Small increases in ambient temperature reduce offspring body mass in an equatorial mammal.

Human-induced climate change is leading to temperature rises, along with increases in the frequency and intensity of heatwaves. Many animals respond to high temperatures through behavioural thermoregulation, for example by resting in the shade, but this may impose opportunity costs by reducing foraging time (therefore energy supply), and so may be most effective when food is abundant. However, the heat dissipation limit (HDL) theory proposes that even when energy supply is plentiful, high temperatures can still have negative effects. This is because dissipating excess heat becomes harder, which limits processes that generate heat such as lactation. We tested predictions from HDL on a wild, equatorial population of banded mongooses (Mungos mungo). In support of the HDL theory, higher ambient temperatures led to lighter pups, and increasing food availability made little difference to pup weight under hotter conditions. This suggests that direct physiological constraints rather than opportunity costs of behavioural thermoregulation explain the negative impact of high temperatures on pup growth. Our results indicate that climate change may be particularly important for equatorial species, which often experience high temperatures year-round so cannot time reproduction to coincide with cooler conditions.

A double pedigree reveals genetic but not cultural inheritance of cooperative personalities in wild banded mongooses.

Personality traits, such as the propensity to cooperate, are often inherited from parents to offspring, but the pathway of inheritance is unclear. Traits could be inherited via genetic or parental effects, or culturally via social learning from role models. However, these pathways are difficult to disentangle in natural systems as parents are usually the source of all of these effects. Here, we exploit natural 'cross fostering' in wild banded mongooses to investigate the inheritance of cooperative behaviour. Our analysis of 800 adult helpers over 21 years showed low but significant genetic heritability of cooperative personalities in males but not females. Cross fostering revealed little evidence of cultural heritability: offspring reared by particularly cooperative helpers did not become more cooperative themselves. Our results demonstrate that cooperative personalities are not always highly heritable in wild, and that the basis of behavioural traits can vary within a species (here, by sex).

Inbreeding depresses altruism in a cooperative society.

In some animal species, individuals regularly breed with relatives, including siblings and parents. Given the high fitness costs of inbreeding, evolutionary biologists have found it challenging to understand the persistence of these inbred societies in nature. One appealing but untested explanation is that early life care may create a benign environment that offsets inbreeding depression, allowing inbred societies to evolve. We test this possibility using 21 years of data from a wild cooperatively breeding mammal, the banded mongoose, a species where almost one in ten young result from close inbreeding. We show that care provided by parents and alloparents mitigates inbreeding depression for early survival. However, as adults, inbred individuals provide less care, reducing the amount of help available to the next generation. Our results suggest that inbred cooperative societies are rare in nature partly because the protective care that enables elevated levels of inbreeding can be reduced by inbreeding depression.

Early sexual dimorphism in the developing gut microbiome of northern elephant seals.

The gut microbiome is an integral part of a species' ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals (Mirounga angustirostris) during a critical developmental window of 6 weeks after weaning, when the pups stay ashore without feeding. We found substantial sex differences in the early-life gut microbiome, even though males and females could not yet be distinguished morphologically. Sex and age both explained around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual showed high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity was explained by health status, assessed by full blood counts, but clinically healthy individuals had a greater microbial alpha diversity than their clinically abnormal peers. Across the post-weaning period, the northern elephant seal gut microbiome was highly dynamic. We found evidence for several colonization and extinction events as well as a decline in Bacteroides and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness was correlated with gut microbiome similarity in males but not females, again reflecting early sex differences. Our study represents a naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.

Explaining negative kin discrimination in a cooperative mammal society.

