Defence against the intergenerational cost of reproduction in males: oxidative shielding of the germline.

Reproduction is expected to carry an oxidative cost, yet in many species breeders appear to sustain lower levels of oxidative damage compared to non-breeders. This paradox may be explained by considering the intergenerational costs of reproduction. Specifically, a reduction in oxidative damage upon transitioning to a reproductive state may represent a pre-emptive shielding strategy to protect the next generation from intergenerational oxidative damage (IOD) - known as the oxidative shielding hypothesis. Males may be particularly likely to transmit IOD, because sperm are highly susceptible to oxidative damage. Yet, the possibility of male-mediated IOD remains largely uninvestigated. Here, we present a conceptual and methodological framework to assess intergenerational costs of reproduction and oxidative shielding of the germline in males. We discuss variance in reproductive costs and expected payoffs of oxidative shielding according to species' life histories, and the expected impact on offspring fitness. Oxidative shielding presents an opportunity to incorporate intergenerational effects into the advancing field of life-history evolution.

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.

Temporal dynamics of mother-offspring relationships in Bigg's killer whales: opportunities for kin-directed help by post-reproductive females.

Age-related changes in the patterns of local relatedness (kinship dynamics) can be a significant selective force shaping the evolution of life history and social behaviour. In humans and some species of toothed whales, average female relatedness increases with age, which can select for a prolonged post-reproductive lifespan in older females due to both costs of reproductive conflict and benefits of late-life helping of kin. Killer whales (Orcinus orca) provide a valuable system for exploring social dynamics related to such costs and benefits in a mammal with an extended post-reproductive female lifespan. We use more than 40 years of demographic and association data on the mammal-eating Bigg's killer whale to quantify how mother-offspring social relationships change with offspring age and identify opportunities for late-life helping and the potential for an intergenerational reproductive conflict. Our results suggest a high degree of male philopatry and female-biased budding dispersal in Bigg's killer whales, with some variability in the dispersal rate for both sexes. These patterns of dispersal provide opportunities for late-life helping particularly between mothers and their adult sons, while partly mitigating the costs of mother-daughter reproductive conflict. Our results provide an important step towards understanding why and how menopause has evolved in Bigg's killer whales.

Us, them, and the others: Testing for discrimination amongst outgroups in a single-piece nesting termite, Zootermopsis angusticollis.

Recognition of group members is an important adaptation in social organisms because it allows help to be directed toward kin or individuals that are likely to reciprocate, and harm to be directed toward members of competing groups. Evidence in a wide range of animals shows that responses to outgroups vary with context, suggesting that cues to group membership also depend on the social or environmental context. In termites, intergroup encounters are frequent and their outcomes highly variable, ranging from destruction of a colony to colony fusion. As well as genetic factors, nestmate recognition in social insects commonly relies on cues that are mediated by environmental factors such as food source. However, single-piece nesting termite colonies share nesting material and food source with rival colonies (their wood substrate serves as both). In principle, the shared environment of single-piece nesting termite colonies could constrain their ability to identify non-nestmates, contributing to some of the variation seen in encounters, but this has not been investigated. In this study, we raised incipient colonies of a single-piece nesting termite, Zootermopsis angusticollis, on two different wood types and conducted behavioral assays to test whether nestmate discrimination can be constrained by common environmental conditions. We found that non-nestmates elicited higher rates of identity checking and defense behavior compared to nestmates, but there was no effect of wood type on the strength of behavioral responses to non-nestmates. We also found that one key cooperative behavior (allogrooming) was performed equally toward both nestmates and non-nestmates. These findings offer no support for the hypothesis that common wood type constrains the nestmate recognition system of single piece nesting termites. We suggest that where groups encounter each other frequently in a common environment, selection will favor discrimination based on genetic and/or higher resolution environmentally mediated cues.

Costly lifetime maternal investment in killer whales.

