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Female reproductive maturation is a critical life-history milestone, initiating an individual’s reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more “classic” socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas—a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to “faster” development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.

International audience; The causes and consequences of being in a particular dominance position have been illuminated in various animal species, and new methods to assess dominance relationships and to describe the structure of dominance hierarchies have been developed in recent years. Most research has focused on same-sex relationships, however, so that intersexual dominance relationships and hierarchies including both sexes have remained much less studied. In particular, different methods continue to be employed to rank males and females along a dominance hierarchy, and sex biases in dominance are still widely regarded as simple byproducts of sexual size dimorphism. However, males and females regularly compete over similar resources when living in the same group, and sexual conflict takes a variety of forms across Frontiers in Ecology and Evolution 01 frontiersin.org Kappeler et al. 10.3389/fevo.2022.918773 societies. These processes affect the fitness of both sexes, and are mitigated by intersexual hierarchies. In this study, we draw on data from free-ranging populations of nine species of mammals that vary in the degree to which members of one sex dominate members of the other sex to explore the consequences of using different criteria and procedures for describing intraand intersexual dominance relationships in these societies. Our analyses confirmed a continuum in patterns of intersexual dominance, from strictly male-dominated species to strictly female-dominated species. All indices of the degree of female dominance were well correlated with each other. The rank order among same-sex individuals was highly correlated between the intra-and intersexual hierarchies, and such correlation was not affected by the degree of female dominance. The relative prevalence of aggression and submission was sensitive to variation in the degree of female dominance across species, with more submissive signals and fewer aggressive acts being used in societies where female dominance prevails. Thus, this study provides important insights and key methodological tools to study intersexual dominance relationships in mammals.

Increasing evidence indicates that sexual coercion is widespread. While some coercive strategies are conspicuous, such as forced copulation or sexual harassment, less is known about the ecology and evolution of intimidation, where repeated male aggression promotes future rather than immediate mating success with targeted females. Although known in humans, intimidation was recently reported in chimpanzees (Pan troglodytes) and chacma baboons (Papio ursinus), where males are regularly violent against females. Here, we investigate the nature of male coercive strategies in wild mandrills (Mandrillus sphinx), a primate living in large polygynandrous groups where severe male aggression towards females is rare and females can form coalitions against males. Yet, we found support for all three predictions of the sexual coercion hypothesis, namely that male aggression (1) specifically targets sexually receptive females, (2) inflicts costs to these females, and (3) increases male mating success in the long-term. These results hold true when considering only non-physical threats, or only severe aggression. Finally, we show that high-ranking females are most targeted by males, probably because of their higher reproductive performances, while high-ranking males are most coercive. These results indicate that sexual intimidation is widespread in sexually dimorphic and group-living mammals, and that males and females vary in their propensities to use, and to be exposed to sexual coercion, respectively.

Mechanistic models suggest that individuals’ memories could shape home range patterns and dynamics, and how neighbors share space. In social species, such dynamics of home range overlap may be affected by the pre-dispersal memories of immigrants. We tested this “immigrant knowledge hypothesis” in a wild population of chacma baboons (Papio ursinus). We predicted that overlap dynamics with a given neighboring troop’s home range should reflect males’ adaptive interests in overlap when the alpha male had immigrated from this neighboring troop but less so when the alpha male originated from elsewhere. We used data collected between 2005 and 2013 on two neighboring troops in Namibia, comprising GPS records of daily ranges, male natal origins, daily females’ reproductive status, and a satellite index of vegetation growth. We found support for our prediction in line with male reproductive strategies but not in line with foraging conditions. In periods with a higher relative number of fertile females over adult males in the focal troop, male baboons would benefit from reducing overlap with their neighbors to mitigate the costs of between-troop mating competition. This was indeed observed but only when the alpha male of the focal troop was an immigrant from that neighboring troop, and not with alpha males of other origins, presumably due to their different knowledge of the neighboring troop. Our findings highlight the role of reproductive competition in the range dynamics of social groups, and suggest that spatial segregation between groups could increase through the combination of dispersal and memory.

Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

Early-life microbial colonization is an important process shaping host physiology

Animal reproductive phenology varies from strongly seasonal to non-seasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of non-seasonal breeding in seasonal environments. We investigated the evolutionary determinants of non-seasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that non-seasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favouring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals, and (ii) females delay their reproductive timings (fertility periods and conceptions) according to other females in the group to stagger conceptions. These results indicate that reproductive competition generates reproductive asynchrony, weakening the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in gregarious organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Background Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. Results Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas (Theropithecus gelada). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. Conclusion Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa.