Kin selection theory predicts that, where kin discrimination is possible, animals should typically act more favorably toward closer genetic relatives and direct aggression toward less closely related individuals. Contrary to this prediction, we present data from an 18-y study of wild banded mongooses, Mungos mungo, showing that females that are more closely related to dominant individuals are specifically targeted for forcible eviction from the group, often suffering severe injury, and sometimes death, as a result. This pattern cannot be explained by inbreeding avoidance or as a response to more intense local competition among kin. Instead, we use game theory to show that such negative kin discrimination can be explained by selection for unrelated targets to invest more effort in resisting eviction. Consistent with our model, negative kin discrimination is restricted to eviction attempts of older females capable of resistance; dominants exhibit no kin discrimination when attempting to evict younger females, nor do they discriminate between more closely or less closely related young when carrying out infanticidal attacks on vulnerable infants who cannot defend themselves. We suggest that in contexts where recipients of selfish acts are capable of resistance, the usual prediction of positive kin discrimination can be reversed. Kin selection theory, as an explanation for social behavior, can benefit from much greater exploration of sequential social interactions.

A high-quality pedigree and genetic markers both reveal inbreeding depression for quality but not survival in a cooperative mammal.

Inbreeding depression, the reduced fitness of offspring of closely related parents, is commonplace in both captive and wild populations and has important consequences for conservation and mating system evolution. However, because of the difficulty of collecting pedigree and life-history data from wild populations, relatively few studies have been able to compare inbreeding depression for traits at different points in the life cycle. Moreover, pedigrees give the expected proportion of the genome that is identical by descent (IBDg ) whereas in theory with enough molecular markers realized IBDg can be quantified directly. We therefore investigated inbreeding depression for multiple life-history traits in a wild population of banded mongooses using pedigree-based inbreeding coefficients (fped ) and standardized multilocus heterozygosity (sMLH) measured at 35-43 microsatellites. Within an information theoretic framework, we evaluated support for either fped or sMLH as inbreeding terms and used sequential regression to determine whether the residuals of sMLH on fped explain fitness variation above and beyond fped . We found no evidence of inbreeding depression for survival, either before or after nutritional independence. By contrast, inbreeding was negatively associated with two quality-related traits, yearling body mass and annual male reproductive success. Yearling body mass was associated with fped but not sMLH, while male annual reproductive success was best explained by both fped and residual sMLH. Thus, our study not only uncovers variation in the extent to which different traits show inbreeding depression, but also reveals trait-specific differences in the ability of pedigrees and molecular markers to explain fitness variation and suggests that for certain traits, genetic markers may capture variation in realized IBDg above and beyond the pedigree expectation.

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

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 other predictors of the costs and benefits of cooperation, without the need for possibly costly within-group kin discrimination.

Policing of reproduction by hidden threats in a cooperative mammal.

The evolution of cooperation in animal and human societies is associated with mechanisms to suppress individual selfishness. In insect societies, queens and workers enforce cooperation by "policing" selfish reproduction by workers. Insect policing typically takes the form of damage limitation after individuals have carried out selfish acts (such as laying eggs). In contrast, human policing is based on the use of threats that deter individuals from acting selfishly in the first place, minimizing the need for damage limitation. Policing by threat could in principle be used to enforce reproductive suppression in animal societies, but testing this idea requires an experimental approach to simulate reproductive transgression and provoke out-of-equilibrium behavior. We carried out an experiment of this kind on a wild population of cooperatively breeding banded mongooses (Mungos mungo) in Uganda. In this species, each group contains multiple female breeders that give birth to a communal litter, usually on the same day. In a 7-y experiment we used contraceptive injections to manipulate the distribution of maternity within groups, triggering hidden threats of infanticide. Our data suggest that older, socially dominant females use the threat of infanticide to deter selfish reproduction by younger females, but that females can escape the threat of infanticide by synchronizing birth to the same day as older females. Our study shows that reproduction in animal societies can be profoundly influenced by threats that remain hidden until they are triggered experimentally. Coercion may thus extend well beyond the systems in which acts of infanticide are common.

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: (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.

Banded mongooses avoid inbreeding when mating with members of the same natal group.

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard-female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate-guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.

Lack of intergenerational reproductive conflict, rather than lack of inclusive fitness benefits, explains absence of post-reproductive lifespan in long-finned pilot whales.

