Cycle length flexibility: is the duration of sexual receptivity associated with changes in social pressures?

Research in social mammals has revealed the complexity of strategies females use in response to female-female reproductive competition and sexual conflict. One point at which competition and conflict manifests acutely is during sexual receptivity, indicated by swellings in some primates. Whether females can adjust their sexual receptivity from cycle to cycle to decrease reproductive competition and sexual conflict in response to social pressures has not been tested. As a first step, this study explores whether sexual receptivity duration is predicted by social pressures in wild female chacma baboons (Papio ursinus). Given that female baboons face intense reproductive competition and sexual coercion, we predicted that: females could shorten the duration of their sexual receptive period to reduce female-female aggression and male coercion or increase it to access multiple or their preferred male(s). We quantified 157 ovulatory cycles from 46 wild females living in central Namibia recorded over 15 years. We found no support for our hypothesis; however, our analyses revealed a negative correlation between maximal-swelling duration and group size, a proxy of within-group competition. This study provides further evidence that swelling is costly as well as a testable framework for future investigations of 'cycle length manipulation'.

Assessing the recovery of Y chromosome microsatellites with population genomic data using Papio and Theropithecus genomes.

Y chromosome markers can shed light on male-specific population dynamics but for many species no such markers have been discovered and are available yet, despite the potential for recovering Y-linked loci from available genome sequences. Here, we investigated how effective available bioinformatic tools are in recovering informative Y chromosome microsatellites from whole genome sequence data. In order to do so, we initially explored a large dataset of whole genome sequences comprising individuals at various coverages belonging to different species of baboons (genus: Papio) using Y chromosome references belonging to the same genus and more distantly related species (Macaca mulatta). We then further tested this approach by recovering Y-STRs from available Theropithecus gelada genomes using Papio and Macaca Y chromosome as reference sequences. Identified loci were validated in silico by a) comparing within-species relationships of Y chromosome lineages and b) genotyping male individuals in available pedigrees. Each STR was selected not to extend in its variable region beyond 100 base pairs, so that loci can be developed for PCR-based genotyping of non-invasive DNA samples. In addition to assembling a first set of Papio and Theropithecus Y-specific microsatellite markers, we released TYpeSTeR, an easy-to-use script to identify and genotype Y chromosome STRs using population genomic data which can be modulated according to available male reference genomes and genomic data, making it widely applicable across taxa.

Social network inheritance and differentiation in wild baboons.

Immatures' social development may be fundamental to understand important biological processes, such as social information transmission through groups, that can vary with age and sex. Our aim was to determine how social networks change with age and differ between sexes in wild immature baboons, group-living primates that readily learn socially. Our results show that immature baboons inherited their mothers' networks and differentiated from them as they aged, increasing their association with partners of similar age and the same sex. Males were less bonded to their matriline and became more peripheral with age compared to females. Our results may pave the way to further studies testing a new hypothetical framework: in female-philopatric societies, social information transmission may be constrained at the matrilineal level by age- and sex-driven social clustering.

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.

Potential applications of personality assessments to the management of non-human primates: a review of 10 years of study.

Studies of primate personality have become increasingly common over the past three decades. Recently, studies have begun to focus on the health, welfare and conservation implications of personality, and the potential applications of incorporating quantitative personality assessments into animal management programmes. However, this literature is dispersed across a multitude of settings and scientific disciplines. We conducted a review of nonhuman primate personality studies relevant to these issues published since 2010, following on from an earlier review. The databases ScienceDirect, PubMed and Web of Science were used to identify relevant articles. After eliminating irrelevant or duplicate papers, 69 studies were selected. Our review reveals that, while primate personality research is carried out on a range of species, there is strong taxonomic bias. While 28 species appeared within the reviewed literature, 52% of studies were carried out on just five species. Further, the most common research focus (43%) was validating new assessment methods or describing personality in different species, rather than exploring the links between personality and animal welfare using existing validated methods. However, among the remaining studies that did explore the role of animal personality in husbandry, health, and welfare, we identified progression towards integrating personality data into various aspects of animal management. Evidence suggests the assessment of personality may benefit social group management, enrichment practices, training protocols, health and welfare monitoring, and conservation planning for endangered species. We argue that further research which develops our understanding of primate personality and its influence in these areas will provide a valuable tool to inform animal management practices.

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.

Corrigendum: A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

[This corrects the article DOI: 10.1093/biosci/biaa082.].

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.

A Severe Lack of Evidence Limits Effective Conservation of the World's Primates.