Parents often sacrifice their own future reproductive success to boost the survival of their offspring, a phenomenon referred to as parental investment. In several social mammals, mothers continue to improve the survival of their offspring well into adulthood;1,2,3,4,5 however, whether this extended care comes at a reproductive costs to mothers, and therefore represents maternal investment, is not well understood. We tested whether lifetime maternal care is a form of parental investment in fish-eating "resident" killer whales. Adult killer whales, particularly males, are known to receive survival benefits from their mothers;3 however, whether this comes at a cost to mothers' reproductive success is not known. Using multiple decades of complete census data from the "southern resident" population, we found a strong negative correlation between females' number of surviving weaned sons and their annual probability of producing a viable calf. This negative effect did not attenuate as sons grew older, and the cost of sons could not be explained by long-term costs of lactation or group composition effects, supporting the hypothesis that caring for adult sons is reproductively costly. This is the first direct evidence of lifetime maternal investment in an iteroparous animal, revealing a previously unknown life history strategy.

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.

Fighting force and experience combine to determine contest success in a warlike mammal.

Conflicts between social groups or "intergroup contests" are proposed to play a major role in the evolution of cooperation and social organization in humans and some nonhuman animal societies. In humans, success in warfare and other collective conflicts depends on both fighting group size and the presence and actions of key individuals, such as leaders or talismanic warriors. Understanding the determinants of intergroup contest success in other warlike animals may help to reveal the role of these contests in social evolution. Using 19 y of data on intergroup encounters in a particularly violent social mammal, the banded mongoose (Mungos mungo), we show that two factors, the number of adult males and the age of the oldest male (the "senior" male), have the strongest impacts on the probability of group victory. The advantage conferred by senior males appears to stem from their fighting experience. However, the galvanizing effect of senior males declines as they grow old until, at very advanced ages, senior males become a liability rather than an asset and can be evicted. As in human conflict, strength in numbers and the experience of key individuals combine to determine intergroup contest success in this animal society. We discuss how selection arising from intergroup contests may explain a suite of features of individual life history and social organization, including male eviction, sex-assortative alloparental care, and adult sex ratio.

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.

Kinship dynamics: patterns and consequences of changes in local relatedness.

Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.

A long postreproductive life span is a shared trait among genetically distinct killer whale populations.

The extended female postreproductive life span found in humans and some toothed whales remains an evolutionary puzzle. Theory predicts demographic patterns resulting in increased female relatedness with age (kinship dynamics) can select for a prolonged postreproductive life span due to the combined costs of intergenerational reproductive conflict and benefits of late-life helping. Here, we test this prediction using >40 years of longitudinal demographic data from the sympatric yet genetically distinct killer whale ecotypes: resident and Bigg's killer whales. The female relatedness with age is predicted to increase in both ecotypes, but with a less steep increase in Bigg's due to their different social structure. Here, we show that there is a significant postreproductive life span in both ecotypes with >30% of adult female years being lived as postreproductive, supporting the general prediction that an increase in local relatedness with age predisposes the evolution of a postreproductive life span. Differences in the magnitude of kinship dynamics however did not influence the timing or duration of the postreproductive life span with females in both ecotypes terminating reproduction before their mid-40s followed by an expected postreproductive period of about 20 years. Our results highlight the important role of kinship dynamics in the evolution of a long postreproductive life span in long-lived mammals, while further implying that the timing of menopause may be a robust trait that is persistent despite substantial variation in demographic patterns among populations.

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).

Age and sex influence social interactions, but not associations, within a killer whale pod.