Life-history theory suggests that individuals should reproduce until death, yet females of a small number of mammals live for a significant period after ceasing reproduction, a phenomenon known as post-reproductive lifespan. It is thought that the evolution of this trait is facilitated by increasing local relatedness throughout a female's lifetime. This allows older females to gain inclusive fitness through helping their offspring (known as a mother effect) and/or grandoffspring (known as a grandmother effect), rather than gaining direct fitness through reproducing. However, older females may only benefit from stopping reproducing when their direct offspring compete with those of their daughters. Here, we investigate whether a lack of post-reproductive lifespan in long-finned pilot whales (Globicephala melas) results from minimal benefits incurred from the presence of older females, or from a lack of costs resulting from mother-daughter co-reproduction. Using microsatellite data, we conducted parentage analysis on individuals from 25 pods and find that younger females were more likely to have offspring if their mother was present in their pod, indicating that mothers may assist inexperienced daughters to reproduce. However, we found no evidence of reproductive conflict between co-reproducing mothers and daughters, indicating that females may be able to reproduce into old age while simultaneously aiding their daughters in reproduction. This highlights the importance of reproductive conflict in the evolution of a post-reproductive lifespan and demonstrates that mother and grandmother effects alone do not result in the evolution of a post-reproductive lifespan.

Fine-scale spatiotemporal patterns of genetic variation reflect budding dispersal coupled with strong natal philopatry in a cooperatively breeding mammal.

The relatedness structure of animal populations is thought to be a critically important factor underlying the evolution of mating systems and social behaviours. While previous work has shown that population structure is shaped by many biological processes, few studies have investigated how these factors vary over time. Consequently, we explored the fine-scale spatiotemporal genetic structure of an intensively studied population of cooperatively breeding banded mongooses (Mungos mungo) over a 10-year period. Overall population structure was strong (average F(ST)  = 0.129) but groups with spatially overlapping territories were not more genetically similar to one another than noncontiguous groups. Instead, genetic differentiation was associated with historical group-fission (budding) events, with new groups diverging from their parent groups over time. Within groups, relatedness was high within but not between the sexes, although the latter increased over time since group formation due to group founders being replaced by philopatric young. This trend was not mirrored by a decrease in average offspring heterozygosity over time, suggesting that close inbreeding may often be avoided, even when immigration into established groups is virtually absent and opportunities for extra-group matings are rare. Fine-scale spatiotemporal population structure could have important implications in social species, where relatedness between interacting individuals is a vital component in the evolution of patterns of inbreeding avoidance, reproductive skew and kin-selected helping and harming.

A case of cooperative breeding in the European Starling, Sturnus vulgaris.

Cooperative breeding, where individuals other than the parents help to raise offspring, occurs in only ~9% of bird species. Although many starlings (Sturnidae) are cooperative breeders, the European starling (Sturnus vulgaris) has rarely been observed exhibiting this behavior. Only two other records exist, one of which was limited to a juvenile giving food to chicks that had already been collected by a parent (and hence providing limited help). Herein, we report a case of cooperative breeding by a juvenile European starling, which represents the second with any evidence of the juvenile collecting food independently and the first to document the extent of such help in the form of feeding rates. Over a period of at least 3 days, a juvenile starling assisted two parents to feed their second brood of the year, and it fed the chicks at the same rate as the adults (~3.5 feeds per hour). In considering potential explanations for this behavior, we conducted an ancestral state estimation of cooperative breeding across starlings and were able to eliminate the possibility that this is a rarely expressed behavior inherited from cooperatively breeding ancestors. Instead, we propose that our observations point to a behavioral innovation, which may be in response to environmental change such as climate change (which has previously been associated with cooperative breeding). Researchers working on birds should be alert to such behavior to determine whether this apparently new breeding strategy will increase as a potential adaptation to environmental change.

Untangling the oxidative cost of reproduction: An analysis in wild banded mongooses.

