Lifetime trajectories of male mating effort under reproductive conflict in a cooperatively breeding mammal.

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.

Novel insights into paternity skew in a polyandrous social wasp.

Females of many species are polyandrous. However, polyandry can give rise to conflict among individuals within families. We examined the level of polyandry and paternity skew in the common eastern yellowjacket wasp, Vespula maculifrons, in order to gain a greater understanding of conflict in social insects. We collected 10 colonies of V. maculifrons and genotyped workers and prereproductive queens at highly variable microsatellite markers to assign each to a patriline. Genotypic data revealed evidence of significant paternity skew among patrilines. In addition, we found that patrilines contributed differentially to caste production (worker vs. queen), suggesting an important role for reproductive conflict not previously discovered. We also investigated if patterns of paternity skew and mate number varied over time. However, we found no evidence of changes in levels of polyandry when compared to historical data dating back almost 40 years. Finally, we measured a suite of morphological traits in individuals from the most common and least common patrilines in each colony to test if males that showed highly skewed reproductive success also produced offspring that differed in phenotype. Our data revealed weak correlation between paternity skew and morphological phenotype of offspring sired by different males, suggesting no evidence of evolutionary tradeoffs at the level investigated. Overall, this study is the first to report significant paternity and caste-associated skew in V. maculifrons, and to investigate the phenotypic consequences of skew in a social wasp. Our results suggest that polyandry can have important consequences on the genetic and social structure of insect societies.

Elusive workers are more likely to differentiate into replacement reproductives than aggressive workers in a lower termite.

One of the most intriguing questions in eusocial insects is to understand how the overt reproductive conflict in the colony appears limited when queens or kings are senescent or lost because the morphologically similar individuals in the colony are reproductively totipotent. Whether there are some individuals who preferentially differentiate into replacement reproductives or not has received little attention. The consistent individual behavioral differences (also termed "animal personality") of individuals from the colony can shape cunningly their task and consequently affect the colony fitness but have been rarely investigated in eusocial insects. Here, we used the termite Reticulitermes labralis to investigate if variations in individual personalities (elusiveness and aggressiveness) may predict which individuals will perform reproductive differentiation within colonies. We observed that when we separately reared elusive and aggressive workers, elusive workers differentiate into reproductives significantly earlier than aggressive workers. When we reared them together in the proportions 12:3, 10:5, and 8:7 (aggressive workers: elusive workers), the first reproductives mostly differentiated from the elusive workers, and the reproductives differentiated from the elusive workers significantly earlier than from aggressive workers. Furthermore, we found that the number of workers participating in reproductive differentiation was significantly lower in the groups of both types of workers than in groups containing only elusive workers. Our results demonstrate that the elusiveness trait was a strong predictor of workers' differentiation into replacement reproductives in R. labralis. Moreover, our results suggest that individual personalities within the insect society could play a key role in resolving the overt reproductive conflict.

Kin networks and opportunities for reproductive cooperation and conflict among hunter-gatherers.

Little is known about the potential for reproductive conflict among hunter-gatherer populations, who are characterized by bilateral kinship ties, flexible residential mobility, and high offspring mortality. To assess the potential for reproductive conflict, we use longitudinal residence and reproductive history data for two bands of South American foragers. Using multilevel logistic regressions (N = 44 women, N = 712 person years), we examine how yearly measures of (i) camp composition, (ii) distribution of female kin and (iii) a woman's position in a female kinship network impact the likelihood of giving birth or experiencing a child's death. We compare conflict models to a demographic model that accounts for the proportion of women giving birth in a given year. Contrary to conflict models, results show that the odds of giving birth increase with the presence of highly related women. However, the odds of experiencing an offspring death are insensitive to the presence of coresident women. Network measures of closeness and centrality in the female kin network also show no significant effect on reproductive outcomes. Furthermore, chances of both births and deaths increase in years when proportionally more women are giving birth. We argue that demographic stochasticity relating to ecological conditions best predicts reproductive outcomes for women. This article is part of the theme issue 'Cooperation among women: evolutionary and cross-cultural perspectives'.

Social structure of perennial Vespula squamosa wasp colonies.

Many social species show variation in their social structure in response to different environmental conditions. For example, colonies of the yellowjacket wasp Vespula squamosa are typically headed by a single reproductive queen and survive for only a single season. However, in warmer climates, V. squamosa colonies sometimes persist for multiple years and can grow to extremely large size. We used genetic markers to understand patterns of reproduction and recruitment within these perennial colonies. We genotyped V. squamosa workers, pre-reproductive queens, and males from perennial colonies in the southeastern United States at 10 polymorphic microsatellite loci and one mitochondrial DNA locus. We found that V. squamosa from perennial nests were produced by multiple reproductives, in contrast to typical annual colonies. Relatedness of nestmates from perennial colonies was significantly lower than relatedness of nestmates from annual colonies. Our analyses of mitochondrial DNA indicated that most V. squamosa perennial colonies represented semiclosed systems whereby all individuals belonged to a single matriline despite the presence of multiple reproductive females. However, new queens recruited into perennial colonies apparently mated with non-nestmate males. Notably, perennial and annual colonies did not show significant genetic differences, supporting the hypothesis that perennial colony formation represents an instance of social plasticity. Overall, our results indicate that perennial V. squamosa colonies show substantial changes to their social biology compared to typical annual colonies and demonstrate variation in social behaviors in highly social species.