Social structure is a fundamental aspect of animal populations. In order to understand the function and evolution of animal societies, it is important to quantify how individual attributes, such as age and sex, shape social relationships. Detecting these influences in wild populations under natural conditions can be challenging, especially when social interactions are difficult to observe and broad-scale measures of association are used as a proxy. In this study, we use unoccupied aerial systems to observe association, synchronous surfacing, and physical contact within a pod of southern resident killer whales (Orcinus orca). We show that interactions do not occur randomly between associated individuals, and that interaction types are not interchangeable. While age and sex did not detectably influence association network structure, both interaction networks showed significant social homophily by age and sex, and centrality within the contact network was higher among females and young individuals. These results suggest killer whales exhibit interesting parallels in social bond formation and social life histories with primates and other terrestrial social mammals, and demonstrate how important patterns can be missed when using associations as a proxy for interactions in animal social network studies.

Network-level consequences of outgroup threats in banded mongooses: Grooming and aggression between the sexes.

Animal groups are heterogeneous assemblages of individuals with differing fitness interests, which may lead to internal conflict over investment in group territorial defence. Differences between individuals may lead to different behavioural responses to intergroup conflict, particularly between the sexes. These potential impacts have been little studied. We used social network analysis to investigate the impact of simulated intergroup conflicts on social relationships in groups of wild banded mongooses Mungos mungo, in which intergroup fights are more costly for males than females. We predicted that social cohesion (specifically male-to-male and female-to-male grooming) would increase after conflict, and aggression would decrease, to minimize conflict between the sexes. Simulated intergroup conflicts were performed by exposing banded mongoose groups to scents, 'war cry' playbacks, and live intruders from a rival group. All grooming and aggression interactions between individuals were recorded, and grooming and aggression social networks were created for the 2 days preceding a simulated intergroup conflict (pre-conflict network) and the 2 days after (post-conflict network). We found no evidence of an increase in social cohesion after simulated conflicts, measured as grooming eigenvector centrality. Male-to-male, male-to-female and female-to-male grooming strength decreased after simulated intrusions compared to female-to-female grooming strength. However, male-female aggression decreased in intrusion trials compared to other interaction types, consistent with the hypothesis that intergroup encounters reduce the level of intragroup conflict between males and females. Males were more affected socially by intergroup encounters than females, which may be because they are investing in defence rather than internal relationships. Focusing on individual relationship changes, using social network analysis, can reveal changes in the directionality of behaviour in response to intergroup encounters, and highlight how individual responses to conflict may scale up to affect social networks and, potentially, group performance. This study highlights the importance of studying both group-level behaviours and individual relationships to more fully understand responses to intergroup encounters.

The dynamics of social cohesion in response to simulated intergroup conflict in banded mongooses.

Intergroup conflict is widespread in nature and is proposed to have strong impacts on the evolution of social behavior. The conflict-cohesion hypothesis predicts that exposure to intergroup conflict should lead to increased social cohesion to improve group success or resilience in future conflicts. There is evidence to support this prediction from studies of affiliative responses to outgroup threats in some animal societies. However, most of these studies have focused on behavioral changes over short time periods (minutes and hours after exposure to an outgroup), and hence very little is known about the dynamics and durability of responses to intergroup conflict over the longer term. We investigated this question by simulating intergroup encounters in wild banded mongooses (Mungos mungo) and measuring social behavior before, during, and after these encounters over a 5-day period. We also ran control trials with non-threatening stimuli. Banded mongooses reacted immediately to intrusion stimuli by vocalizing, grouping together, and advancing on the stimulus. In the first 5 min after simulated intrusions, we saw an elevation in grooming levels, but in the hour after exposure grooming rates declined sharply, contrary to our expectation. In the two subsequent days, grooming rates remained at this depressed rate. In control trials, the initial increase in grooming was not seen, but grooming declined compared to the longer-term time periods. Grooming changed across time, but not in the same pattern as during intrusions, suggesting that intrusions had an impact above and beyond that of the experimental setup. The dynamics of grooming responses were short lived and more complex than we initially expected. We suggest this unexpected result may be linked to the frequency of aggressive intergroup encounters in this system. As control and experimental trials were run at different times of year, future work would be needed to confirm that these relative patterns are replicable. Our results indicate short-lived impacts of outgroup threat on measures of social cohesion in this species, but cannot confirm longer-term changes.

