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The costs of reproductive conflict can shape the evolution of life-histories in animal societies. These costs may change as individuals age and grow, and with within-group competition. Social costs of reproductive conflict have been invoked to explain why females might gain from delaying maturity or ceasing reproduction midway through life, but not in males. Here, we analyse more than 20 years of data to understand how individual male banded mongooses adjust their reproductive activity in response to the costs of reproductive conflict. In banded mongoose groups, multiple female breeders enter oestrus synchronously that are each guarded by a single male that aggressively wards-off rivals. The heaviest males in the group gained the greatest share of paternity. Those lighter males that are reproductively active paid disproportionate survival costs, and by engaging in reproductive activity early had lower lifetime reproductive success. Our results suggest that reproductive inactivity early in life is adaptive, as males recoup any lost fitness by first growing before engaging in less costly and more profitable reproductive activity later in life. These results suggest that resource holding potential of males and the intensity of reproductive conflict interact to shape lifetime schedules of reproductive behaviour.

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., (© 2023 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.)

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.

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'.

The evolutionary puzzle of the extended post-reproductive life of female humans has been explained by indirect fitness benefits gained by grandmothers helping raise their grandchildren. Two new studies support this 'grandmother hypothesis' and explore its limits in space and time., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

In most species the reproductive system ages at the same rate as somatic tissue and individuals continue reproducing until death. However, females of three species - humans, killer whales and short-finned pilot whales - have been shown to display a markedly increased rate of reproductive senescence relative to somatic ageing. In these species, a significant proportion of females live beyond their reproductive lifespan: they have a post-reproductive lifespan. Research into this puzzling life-history strategy is hindered by the difficulties of quantifying the rate of reproductive senescence in wild populations. Here we present a method for measuring the relative rate of reproductive senescence in toothed whales using published physiological data. Of the sixteen species for which data are available (which does not include killer whales), we find that three have a significant post-reproductive lifespan: short-finned pilot whales, beluga whales and narwhals. Phylogenetic reconstruction suggests that female post-reproductive lifespans have evolved several times independently in toothed whales. Our study is the first evidence of a significant post-reproductive lifespan in beluga whales and narwhals which, when taken together with the evidence for post-reproductive lifespan in killer whales, doubles the number of non-human mammals known to exhibit post-reproductive lifespans in the wild.

Life-history theory assumes that reproduction and lifespan are constrained by trade-offs which prevent their simultaneous increase. Recently, there has been considerable interest in the possibility that this cost of reproduction is mediated by oxidative stress. However, empirical tests of this theory have yielded equivocal support. We carried out a meta-analysis to examine associations between reproduction and oxidative damage across markers and tissues. We show that oxidative damage is positively associated with reproductive effort across females of various species. Yet paradoxically, categorical comparisons of breeders versus non-breeders reveal that transition to the reproductive state is associated with a step-change reduction in oxidative damage in certain tissues and markers. Developing offspring may be particularly sensitive to harm caused by oxidative damage in mothers. Therefore, such reductions could potentially function to shield reproducing mothers, gametes and developing offspring from oxidative insults that inevitably increase as a consequence of reproductive effort. According to this perspective, we hypothesise that the cost of reproduction is mediated by dual impacts of maternally-derived oxidative damage on mothers and offspring, and that mothers may be selected to diminish such damage. Such oxidative shielding may explain why many existing studies have concluded that reproduction has little or no oxidative cost. Future advance in life-history theory therefore needs to take account of potential transgenerational impacts of the mechanisms underlying life-history trade-offs., (© 2015 Cambridge Philosophical Society.)

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., (© 2016 The Authors.)

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.

Remarkable variation exists in the distribution of reproduction (skew) among members of cooperatively breeding groups, both within and between species. Reproductive skew theory has provided an important framework for understanding this variation. In the primitively eusocial Hymenoptera, two models have been routinely tested: concessions models, which assume complete control of reproduction by a dominant individual, and tug-of-war models, which assume on-going competition among group members over reproduction. Current data provide little support for either model, but uncertainty about the ability of individuals to detect genetic relatedness and difficulties in identifying traits conferring competitive ability mean that the relative importance of concessions versus tug-of-war remains unresolved. Here, we suggest that the use of social parasitism to generate meaningful variation in key social variables represents a valuable opportunity to explore the mechanisms underpinning reproductive skew within the social Hymenoptera. We present a direct test of concessions and tug-of-war models in the paper wasp Polistes dominulus by exploiting pronounced changes in relatedness and power structures that occur following replacement of the dominant by a congeneric social parasite. Comparisons of skew in parasitized and unparasitized colonies are consistent with a tug-of-war over reproduction within P. dominulus groups, but provide no evidence for reproductive concessions.