Threats to biodiversity are well documented. However, to effectively conserve species and their habitats, we need to know which conservation interventions do (or do not) work. Evidence-based conservation evaluates interventions within a scientific framework. The Conservation Evidence project has summarized thousands of studies testing conservation interventions and compiled these as synopses for various habitats and taxa. In the present article, we analyzed the interventions assessed in the primate synopsis and compared these with other taxa. We found that despite intensive efforts to study primates and the extensive threats they face, less than 1% of primate studies evaluated conservation effectiveness. The studies often lacked quantitative data, failed to undertake postimplementation monitoring of populations or individuals, or implemented several interventions at once. Furthermore, the studies were biased toward specific taxa, geographic regions, and interventions. We describe barriers for testing primate conservation interventions and propose actions to improve the conservation evidence base to protect this endangered and globally important taxon.

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.

Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons.

Cognitive abilities underpin many of the behavioural decisions of animals. However, we still have very little understanding of how and why cognitive abilities vary between individuals of the same species in wild populations. In this study, we assessed the associative learning abilities of wild chacma baboons (Papio ursinus) across two troops in Namibia with a simple operant conditioning task. We evaluated the ability of individuals to correctly associate a particular colour of corn kernels with a distasteful flavour through repeated presentations of two small piles of corn dyed different colours, one of which had been treated with a non-toxic bitter substance. We also assessed whether individual variation in learning ability was associated with particular phenotypic traits (sex, social rank and neophilia) and states (age and prior vigilance). We found no evidence of learning the association either within each trial or across trials, nor any variation based on individuals' phenotypes. This appeared to be due to a high tolerance for bitter foods leading to similar acceptance of both palatable and unpalatable kernels. Earlier avoidance of the bitter kernels during pilot trials suggests this higher tolerance may have been largely driven by a drought during the experiments. Overall, our findings highlight the potential influence of current environmental challenges associated with conducting cognitive tests of animals in the wild.

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.

Environment and time as constraints on the biogeographical distribution of gibbons.

We develop a time budget model for the hylobatid family with the aim of assessing the extent to which their contemporary and historical biogeographic distributions might be explained by ecological constraints. The model uses local climate to predict time budgets, and from this the limiting size of social group that animals could manage at a given location. The model predicts maximum group sizes that vary between 3 and 15 within the taxon's current distribution, indicating that the combination of their dietary and locomotor styles with the kinds of habitats they inhabit radically constrain group size. Beyond the edges of their current distribution, sustainable group size rapidly tends to zero, although if they had been able to bypass some of these areas, they would have found very suitable habitats in southern India and beyond the Wallace Line. While travel time would be a major constraint on group size at larger group sizes, as it is in great apes, the main factor limiting the gibbon's current distribution is the time they need to spend resting that is imposed on them by the environment. The model also indicates that gibbons would not now be able to survive in regions of central and southeastern China where they are known to have occurred within historical times, perhaps because historical climate change following the Little Ice Age of the C18th made these regions uninhabitable for them. Finally, our results indicate that gibbons have the ecological capacity to live in larger groups than they do, making it unlikely that their adoption of monogamy reflects purely ecological constraints.

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.

Rural protein insufficiency in a wildlife-depleted West African farm-forest landscape.

INTRODUCTION: Wildlife is an important source of protein for many people in developing countries. Yet wildlife depletion due to overexploitation is common throughout the humid tropics and its effect on protein security, especially for vulnerable households, is poorly understood. This is problematic for both sustainable rural development and conservation management. METHODS: This study investigates a key dimension of protein security in a cash-crop farming community living in a wildlife-depleted farm-forest landscape in SW Ghana, a region where protein-energy malnutrition persists. Specifically, we monitored protein sufficiency, defined as whether consumption met daily requirements, as benchmarked by recommended daily allowance (RDA). We focus on whether more vulnerable households were less likely to be able to meet their protein needs, where vulnerability was defined by wealth, agricultural season and gender of the household head. Our central hypothesis was: (a) vulnerable households are less likely to consume sufficient protein. In the context that most plant proteins were home-produced, so likely relatively accessible to all households, while most animal proteins were purchased, so likely less accessible to vulnerable households, we tested two further hypotheses: (b) vulnerable households depend more on plant protein to cover their protein needs; and (c) vulnerable households are less likely to earn sufficient cash income to meet their protein needs through purchased animal sources. RESULTS: Between 14% and 60% of households (depending on plant protein content assumptions) consumed less than the RDA for protein, but neither protein consumption nor protein sufficiency co-varied with household vulnerability. Fish, livestock and food crops comprised 85% of total protein intake and strongly affected protein sufficiency. However, bushmeat remained an important protein source (15% of total consumption), especially during the post-harvest season when it averaged 26% of total protein consumption. Across the year, 89% of households experienced at least one occasion when they had insufficient income to cover their protein needs through animal protein purchases. The extent of this income shortage was highest during the lean season and among poorer households. CONCLUSIONS: These findings indicate that despite wildlife depletion, bushmeat continues to make a substantial contribution to protein consumption, especially during the agricultural lean season. Income shortages among farmers limit their ability to purchase bushmeat or its substitutes, suggesting that wildlife depletion may cause malnutrition.

