The social microbiome: The missing mechanism mediating the sociality-fitness nexus?

In many social mammals, early social life and social integration in adulthood largely predict individual health, lifespan, and reproductive success. So far, research has mainly focused on chronic stress as the physiological mediator between social environment and fitness. Here, we propose an alternative, non-exclusive mechanism relying on microbially mediated effects: social relationships with conspecifics in early life and adulthood might strongly contribute to diversifying host microbiomes and to the transmission of beneficial microbes. In turn, more diverse and valuable microbiomes would promote pathogen resistance and optimal health and translate into lifelong fitness benefits. This mechanism relies on recent findings showing that microbiomes are largely transmitted via social routes and play a pervasive role in host development, physiology and susceptibility to pathogens. We suggest that the social transmission of microbes could explain the sociality-fitness nexus to a similar or higher extent than chronic social stress and deserves empirical studies in social mammals.

Evolutionary Determinants of Nonseasonal Breeding in Wild Chacma Baboons.

AbstractAnimal reproductive phenology varies from strongly seasonal to nonseasonal, 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 nonseasonal breeding in seasonal environments. We investigated the evolutionary determinants of nonseasonal 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 nonseasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favoring 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; (ii) females alter their reproductive timings (fertility periods and conceptions) in relation to previous conceptions in the group; and (iii) the reported effect of birth synchrony on interbirth intervals weakens the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in group-living organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Urinary neopterin reflects immunological variation associated with age, helminth parasitism, and the microbiome in a wild primate.

Neopterin, a product of activated white blood cells, is a marker of nonspecific inflammation that can capture variation in immune investment or disease-related immune activity and can be collected noninvasively in urine. Mounting studies in wildlife point to lifetime patterns in neopterin related to immune development, aging, and certain diseases, but rarely are studies able to assess whether neopterin can capture multiple concurrent dimensions of health and disease in a single system. We assessed the relationship between urinary neopterin stored on filter paper and multiple metrics of health and disease in wild geladas (Theropithecus gelada), primates endemic to the Ethiopian highlands. We tested whether neopterin captures age-related variation in inflammation arising from developing immunity in infancy and chronic inflammation in old age, inflammation related to intramuscular tapeworm infection, helminth-induced anti-inflammatory immunomodulation, and perturbations in the gastrointestinal microbiome. We found that neopterin had a U-shaped relationship with age, no association with larval tapeworm infection, a negative relationship with metrics related to gastrointestinal helminth infection, and a negative relationship with microbial diversity. Together with growing research on neopterin and specific diseases, our results demonstrate that urinary neopterin can be a powerful tool for assessing multiple dimensions of health and disease in wildlife.

Social correlates of androgen levels and dispersal age in juvenile male geladas.

Androgens offer a window into the timing of important male life history events such as maturation. However, when males are the dispersing sex, piecing together normative androgen profiles across development is challenging because dispersing males are difficult to track. Here, we examined the conditions that may be associated with male androgen status (via fecal androgen metabolites, fAMs) and age at dispersal in wild male geladas (Theropithecus gelada). Gelada male life histories are highly variable - dispersal may occur before sexual maturation, dispersal itself can be immediate or drawn out, and, due to their multi-leveled society, social conditions affecting dispersal can vary for juveniles living in different reproductive units within the same band. Using longitudinal data from known natal males, we examined how androgen levels and age at dispersal were associated with: (1) access to maternal resources (i.e., maternal rank, birth of a younger sibling, experiencing maternal loss), and (2) access to male peers (i.e., number of similar-aged males in their unit). We found that androgens were significantly lower in males with high-ranking mothers (in males >2.5 years of age; infant androgens were unrelated) and that having more male peers in their social group and larger groups overall predicted an earlier age at dispersal. Moreover, dispersal in geladas was not preceded or followed by a surge in androgen levels. Taken together, results suggest that social environments can cause individual variation in androgens and dispersal age. Whether this variation leads to differences in male fitness in later life remains to be determined.

Maternal effects on early-life gut microbiota maturation in a wild nonhuman primate.