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.

Members of animal societies compete over resources and reproduction, but the extent to which such conflicts of interest are resolved peacefully (without recourse to costly or wasteful acts of aggression) varies widely. Here, we describe two theoretical mechanisms that can help to understand variation in the incidence of overt behavioural conflict: (i) destruction competition and (ii) the use of threats. The two mechanisms make different assumptions about the degree to which competitors are socially sensitive (responsive to real-time changes in the behaviour of their social partners). In each case, we discuss how the model assumptions relate to biological reality and highlight the genetic, ecological and informational factors that are likely to promote peaceful conflict resolution, drawing on empirical examples. We suggest that, relative to males, reproductive conflict among females may be more frequently resolved peacefully through threats of punishment, rather than overt acts of punishment, because (i) offspring are more costly to produce for females and (ii) reproduction is more difficult to conceal. The main need now is for empirical work to test whether the mechanisms described here can indeed explain how social conflict can be resolved without overt aggression.

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.

In primitively eusocial societies, all individuals can potentially reproduce independently. The key fact that we focus on in this paper is that individuals in such societies instead often queue to inherit breeding positions. Queuing leads to systematic differences in expected future fitness. We first discuss the implications this has for variation in behaviour. For example, because helpers nearer to the front of the queue have more to lose, they should work less hard to rear the dominant's offspring. However, higher rankers may be more aggressive than low rankers, even if they risk injury in the process, if aggression functions to maintain or enhance queue position. Second, we discuss how queuing rules may be enforced through hidden threats that rarely have to be carried out. In fishes, rule breakers face the threat of eviction from the group. In contrast, subordinate paper wasps are not injured or evicted during escalated challenges against the dominant, perhaps because they are more valuable to the dominant. We discuss evidence that paper-wasp dominants avoid escalated conflicts by ceding reproduction to subordinates. Queuing rules appear usually to be enforced by individuals adjacent in the queue rather than by dominants. Further manipulative studies are required to reveal mechanisms underlying queue stability and to elucidate what determines queue position in the first place.

An enduring puzzle of human life history is why women cease reproduction midway through life. Selection can favor postreproductive survival because older females can help their offspring to reproduce. But the kin-selected fitness gains of helping appear insufficient to outweigh the potential benefits of continued reproduction. Why then do women cease reproduction in the first place? Here, we suggest that early reproductive cessation in humans is the outcome of reproductive competition between generations, and we present a simple candidate model of how this competition will be resolved. We show that among primates exhibiting a postreproductive life span, humans exhibit an extraordinarily low degree of reproductive overlap between generations. The rapid senescence of the human female reproductive system coincides with the age at which, in natural fertility populations, women are expected to encounter reproductive competition from breeding females of the next generation. Several lines of evidence suggest that in ancestral hominids, this younger generation typically comprised immigrant females. In these circumstances, relatedness asymmetries within families are predicted to give younger females a decisive advantage in reproductive conflict with older females. A model incorporating both the costs of reproductive competition and the benefits of grandmothering can account for the timing of reproductive cessation in humans and so offers an improved understanding of the evolution of menopause.

The article focuses on the evolution of menopause in female chimpanzees (Pan troglodytes) in the Ngogo community of Uganda. These chimpanzees, living in a relatively undisturbed population, show physiological signs of menopause and can survive long past the end of their reproductive years. This observation challenges previous theories about the evolution of menopause and its role in kin selection.

The recent development of reproductive skew (RS) theory shows striking parallels with that of parent–offspring conflict (POC) theory a decade earlier. In particular, the concept of ‘battleground’ and ‘resolution’ models in POC theory is equally relevant to RS theory. The battleground of conflict in POC and RS has been defined by different constraints (which I term ‘optimization’ and ‘group stability’ constraints, respectively). This distinction is not inherent but arises simply because POC models assume that the fitness benefits of an increasing share of resource show diminishing returns, whereas skew models assume a linear relation between reproductive share and fitness. Incorporating diminishing returns into skew models reveals a simple and almost wholly neglected explanation for reproductive sharing. Models of POC have moved on from simply defining the battleground to consider how conflict within it is resolved. The development of analogous models for RS theory is at a relatively early stage. In particular, more work is needed to understand the manner and extent to which overt aggression can mediate reproductive control. Lessons learned from attempts to test POC theory can help guide tests of RS theory, and provide information on both the nature of the battleground over reproduction and the mechanism by which conflicts are resolved. [Copyright &y& Elsevier]

Develops two models to explore the expected patterns of skew in three member groups in which a female controls the allocation of paternity among two males in cooperative animal breeding. Nature of male-female conflict over reproduction; Relative quality of the subordinate male; Evolutionary cause of variation in skew among males.