The cost of reproduction plays a central role in evolutionary theory, but the identity of the underlying mechanisms remains a puzzle. Oxidative stress has been hypothesized to be a proximate mechanism that may explain the cost of reproduction. We examine three pathways by which oxidative stress could shape reproduction. The "oxidative cost" hypothesis proposes that reproductive effort generates oxidative stress, while the "oxidative constraint" and "oxidative shielding" hypotheses suggest that mothers mitigate such costs through reducing reproductive effort or by pre-emptively decreasing damage levels, respectively. We tested these three mechanisms using data from a long-term food provisioning experiment on wild female banded mongooses (Mungos mungo). Our results show that maternal supplementation did not influence oxidative stress levels, or the production and survival of offspring. However, we found that two of the oxidative mechanisms co-occur during reproduction. There was evidence of an oxidative challenge associated with reproduction that mothers attempted to mitigate by reducing damage levels during breeding. This mitigation is likely to be of crucial importance, as long-term offspring survival was negatively impacted by maternal oxidative stress. This study demonstrates the value of longitudinal studies of wild animals in order to highlight the interconnected oxidative mechanisms that shape the cost of reproduction.

Patterns and consequences of age-linked change in local relatedness in animal societies.

The ultimate payoff of behaviours depends not only on their direct impact on an individual, but also on the impact on their relatives. Local relatedness-the average relatedness of an individual to their social environment-therefore has profound effects on social and life history evolution. Recent work has begun to show that local relatedness has the potential to change systematically over an individual's lifetime, a process called kinship dynamics. However, it is unclear how general these kinship dynamics are, whether they are predictable in real systems and their effects on behaviour and life history evolution. In this study, we combine modelling with data from real systems to explore the extent and impact of kinship dynamics. We use data from seven group-living mammals with diverse social and mating systems to demonstrate not only that kinship dynamics occur in animal systems, but also that the direction and magnitude of kinship dynamics can be accurately predicted using a simple model. We use a theoretical model to demonstrate that kinship dynamics can profoundly affect lifetime patterns of behaviour and can drive sex differences in helping and harming behaviour across the lifespan in social species. Taken together, this work demonstrates that kinship dynamics are likely to be a fundamental dimension of social evolution, especially when considering age-linked changes and sex differences in behaviour and life history.

Subspecies hybridization as a potential conservation tool in species reintroductions.

Reintroductions are a powerful tool for the recovery of endangered species. However, their long-term success is strongly influenced by the genetic diversity of the reintroduced population. The chances of population persistence can be improved by enhancing the population's adaptive ability through the mixing of individuals from different sources. However, where source populations are too diverse the reintroduced population could also suffer from outbreeding depression or unsuccessful admixture due to behavioural or genetic barriers. For the reintroduction of Asiatic wild ass Equus hemionus ssp. in Israel, a breeding core was created from individuals of two different subspecies (E. h. onager & E. h. kulan). Today the population comprises approximately 300 individuals and displays no signs of outbreeding depression. The aim of this study was a population genomic evaluation of this conservation reintroduction protocol. We used maximum likelihood methods and genetic clustering analyses to investigate subspecies admixture and test for spatial autocorrelation based on subspecies ancestry. Further, we analysed heterozygosity and effective population sizes in the breeding core prior to release and the current wild population. We discovered high levels of subspecies admixture in the breeding core and wild population, consistent with a significant heterozygote excess in the breeding core. Furthermore, we found no signs of spatial autocorrelation associated with subspecies ancestry in the wild population. Inbreeding and variance effective population size estimates were low. Our results indicate no genetic or behavioural barriers to admixture between the subspecies and suggest that their hybridization has led to greater genetic diversity in the reintroduced population. The study provides rare empirical evidence of the successful application of subspecies hybridization in a reintroduction. It supports use of intraspecific hybridization as a tool to increase genetic diversity in conservation translocations.

Reproductive control via eviction (but not the threat of eviction) in banded mongooses.