Early-life microbial colonization is an important process shaping host physiology,1-3 immunity,4-6 and long-term health outcomes7-10 in humans. However, our understanding of this dynamic process remains poorly investigated in wild animals,11-13 where developmental mechanisms can be better understood within ecological and evolutionarily relevant contexts.11,12 Using one of the largest developmental datasets on a wild primate-the gelada (Theropithecus gelada)-we used 16S rRNA amplicon sequencing to characterize gut microbiota maturation during the first 3 years of life and assessed the role of maternal effects in shaping offspring microbiota assembly. In contrast to recent data on chimpanzees, postnatal microbial colonization in geladas was highly similar to humans:14 microbial alpha diversity increased rapidly following birth, followed by gradual changes in composition until weaning. Dietary changes associated with weaning (from milk- to plant-based diet) were the main drivers of shifts in taxonomic composition and microbial predicted functional pathways. Maternal effects were also an important factor influencing the offspring gut microbiota. During nursing (<12 months), offspring of experienced (multi-time) mothers exhibited faster functional microbial maturation, likely reflecting the general faster developmental pace of infants born to these mothers. Following weaning (>18 months), the composition of the juvenile microbiota tended to be more similar to the maternal microbiota than to the microbiota of other adult females, highlighting that maternal effects may persist even after nursing cessation.15,16 Together, our findings highlight the dynamic nature of early-life gut colonization and the role of maternal effects in shaping this trajectory in a wild primate.

Social drivers of maturation age in female geladas.

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.

The early life microbiota mediates maternal effects on offspring growth in a nonhuman primate.

Maternal parity can impact offspring growth, but the mechanisms driving this effect are unclear. Here, we test the hypothesis that vertically transmitted microbiota may be one potential mechanism. We analyzed 118 fecal and milk samples from mother-offspring vervet monkey dyads across the first 6 months of life. Despite poorer milk production, offspring born to low parity females grew larger than their counterparts. These offspring exhibited reduced alpha diversity in the first days of life, stronger seeding of maternal milk microbiota, Bacteroides fragilis dominance, and a greater abundance of glycan utilization pathways. Moreover, the attainment of greater body mass by 6 months of age was mediated by reduced early life alpha diversity and B. fragilis dominance. This work demonstrates that the establishment of a specialized, milk-oriented gut microbiota promotes infant growth and suggests an evolutionarily conserved developmental role of B. fragilis in primates.

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate.

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.

Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas.

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. Video abstract.

Developmental transitions in body color in chacma baboon infants: Implications to estimate age and developmental pace.

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.

Baboon thanatology: responses of filial and non-filial group members to infants' corpses.

What do animals know of death? What can animals' responses to death tell us about the evolution of species' minds, and the origins of humans' awareness of death and dying? A recent surge in interest in comparative thanatology may provide beginnings of answers to these questions. Here, we add to the comparative thanatology literature by reporting 12 cases of group members' responses to infants' deaths, including 1 miscarriage and 2 stillbirths, recorded over 13 years in wild Namibian chacma baboons. Wild baboons' responses to dead infants were similar to other primates: in general, the mother of the infant carried the infants' corpse for varying lengths of time (less than 1 h to 10 days) and tended to groom the corpses frequently, though, as in other studies, considerable individual differences were observed. However, we have not yet observed any corpse carriage of very long duration (i.e. greater than 20 days), which, though rare, occurs in other Old World monkeys and chimpanzees. We hypothesize this is due to the costs of carrying the corpse over the greater daily distances travelled by the Tsaobis baboons. Additionally, in contrast to other case reports, we observed male friends' 'protection' of the infant corpse on three occasions. We discuss the implications of these reports for current questions in the field.

Oestrous females avoid mating in front of adult male bystanders in wild chacma baboons.

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.

Jealous females? Female competition and reproductive suppression in a wild promiscuous primate.

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.

Male Violence and Sexual Intimidation in a Wild Primate Society.

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.

Multiple sources of celestial compass information in the Central Australian desert ant Melophorus bagoti.

The Central Australian desert ant Melophorus bagoti is known to use celestial cues for compass orientation. We manipulated the available celestial cues for compass orientation for ants that had arrived at a feeder, were captured and then released at a distant test site that had no useful terrestrial panoramic cues. When tested in an enclosed transparent box that blocked some or most of the ultraviolet light, the ants were still well oriented homewards. The ants were again significantly oriented homewards when most of the ultraviolet light as well as the sun was blocked, or when the box was covered with tracing paper that eliminated the pattern of polarised light, although in the latter case, their headings were more scattered than in control (full-cue) conditions. When the position of the sun was reflected 180° by a mirror, the ants headed off in an intermediate direction between the dictates of the sun and the dictates of unrotated cues. We conclude that M. bagoti uses all available celestial compass cues, including the pattern of polarised light, the position of the sun, and spectral and intensity gradients. They average multiple cues in a weighted fashion when these cues conflict.

Backtracking behaviour in lost ants: an additional strategy in their navigational toolkit.

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.

MHC-disassortative mate choice and inbreeding avoidance in a solitary primate.

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by-product of inbreeding avoidance based on MHC-independent cues. Here, we used 454-sequencing and a 10-year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC-dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB-disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC-dependent mate choice.

Large-scale MHC class II genotyping of a wild lemur population by next generation sequencing.

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.