Group size and visitor number predict faecal glucocorticoid concentrations in zoo meerkats

This is the author accepted manuscript. The final version is freely available from Royal Society via the DOI in this record.Measures of physiological stress in zoo animals can give important insights into how they are affected by aspects of their captive environment. We analysed the factors influencing variation in glucocorticoid metabolites in faeces (fGCs) from zoo meerkats as a proxy for blood cortisol concentration, high levels of which are associated with a stress response. Levels of fGCs in captive meerkats declined with increasing group size. Compared to data from wild meerkats, this contrasts with the patterns seen in large stabile groups but matches the pattern seen in dispersing coalitions. In the wild, very small groups of meerkats are at a higher risk of predation, while in larger groups there is increased competition for resources. Indeed, group sizes in captivity tend to be closer to those seen in unstable coalitions in the wild, which may represent a stressful condition to meerkats in captivity and predispose them to chronic stress, even in absence of natural predators. Individuals in large enclosures showed lower levels of stress, but meerkat density had no effect on the stress measures. In contrast to data from wild meerkats, neither sex, age, nor dominance status predicted physiological stress levels in captivity, which may reflect less food stress owing to more equal access to resources in captivity versus wild. Median number of visitors at the enclosure was positively correlated with fGC concentrations on the following day, with variation in the visitor numbers having the opposite effect. Our results are consistent with the hypothesis that there is an optimum group size which minimises physiological stress in meerkats, and that zoo meerkats at most risk of physiological stress are those kept in small groups and small enclosures and are exposed to consistently high numbers of visitors.Funding was provided by a European Social Fund studentship and a Society for Endocrinology grant awarded to K.S., and by NERC grant awarded to M.A.C. (NE/J010278/1)

Heterozygosity but not inbreeding coefficient predicts parasite burdens in the banded mongoose

This is the author accepted manuscript. The final version is available from Wiley via the DOI in this record.Inbreeding, reproduction between relatives, often impinges on the health and survival of resulting offspring. Such inbreeding depression may manifest itself through immunological costs as inbred individuals suffer increased propensity to disease, infection and parasites compared to outbred conspecifics. Here, we assess how the intestinal parasite loads of wild banded mongooses (Mungos mungo) vary with pedigree inbreeding coefficient (ƒ) and standardized multi-locus heterozygosity. We find a significant association between increased heterozygosity and lower parasite loads; however, this correlation does not stand when considering ƒ. Such findings may be explained by local genetic effects, linkage between genetic markers and genes influencing parasite burdens. Indeed, we find heterozygosity at certain loci to correlate with parasite load. Although these tentative local effects are lost following multiple test correction, they warrant future investigation to determine their strength and impact. We also suggest frequent inbreeding within banded mongooses may mean heterozygosity is a better predictor of inbreeding than pedigree ƒ. This is because inbreeding facilitates linkage disequilibrium, increasing the chances of neutral markers representing genome-wide heterozygosity. Finally, neither ƒ nor heterozygosity had a significant influence on the loads of two specific gastrointestinal parasites. Nevertheless, more heterozygous individuals benefited from reduced overall parasitic infection and genetic diversity appears to explain some variation in parasite burdens in the banded mongoose

Reproductive competition triggers mass eviction in cooperative banded mongooses

In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are (1) the reproductive competition hypothesis; (2) the coercion of cooperation hypothesis; and (3) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution

Female reproductive competition explains variation in prenatal investment in wild banded mongooses

Female intrasexual competition is intense in cooperatively breeding species where offspring compete locally for resources and helpers. In mammals, females have been proposed to adjust prenatal investment according to the intensity of competition in the postnatal environment (a form of ‘predictive adaptive response’; PAR). We carried out a test of this hypothesis using ultrasound scanning of wild female banded mongooses in Uganda. In this species multiple females give birth together to a communal litter, and all females breed regularly from one year old. Total prenatal investment (size times the number of fetuses) increased with the number of potential female breeders in the group. This relationship was driven by fetus size rather than number. The response to competition was particularly strong in low weight females and when ecological conditions were poor. Increased prenatal investment did not trade off against maternal survival. In fact we found the opposite relationship: females with greater levels of prenatal investment had elevated postnatal maternal survival. Our results support the hypothesis that mammalian prenatal development is responsive to the intensity of postnatal competition. Understanding whether these responses are adaptive requires information on the long-term consequences of prenatal investment for offspring fitness