The evolutionary benefits of reproductive seasonality are often measured by a single-fitness component, namely offspring survival. Yet different fitness components may be maximized by different birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons ( Papio ursinus ) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. We identify two distinct optimal birth timings in the annual cycle, located four-month apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother–offspring conflict. Maternal trade-offs over birth timing, which extend into mother–offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.

Reconciliation, or postconflict (PC) affiliation between former opponents, is a widespread conflict management strategy in animal societies, so-named for its relationship repair function. However, another possibility is that PC affiliation reflects a submissive response of victims towards aggressors to limit conflict escalation when the power imbalance between the opponents is large. Here we investigated this hypothesis in a highly asymmetric relationship context: heterosexual wild chacma baboon, Papio ursinus, dyads involving sexually receptive females, where sexual coercion by males is common. We found several lines of support for the submissive hypothesis in the context of sexual coercion. First, rates of sexual and nonsexual PC affiliative interactions in these dyads exhibited significant and comparable increases compared to baseline conditions (ca. three-fold). Second, the baseline strength of the heterosexual social bond (outside of an aggressive context) did not predict the likelihood of sexual and nonsexual PC affiliation. Third, mate-guarded females, who could not escape the proximity of their aggressor (and faced high risks of renewed aggression), exhibited the most PC affiliation with males. Finally, most PC affiliation sequences contained at least one sexual act, and the first sexual affiliative act was primarily initiated by females via presenting. This suggests that female victims affiliate in a submissive way by displaying sexual compliance to aggressive males. Nevertheless, we cannot exclude the co-occurrence of ‘true’ reconciliation: a quarter of PC affiliations between males and receptive females were exclusively nonsexual, and the first general affiliative act was equally initiated by males and females. Overall, our results suggest a mixed PC affiliation strategy in which submission may play an important role in highly asymmetric relationships and indicate that the function of PC affiliation may vary from submission to reconciliation depending on the species, dyads, individuals and conflicts under consideration. Future research on PC interactions would usefully consider this full spectrum.

OBJECTIVES: In many primates, one of the most noticeable morphological developmental traits is the transition from natal fur and skin color to adult coloration. Studying the chronology and average age at such color transitions can be an easy and noninvasive method to (a) estimate the age of infants whose dates of birth were not observed, and (b) detect interindividual differences in the pace of development for infants with known birth dates. MATERIALS AND METHODS: Using a combination of photographs and field observations from 73 infant chacma baboons (Papio ursinus) of known ages, we (a) scored the skin color of six different body parts from pink to gray, as well as the color of the fur from black to gray; (b) validated our method of age estimation using photographic and field observations on an independent subset of 22 infants with known date of birth; and (c) investigated ecological, social, and individual determinants of age-related variation in skin and fur color. RESULTS: Our results show that transitions in skin color can be used to age infant chacma baboons less than 7 months old with accuracy (median number of days between actual and estimated age = 10, range = 0-86). We also reveal that food availability during the mother's pregnancy, but not during lactation, affects infant color-for-age and therefore acts as a predictor of developmental pace. DISCUSSION: This study highlights the potential of monitoring within- and between-infant variation in color to estimate age when age is unknown, and developmental pace when age is known.

International audience; Male aggression towards females is a common and often costly occurrence in species that live in bisexual groups. But preferential heterosexual relationships are also known to confer numerous fitness advantages to both sexes—making it of interest to explore how aggression is managed among male–female dyads through strategies like reconciliation (i.e. postconflict affiliative reunions between former opponents). In this study, we build on the traditional postconflict matched-control (PC-MC), time rule and rate methods to validate a novel methodological approach that tests for the presence and form of reconciliation between male and female wild chacma baboons, Papio ursinus. We show that heterosexual opponents exhibit friendly postconflict reunions, further demonstrating that reconciliation occurs almost exclusively between males and pregnant/lactating females who form tight social bonds. Such ‘friendships’ represent stable associations offering proximate and ultimate benefits to both parties—mainly improving (future) offspring survival. This aligns our findings with the ‘valuable relationship hypothesis’, which predicts rates of reconciliation to increase with the fitness consequences of the opponents' bond. Moreover, patterns concerning the initiative to reconcile reveal that males are as likely as females to initiate reconciliation, suggesting that males play a heretofore underappreciated role in maintaining heterosexual friendships. Beyond proposing a multivariate methodological technique applicable to other long-term observational data sets, the present research illuminates how male–female aggression in promiscuous societies may be mitigated via relationship repair strategies like reconciliation, the balance in those efforts between partners shedding new light on the mutual investment in such bonds