Exploitative leaders incite intergroup warfare in a social mammal.

Collective conflicts among humans are widespread, although often highly destructive. A classic explanation for the prevalence of such warfare in some human societies is leadership by self-serving individuals that reap the benefits of conflict while other members of society pay the costs. Here, we show that leadership of this kind can also explain the evolution of collective violence in certain animal societies. We first extend the classic hawk-dove model of the evolution of animal aggression to consider cases in which a subset of individuals within each group may initiate fights in which all group members become involved. We show that leadership of this kind, when combined with inequalities in the payoffs of fighting, can lead to the evolution of severe intergroup aggression, with negative consequences for population mean fitness. We test our model using long-term data from wild banded mongooses, a species characterized by frequent intergroup conflicts that have very different fitness consequences for male and female group members. The data show that aggressive encounters between groups are initiated by females, who gain fitness benefits from mating with extragroup males in the midst of battle, whereas the costs of fighting are borne chiefly by males. In line with the model predictions, the result is unusually severe levels of intergroup violence. Our findings suggest that the decoupling of leaders from the costs that they incite amplifies the destructive nature of intergroup conflict.

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.

Postreproductive killer whale grandmothers improve the survival of their grandoffspring.

Understanding why females of some mammalian species cease ovulation prior to the end of life is a long-standing interdisciplinary and evolutionary challenge. In humans and some species of toothed whales, females can live for decades after stopping reproduction. This unusual life history trait is thought to have evolved, in part, due to the inclusive fitness benefits that postreproductive females gain by helping kin. In humans, grandmothers gain inclusive fitness benefits by increasing their number of surviving grandoffspring, referred to as the grandmother effect. Among toothed whales, the grandmother effect has not been rigorously tested. Here, we test for the grandmother effect in killer whales, by quantifying grandoffspring survival with living or recently deceased reproductive and postreproductive grandmothers, and show that postreproductive grandmothers provide significant survival benefits to their grandoffspring above that provided by reproductive grandmothers. This provides evidence of the grandmother effect in a nonhuman menopausal species. By stopping reproduction, grandmothers avoid reproductive conflict with their daughters, and offer increased benefits to their grandoffspring. The benefits postreproductive grandmothers provide to their grandoffspring are shown to be most important in difficult times where the salmon abundance is low to moderate. The postreproductive grandmother effect we report, together with the known costs of late-life reproduction in killer whales, can help explain the long postreproductive life spans of resident killer whales.

Stable isotopes are quantitative indicators of trophic niche.

Hette-Tronquart (2019, Ecol. Lett.) raises three concerns about our interpretation of stable isotope data in Sheppard et al. (2018, Ecol. Lett., 21, 665). We feel that these concerns are based on comparisons that are unreasonable or ignore the ecological context from which the data were collected. Stable isotope ratios provide a quantitative indication of, rather than being exactly equivalent to, trophic niche.

Elevated aggression is associated with uncertainty in a network of dog dominance interactions.

Dominance hierarchies are widespread in animal societies and reduce the costs of within-group conflict over resources and reproduction. Variation in stability across a social hierarchy may result in asymmetries in the benefits obtained from hierarchy formation. However, variation in the stability and behavioural costs of dominance interactions with rank remain poorly understood. Previous theoretical models have predicted that the intensity of dominance interactions and aggression should increase with rank, but these models typically assume high reproductive skew, and so their generality remains untested. Here we show in a pack of free-living dogs with a sex-age-graded hierarchy that the central region of the hierarchy was dominated by more unstable social relationships and associated with elevated aggression. Our results reveal unavoidable costs of ascending a dominance hierarchy, run contrary to theoretical predictions for the relationship between aggression and social rank in high-skew societies, and widen our understanding of how heterogeneous benefits of hierarchy formation arise in animal societies.

Live long and prosper: durable benefits of early-life care in banded mongooses.

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.