Considerable research has focused on understanding variation in reproductive skew in cooperative animal societies, but the pace of theoretical development has far outstripped empirical testing of the models. One major class of model suggests that dominant individuals can use the threat of eviction to deter subordinate reproduction (the 'restraint' model), but this idea remains untested. Here, we use long-term behavioural and genetic data to test the assumptions of the restraint model in banded mongooses (Mungos mungo), a species in which subordinates breed regularly and evictions are common. We found that dominant females suffer reproductive costs when subordinates breed, and respond to these costs by evicting breeding subordinates from the group en masse, in agreement with the assumptions of the model. We found no evidence, however, that subordinate females exercise reproductive restraint to avoid being evicted in the first place. This means that the pattern of reproduction is not the result of a reproductive 'transaction' to avert the threat of eviction. We present a simple game theoretical analysis that suggests that eviction threats may often be ineffective to induce pre-emptive restraint among multiple subordinates and predicts that threats of eviction (or departure) will be much more effective in dyadic relationships and linear hierarchies. Transactional models may be more applicable to these systems. Greater focus on testing the assumptions rather than predictions of skew models can lead to a better understanding of how animals control each other's reproduction, and the extent to which behaviour is shaped by overt acts versus hidden threats.

GCalignR: An R package for aligning gas-chromatography data for ecological and evolutionary studies.

Chemical cues are arguably the most fundamental means of animal communication and play an important role in mate choice and kin recognition. Consequently, there is growing interest in the use of gas chromatography (GC) to investigate the chemical basis of eco-evolutionary interactions. Both GC-MS (mass spectrometry) and FID (flame ionization detection) are commonly used to characterise the chemical composition of biological samples such as skin swabs. The resulting chromatograms comprise peaks that are separated according to their retention times and which represent different substances. Across chromatograms of different samples, homologous substances are expected to elute at similar retention times. However, random and often unavoidable experimental variation introduces noise, making the alignment of homologous peaks challenging, particularly with GC-FID data where mass spectral data are lacking. Here we present GCalignR, a user-friendly R package for aligning GC-FID data based on retention times. The package was developed specifically for ecological and evolutionary studies that seek to investigate similarity patterns across multiple and often highly variable biological samples, for example representing different sexes, age classes or reproductive stages. The package also implements dynamic visualisations to facilitate inspection and fine-tuning of the resulting alignments and can be integrated within a broader workflow in R to facilitate downstream multivariate analyses. We demonstrate an example workflow using empirical data from Antarctic fur seals and explore the impact of user-defined parameter values by calculating alignment error rates for multiple datasets. The resulting alignments had low error rates for most of the explored parameter space and we could also show that GCalignR performed equally well or better than other available software. We hope that GCalignR will help to simplify the processing of chemical datasets and improve the standardization and reproducibility of chemical analyses in studies of animal chemical communication and related fields.

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 [4, 5] and biases toward copying particular individuals [6, 7] can result in the rapid spread of culturally transmitted behavioral traits and a consequent increase in behavioral homogeneity within groups and populations [8, 9]. These findings support classic models of cultural evolution [10, 11], which predict that many-to-one or one-to-many transmission erodes within-group variance in culturally inherited traits. However, classic theory [10, 11] 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 behavior. 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.

Smelling fit: scent marking exposes parasitic infection status in the banded mongoose.

Preference for uninfected mates is presumed beneficial as it minimizes one's risk of contracting an infection and infecting one's offspring. In avian systems, visual ornaments are often used to indicate parasite burdens and facilitate mate choice. However, in mammals, olfactory cues have been proposed to act as a mechanism allowing potential mates to be discriminated by infection status. The effect of infection upon mammalian mate choice is mainly studied in captive rodents where experimental trials support preference for the odors of uninfected mates and some data suggest scent marking is reduced in individuals with high infection burdens. Nevertheless, whether such effects occur in nonmodel and wild systems remains poorly understood. Here, we investigate the interplay between parasite load (estimated using fecal egg counts) and scent marking behavior in a wild population of banded mongooses Mungos mungo. Focusing on a costly protozoan parasite of the genus Isospora and the nematode worm Toxocara, we first show that banded mongooses that engage in frequent, intensive scent marking have lower Isospora loads, suggesting marking behavior may be an indicator trait regarding infection status. We then use odor presentations to demonstrate that banded mongooses mark less in response to odors of opposite sexed individuals with high Isospora and Toxocara loads. As both of these parasites are known to have detrimental effects upon the health of preweaned young in other species, they would appear key targets to avoid during mate choice. Results provide support for scent as an important ornament and mechanism for advertising parasitic infection within wild mammals.