In social species, female mating strategies can be constrained by both male and female groupmates through sexual conflict and reproductive competition, respectively. This study tests if females adjust their sexual behaviour according to the presence of male and female bystanders in wild chacma baboons ( Papio ursinus ) and assesses their relative importance. Our results show that oestrous females initiate fewer copulations in the presence of adult male bystanders, irrespective of whether they are mate-guarded or not. This inhibitory effect probably reflects a response to indirect sexual coercion by males, whose close proximity may dissuade females to initiate copulations with rival males to avoid punishment and/or aggressive mating interference. By contrast, females initiate more matings with their mate-guard in the presence of higher-ranking female bystanders, which may reflect an attempt to secure bodyguard services from their mate when they feel threatened. These results emphasize the importance of intra- and intersexual conflicts in shaping female sexual behaviour in this promiscuous society.

International audience; Close associations between adult males and lactating females occur in several promiscuous primate species. Benefits gained by males from such bonds may include increases in offspring fitness through paternal effort (the “mate-then-care” hypothesis) and/or subsequent mating opportunities with the female (the “care-then-mate” hypothesis). Heterosexual friendships between males and females have been described as tightly linked to the presence of a dependent infant, but few studies have investigated whether these associations may be longer, starting before an infant birth and lasting after its independence, and whether they may vary in strength across time and dyads. We investigated the stability and strength of heterosexual bonds in two groups of wild chacma baboons (Papio ursinus) to test whether male-female associations (1) last from offspring conception to independence, as expected under the mate-then-care hypothesis, (2) last after maternal cycling resumption and increase male mating success, as expected under the care-then-mate hypothesis, and (3) vary in strength depending on female reproductive state, age and rank. Our results show that most male-female bonds were already present at offspring conception, were maintained during pregnancy and lactation and disappeared when mothers resumed cycling. Moreover, heterosexual bonds were most intense during early lactation and for high-ranking females, and did not predict subsequent mating activity. Those findings favour the mate-then-care hypothesis, and confirm that male paternity assessment may, at least partially, rely on mating history. Overall, stable heterosexual friendships exist outside early lactation and last longer than previously thought, suggesting that male-female bonds could play an important and under-appreciated role on the social structure of groups in promiscuous primate societies.

Recent research reveals that female reproductive competition is common and may shape the social and reproductive strategies of female mammals. This study explores the determinants and intensity of female intrasexual conflicts in a wild promiscuous primate, the chacma baboon, Papio ursinus. We tested a suite of hypotheses to assess whether female–female aggression was primarily driven by instantaneous competition for food, mates or paternal care, or aimed at reducing future competition among offspring via reproductive suppression. Behavioural data were gathered from 53 females in two groups over two contrasting 2-year periods (2005–2006, 2013–2014): the first characterized by stability in the male dominance hierarchies, the second by instability induced by several immigration events and male take-overs. In both periods, we found that sexually receptive females received high levels of aggression from other sexually receptive females, consistent with competition over mating opportunities. In the unstable period, females exchanged higher rates of aggression than in the stable period, regardless of reproductive state, but lactating females received most aggression, consistent with higher competition over social access to male partners in response to increased infanticide risk. There was no evidence that aggression between females reflected either competition over food or reproductive suppression. These findings indicate that patterns of aggression between females fluctuate with sociodemographic factors affecting sexual and social access to males and reflect reproductive competition more closely than resource competition in this promiscuous primate society.