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.

Switching spatial scale reveals dominance-dependent social foraging tactics in a wild primate.

When foraging in a social group, individuals are faced with the choice of sampling their environment directly or exploiting the discoveries of others. The evolutionary dynamics of this trade-off have been explored mathematically through the producer-scrounger game, which has highlighted socially exploitative behaviours as a major potential cost of group living. However, our understanding of the tight interplay that can exist between social dominance and scrounging behaviour is limited. To date, only two theoretical studies have explored this relationship systematically, demonstrating that because scrounging requires joining a competitor at a resource, it should become exclusive to high-ranking individuals when resources are monopolisable. In this study, we explore the predictions of this model through observations of the natural social foraging behaviour of a wild population of chacma baboons (Papio ursinus). We collected data through over 800 h of focal follows of 101 adults and juveniles across two troops over two 3-month periods. By recording over 7,900 social foraging decisions at two spatial scales we show that, when resources are large and economically indefensible, the joining behaviour required for scrounging can occur across all social ranks. When, in contrast, dominant individuals can aggressively appropriate a resource, such joining behaviour becomes increasingly difficult to employ with decreasing social rank because adult individuals can only join others lower ranking than themselves. Our study supports theoretical predictions and highlights potentially important individual constraints on the ability of individuals of low social rank to use social information, driven by competition with dominant conspecifics over monopolisable resources.

Widespread dieback of riparian trees on a dammed ephemeral river and evidence of local mitigation by tributary flows.

Ephemeral rivers act as linear oases in drylands providing key resources to people and wildlife. However, not much is known about these rivers' sensitivities to human activities. We investigated the landscape-level determinants of riparian tree dieback along the Swakop River, a dammed ephemeral river in Namibia, focusing on the native ana tree (Faidherbia albida) and the invasive mesquite (Prosopis spp.). We surveyed over 1,900 individual trees distributed across 24 sites along a 250 km stretch of the river. General linear mixed models were used to test five hypotheses relating to three anthropogenic threats: river flow disruption from damming, human settlement and invasive species. We found widespread dieback in both tree populations: 51% mortality in ana tree, with surviving trees exhibiting 18% canopy death (median); and 26% mortality in mesquite, with surviving trees exhibiting 10% canopy death. Dieback in the ana tree was most severe where trees grew on drier stretches of the river, where tributary flow was absent and where mesquite grew more abundantly. Dieback in the mesquite, a more drought-tolerant taxon, did not show any such patterns. Our findings suggest that dieback in the ana tree is primarily driven by changes in river flow resulting from upstream dam creation and that tributary flows provide a local buffer against this loss of main channel flow. The hypothesis that the invasive mesquite may contribute to ana tree dieback was also supported. Our findings suggest that large dams along the main channels of ephemeral rivers have the ability to cause widespread mortality in downstream riparian trees. To mitigate such impacts, management might focus on the maintenance of natural tributary flows to buffer local tree populations from the disruption to main channel flow.

Sequential phenotypic constraints on social information use in wild baboons.

Social information allows the rapid dissemination of novel information among individuals. However, an individual's ability to use information is likely to be dependent on phenotypic constraints operating at three successive steps: acquisition, application, and exploitation. We tested this novel framework by quantifying the sequential process of social information use with experimental food patches in wild baboons (Papio ursinus). We identified phenotypic constraints at each step of the information use sequence: peripheral individuals in the proximity network were less likely to acquire and apply social information, while subordinate females were less likely to exploit it successfully. Social bonds and personality also played a limiting role along the sequence. As a result of these constraints, the average individual only acquired and exploited social information on.

Information use and resource competition: an integrative framework.

Organisms may reduce uncertainty regarding how best to exploit their environment by collecting information about resource distribution. We develop a model to demonstrate how competition can facilitate or constrain an individual's ability to use information when acquiring resources. As resource distribution underpins both selection on information use and the strength and nature of competition between individuals, we demonstrate interdependencies between the two that should be common in nature. Individuals in our model can search for resources either personally or by using social information. We explore selection on social information use across a comprehensive range of ecological conditions, generalizing the producer-scrounger framework to a wide diversity of taxa and resources. We show that resource ecology--defined by scarcity, depletion rate and monopolizability--determines patterns of individual differences in social information use. These differences suggest coevolutionary processes linking dominance systems and social information use, with implications for the evolutionary demography of populations.