis baboons (Papio anubis) from outside the basin. We found that males and females differed in the extent to which various factors influenced their maturation. Surprisingly, we found that male maturation was most strongly related to the proportion of anubis ancestry revealed by their microsatellite genotypes: hybrid males matured earlier than yellow males. In contrast, although hybrid females reached menarche slightly earlier than yellow females, maternal rank and the presence of maternal relatives had the largest effects on female maturation, followed by more modest effects of group size and rainfall. Our results indicate that a complex combination of demographic, genetic, environmental, and maternal effects contribute to variation in the timing of these life‐history milestones.

Message ‘scent’: lemurs detect the genetic relatedness and quality of conspecifics via olfactory cues

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.

Paternal effects on offspring fitness in a multimale primate society

When females mate with multiple males, paternal care is generally expected to be negligible, because it may be difficult or impossible for males to discriminate their own offspring from those of other males, and because engaging in paternal care may reduce male mating opportunities. Consequently, males in multimale societies are not predicted to provide direct benefits to their offspring. We have recently demonstrated, however, that males in a typical multimale primate society (yellow baboons, Papio cynocephalus) discriminate their own offspring from those of other males and provide care to them in the form of repeated support during agonistic encounters. This observation raises the question of whether fathers enhance offspring fitness in this species. Here we use 30 years of data on age at maturity for 118 yellow baboons with known fathers. We show that the fathers presence in the offsprings social group during the offsprings immature period accelerated the timing of physiological maturation in daughters. Sons also experienced accelerated maturation if their father was present during their immature period, but only if the father was high ranking at the time of their birth. Because age at reproductive maturity has a large impact on lifetime reproductive success, our results indicate a direct effect of paternal presence on offspring fitness. This relationship in turn suggests that the multiple roles that males play in multimale animal societies have not been sufficiently examined or appreciated and that paternal effects may be more pervasive than previously appreciated.

Kin discrimination in juvenile mandrills, Mandrillus sphinx

Kin selection theory predicts that the evolution of social behaviours will be promoted if these behaviours increase the inclusive fitness of the individuals that perform them, for example by positively affecting relatives. The ability to identify relatives may thus be crucial in maximizing overall fitness. In primate species, whether individuals discriminate paternal relatives and the mechanisms that might permit such discrimination are still the subject of debate. Some researchers have suggested that primates are not able to discriminate relatives in the absence of familiarity. However, recent studies have shown that paternal kin discrimination could emerge from both age proximity and phenotype matching. We investigated the effects of paternal and maternal kinship on the affiliation index of juvenile mandrills, in a semifree-ranging setting. Juveniles biased their behaviour according to kinship. First, when interacting with adult females, both paternal and maternal half-siblings showed more affiliation than unrelated dyads. Affiliation between juveniles and males was also higher among both father–offspring and maternal half-sibling dyads than among unrelated dyads. While these results suggest that juvenile mandrills are able to discriminate paternal relatives, other results do not. Maternal half-siblings had a higher affiliation index than paternal half-siblings and distant kin, the latter showing no significant differences. Finally, when the mechanisms involved in discrimination of paternal kin were analysed, we found no evidence to confirm either the phenotype-matching or the age proximity hypotheses.

Decoding an olfactory mechanism of kin recognition and inbreeding avoidance in a primate

BackgroundLike 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.ResultsDespite 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.ConclusionWe 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 individuals 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.

Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population

The process and consequences of hybridization are of interest to evolutionary biologists because of the importance of hybridization in understanding reproductive isolation, speciation, and the influence of introgression on population genetic structure. Recent studies of hybridization have been enhanced by the advent of sensitive, genetic marker‐based techniques for inferring the degree of admixture occurring within individuals. Here we present a genetic marker‐based analysis of hybridization in a large‐bodied, long‐lived mammal over multiple generations. We analysed patterns of hybridization between yellow baboons (Papio cynocephalus) and anubis baboons (Papio anubis) in a well‐studied natural population in Amboseli National Park, Kenya, using genetic samples from 450 individuals born over the last 36 years. We assigned genetic hybrid scores based on genotypes at 14 microsatellite loci using the clustering algorithm implemented in structure 2.0, and assessed the robustness of these scores by comparison to pedigree information and through simulation. The genetic hybrid scores showed generally good agreement with previous morphological assessments of hybridity, but suggest that genetic methods may be more sensitive for identification of low levels of hybridity. The results of our analysis indicate that the proportion of hybrids in the Amboseli population has grown over time, but that the average proportion of anubis ancestry within hybrids is gradually decreasing. We argue that these patterns are probably a result of both selective and nonselective processes, including differences in the timing of life‐history events for hybrid males relative to yellow baboon males, and stochasticity in long‐distance dispersal from the source anubis population into Amboseli.