Summary Sexual violence occurring in the context of long-term heterosexual relationships, such as sexual intimidation, is widespread across human populations [1–3]. However, its evolutionary origins remain speculative because few studies have investigated the existence of comparable forms of sexual coercion in animals [4, 5], in which repeated male aggression toward a female provides the aggressor with delayed mating benefits [6]. Here, we test whether male aggression toward females functions as sexual coercion in wild chacma baboons ( Papio ursinus ). We found support for all three main predictions of the sexual coercion hypothesis [7]: male aggression (1) is greatest against cycling females, (2) is costly and represents the main source of injuries for cycling females, and (3) increases male mating success with their victims in the future. Detailed analysis of chronological sequences between aggression and matings ruled out other coercive mechanisms, such as short-term harassment and punishment, by showing that aggression and matings are temporally decoupled. This decoupling may explain why some forms of sexual violence have been largely overlooked in well-studied animal populations despite their likely impact on the fitness of both sexes. Finally, we found no support for alternative hypotheses such as a female preference for aggressive males [8, 9]. This new, detailed study of the forms and intensity of sexual intimidation in a wild primate suggests that it may be widespread across mammalian societies, with important implications for understanding the evolution of mate choice and sexual conflict in mammals, as well as the origins of human sexual violence.

Female–female competition over paternal care has rarely been investigated in promiscuous mammals, where discreet forms of male care have recently been reported despite low paternity certainty. We investigated female competition over paternal care in a wild promiscuous primate, the chacma baboon ( Papio ursinus ), where pregnant and lactating females establish strong social bonds (friendships) with males that provide care to their offspring. We tested whether pregnant and lactating females interfere with the sexual activity of their male friend to prevent new conceptions that might lead to the subsequent dilution of his paternal care. We found that pregnant and lactating females were more aggressive towards oestrous females when they had recently conceived themselves, and when the oestrous female was mate-guarded by, and showed greater sexual activity with, their male friend. This aggression also reduced the likelihood of conception of the targeted female. These findings indicate that females can aggressively prevent further conceptions with their offspring's carer through reproductive suppression. Competition over access to paternal care may play an important and underestimated role in shaping female social relationships and reproductive strategies in promiscuous mammalian societies.

The critical role of major histocompatibility complex (MHC) genes in disease resistance, along with their putative function in sexual selection, reproduction and chemical ecology, make them an important genetic system in evolutionary ecology. Studying selective pressures acting on MHC genes in the wild nevertheless requires population-wide genotyping, which has long been challenging because of their extensive polymorphism. Here, we report on large-scale genotyping of the MHC class II loci of the grey mouse lemur (Microcebus murinus) from a wild population in western Madagascar. The second exons from MHC-DRB and -DQB of 772 and 672 individuals were sequenced, respectively, using a 454 sequencing platform, generating more than 800,000 reads. Sequence analysis, through a stepwise variant validation procedure, allowed reliable typing of more than 600 individuals. The quality of our genotyping was evaluated through three independent methods, namely genotyping the same individuals by both cloning and 454 sequencing, running duplicates, and comparing parent–offspring dyads; each displaying very high accuracy. A total of 61 (including 20 new) and 60 (including 53 new) alleles were detected at DRB and DQB genes, respectively. Both loci were non-duplicated, in tight linkage disequilibrium and in Hardy–Weinberg equilibrium, despite the fact that sequence analysis revealed clear evidence of historical selection. Our results highlight the potential of 454 sequencing technology in attempts to investigate patterns of selection shaping MHC variation in contemporary populations. The power of this approach will nevertheless be conditional upon strict quality control of the genotyping data. peerReviewed

Erratum to: Immunogenetics (2012) 64:895 – 913 DOI 10.1007/s00251-012-0649-6 The original version of this article unfortunately contains an error in author's name in the original publication. The name Peter M. Kappeler Peter should be corrected as Peter M. Kappeler.

Ants use multiple sources of information to navigate, but do not integrate all this information into a unified representation of the world. Rather, the available information appears to serve three distinct main navigational systems: path integration, systematic search and the use of learnt information—mainly via vision. Here, we report on an additional behaviour that suggests a supplemental system in the ant's navigational toolkit: ‘backtracking’. Homing ants, having almost reached their nest but, suddenly displaced to unfamiliar areas, did not show the characteristic undirected headings of systematic searches. Instead, these ants backtracked in the compass direction opposite to the path that they had just travelled. The ecological function of this behaviour is clear as we show it increases the chances of returning to familiar terrain. Importantly, the mechanistic implications of this behaviour stress an extra level of cognitive complexity in ant navigation. Our results imply: (i) the presence of a type of ‘memory of the current trip’ allowing lost ants to take into account the familiar view recently experienced, and (ii) direct sharing of information across different navigational systems. We propose a revised architecture of the ant's navigational toolkit illustrating how the different systems may interact to produce adaptive behaviours.