Reproductive competition triggers mass eviction in cooperative banded mongooses

This is the final version of the article. Available from the publisher via the DOI in this record.In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are: (i) the reproductive competition hypothesis, (ii) the coercion of cooperation hypothesis, and (iii) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution.Funding was provided by NERC grant no. NE/J010278/1 to M.A.C. and A.J.Y. and ERC grant no. 309249 to M.A.C

Decoupling of genetic and cultural inheritance in a wild mammal

Cultural inheritance, the transmission of socially learned information across generations, is a non-genetic, ‘second inheritance system’ capable of shaping phenotypic variation in humans and many non-human animals[1-3]. Studies of wild animals show that conformity and biases toward copying particular individuals can result in the rapid spread of culturally transmitted behavioural traits and a consequent increase in behavioural homogeneity within groups and populations. These findings support classic models of cultural evolution which predict that many-to-one or one-to-many transmission erodes within-group variance in culturally inherited traits. However, classic theory also predicts that within-group heterogeneity is preserved when offspring each learn from an exclusive role model. We tested this prediction in a wild mammal, the banded mongoose (Mungos mungo), in which offspring are reared by specific adult carers that are not their parents, providing an opportunity to disentangle genetic and cultural inheritance of behaviour. We show using stable isotope analysis that young mongooses inherit their adult foraging niche from cultural role models, not from their genetic parents. As predicted by theory, one-to-one cultural transmission prevented blending inheritance and allowed the stable coexistence of distinct behavioral traditions within the same social groups. Our results confirm that cultural inheritance via role models can promote rather than erode behavioral heterogeneity in natural populations

Caregiver's cognitive traits are associated with pup fitness in a cooperatively breeding mammal.

This is the final version. Available on open access from Nature Research via the DOI in this record. Data availability: The datasets used in this study are available in the Fig Share repository, https://doi.org/10.6084/m9.fgshare. 23615046.v1.Studies across diverse taxa have revealed the importance of early life environment and parenting on characteristics later in life. While some have shown how early life experiences can impact cognitive abilities, very few have turned this around and looked at how the cognitive skills of parents or other carers during early life affect the fitness of young. In this study, we investigate how the characteristics of carers may affect proxies of fitness of pups in the cooperatively breeding banded mongoose (Mungos mungo). We gave adult mongooses a spatial memory test and compared the results to the success of the pups those individuals cared for. Our results show a tradeoff between speed and accuracy in the spatial memory task, with those individuals which were faster to move between cups in the test arena making more erroneous re-visits to cups that they had already checked for food. Furthermore, the accuracy of their carer predicted future survival, but not weight gain of the pups and the effect was contrary to expected, with pups that were cared for by less accurate individuals being more likely to survive to adulthood. Our research also provides evidence that while younger carers were less accurate during the test, the age of the carer did not have an impact on the chance of raising young that live to sexual maturity. Our findings suggest that banded mongoose carers' cognitive traits have fitness consequences for the young they care for, affecting the chance that these young live to maturity.Natural Environment Research Council (NERC)European CommissionElla and Georg Ehrnrooth Foundatio

Biased escorts: offspring sex, not relatedness explains alloparental care patterns in a cooperative breeder

This is the author accepted manuscript. The final version is available from the Royal Society via the DOI in this record.Kin selection theory predicts that animals should direct costly care where inclusive fitness gains are highest. Individuals may achieve this by directing care at closer relatives, yet evidence for such discrimination in vertebrates is equivocal. We investigated patterns of cooperative care in banded mongooses, where communal litters are raised by adult 'escorts' who form exclusive caring relationships with individual pups. We found no evidence that escorts and pups assort by parentage or relatedness. However, the time males spent escorting increased with increasing relatedness to the other group members, and to the pup they had paired with. Thus we found no effect of relatedness in partner choice, but (in males) increasing helping effort with relatedness once partner choices had been made. Unexpectedly, the results showed clear assortment by sex, with female carers being more likely to tend to female pups, and male carers to male pups. This sex-specific assortment in helping behaviour has potential lifelong impacts on individual development, and may impact the future size and composition of natal groups and dispersing cohorts. Where relatedness between helpers and recipients is already high, individuals may be better off choosing partners using predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination.This work was funded by a European Research Council Starting Grant (SOCODEV, grant number 309249) and a Natural Environment Research Council (UK) Standard Grant (NE/J010278/1)