Of key importance for understanding cooperative societies is the way in which reproductive opportunities are distributed among group members. Traditionally, skew has been thought of as a product of intrasexual competition. However, cooperatively breeding species often live in mixed-sex groups, so the behaviour of one sex has the potential to influence skew in the other. We addressed the importance of inter- and intrasexual conflict in determining reproductive skew through a study of paternity sharing in the cooperatively breeding banded mongoose, Mungus mungo. Unlike banded mongoose females, where reproductive skew is low, males exhibited high skew, with 85% of paternities being assigned to the three oldest males in each group. Individual males appeared unable to monopolize reproduction because females come into oestrus in synchrony and mate multiply. Instead, older males increased their success by mate guarding the oldest, most fecund females. Our findings therefore highlight the importance of mate choice in males and reveal the behavioural differences between the sexes that generate reproductive skew. They also emphasize the considerable influence that female behaviour can have on male reproductive skew. [Copyright &y& Elsevier]

Individual differences in contributions to cooperation can be strikingly consistent over time giving rise to alternative cooperative phenotypes within animal societies. Following the social niche specialization hypothesis, these consistent differences may be driven by social conflict over reproductive opportunities if individuals specializing as ‘breeders’ and ‘nonbreeders’ experience a beneficial reduction in social conflict and differential costs associated with cooperating. This hypothesis gives three testable predictions: (1) consistent individual differences in cooperative behaviour will be accompanied by consistent individual differences in reproductive behaviour, (2) individuals contributing heavily to reproduction will contribute relatively little to cooperative behaviours within the same breeding attempt and vice versa, and (3) individuals that consistently contribute heavily to reproduction over their lifetime will also consistently contribute less to cooperative behaviours and vice versa. We tested these predictions with a 15-year investigation into the lifetime patterns of mate guarding and two forms of cooperative offspring care (‘babysitting’ and ‘escorting’) in a wild population of banded mongooses. We found significant repeatability of individual contributions to both cooperative behaviours, as well as significant repeatability of individual levels of mate guarding. However, we found no evidence of negative covariance between contributions to cooperative and reproductive behaviours either within breeding attempts or across lifetimes. This suggests that the observed consistent individual differences in both cooperative behaviour and reproduction are not associated; there is no evidence of a trade-off between reproduction and cooperation. However, we found a significant positive covariance between babysitting and escorting when estimated both within breeding attempts and across lifetimes, which suggests that some group members are generally more cooperative than others, contributing more to both behaviours over their lifetimes. The drivers of this consistent individual variation in contributions to cooperation remain unknown. [ABSTRACT FROM AUTHOR]

In cooperatively breeding vertebrate societies, contributions to offspring care can vary greatly between group members. Kin selection theory predicts that cooperation will be favoured when directed towards relatives and when the cost to benefit ratio is low. The fitness costs of helping in turn depend on the impact of energetic investments in care on future reproductive success, which is likely to vary between helpers. For example, investments may impact more on a young helper, which needs to invest energy in growth and is an inexperienced forager. We investigated how a key predictor of cost, food availability (estimated using rainfall), influences helping behaviour in the banded mongoose, Mungos mungo. In this cooperative carnivore, a variable number of group members breed while almost all help to rear the communal litter. Nonbreeding females and juvenile males helped less when food was scarce, reflecting the potentially high costs of weight loss and reduced growth on survival and future reproductive success. In contrast, adult males maintained their investment in care as food supply decreased, probably because body condition has relatively little impact on male reproductive success in this species. Breeding females (with pups in the communal litter) also maintained their helping effort as food supply decreased. Although mothers invested highly in care, there was no evidence that they preferentially cared for their own pups, probably because synchronized birthing scrambles maternity cues. Patterns of care in the banded mongoose thus seem to reflect the benefits gained from helping and the long-term fitness costs to the helper. [Copyright &y& Elsevier]