Lifetime reproductive benefits of cooperative polygamy vary for males and females in the acorn woodpecker (Melanerpes formicivorus).

Cooperative breeding strategies lead to short-term direct fitness losses when individuals forfeit or share reproduction. The direct fitness benefits of cooperative strategies are often delayed and difficult to quantify, requiring data on lifetime reproduction. Here, we use a longitudinal dataset to examine the lifetime reproductive success of cooperative polygamy in acorn woodpeckers (Melanerpes formicivorus), which nest as lone pairs or share reproduction with same-sex cobreeders. We found that males and females produced fewer young per successful nesting attempt when sharing reproduction. However, males nesting in duos and trios had longer reproductive lifespans, more lifetime nesting attempts and higher lifetime reproductive success than those breeding alone. For females, cobreeding in duos increased reproductive lifespan so the lifetime reproductive success of females nesting in duos was comparable to those nesting alone and higher than those nesting in trios. These results suggest that for male duos and trios, reproductive success alone may provide sufficient fitness benefits to explain the presence of cooperative polygamy, and the benefits of cobreeding as a duo in females are higher than previously assumed. Lifetime individual fitness data are crucial to reveal the full costs and benefits of cooperative polygamy.

Prolonged and variable copulation durations in a promiscuous insect species: No evidence of reproductive benefits for females.

Within promiscuous mating systems, copulation often functions as more than a means of fertilization, and copulation durations can vary widely. Copulating for prolonged durations can enhance both female and male reproductive success, but can also result in costs: females of some insect species experience increased fecundity and fertility through male-provided nutrition during prolonged copulations, but also decreased longevity due to male-driven mechanisms. Here, for a common, promiscuous insect species (the squash bug, Anasa tristis), we first describe the range of copulation duration, which spans from 2 min to over 23 h. To investigate whether female A. tristis benefit from prolonged copulation, we next manipulated copulation duration and female diet, and we documented the resulting fecundity, fertility, and longevity of each female. We found no evidence that prolonged copulation durations affect female reproductive success. Females produced fertile eggs after a single 30 min copulation, and they subsequently produced fertile eggs for an additional 4 weeks. Our findings suggest that females do not benefit from prolonged copulations, that sperm transfer occurs very early during copulations, and that females can store sperm for long durations. Consequently, we suggest that female harassment avoidance and male mate-guarding may explain prolonged copulations in this species.

Cooperative policing behaviour regulates reproductive division of labour in a termite.

Reproductive conflicts are common in insect societies where helping castes retain reproductive potential. One of the mechanisms regulating these conflicts is policing, a coercive behaviour that reduces direct reproduction by other individuals. In eusocial Hymenoptera (ants, bees and wasps), workers or the queen act aggressively towards fertile workers, or destroy their eggs. In many termite species (order Blattodea), upon the death of the primary queen and king, workers and nymphs can differentiate into neotenic reproductives and inherit the breeding position. During this process, competition among neotenics is inevitable, but how this conflict is resolved remains unclear. Here, we report a policing behaviour that regulates reproductive division of labour in the eastern subterranean termite, Reticulitermes flavipes. Our results demonstrate that the policing behaviour is a cooperative effort performed sequentially by successful neotenics and workers. A neotenic reproductive initiates the attack of the fellow neotenic by biting and displays alarm behaviour. Workers are then recruited to cannibalize the injured neotenic. Furthermore, the initiation of policing is age-dependent, with older reproductives attacking younger ones, thereby inheriting the reproductive position. This study provides empirical evidence of policing behaviour in termites, which represents a convergent trait shared between eusocial Hymenoptera and Blattodea.

Kinship ties across the lifespan in human communities.

A hypothesis for the evolution of long post-reproductive lifespans in the human lineage involves asymmetries in relatedness between young immigrant females and the older females in their new groups. In these circumstances, inter-generational reproductive conflicts between younger and older females are predicted to resolve in favour of the younger females, who realize fewer inclusive fitness benefits from ceding reproduction to others. This conceptual model anticipates that immigrants to a community initially have few kin ties to others in the group, gradually showing greater relatedness to group members as they have descendants who remain with them in the group. We examine this prediction in a cross-cultural sample of communities, which vary in their sex-biased dispersal patterns and other aspects of social organization. Drawing on genealogical and demographic data, the analysis provides general but not comprehensive support for the prediction that average relatedness of immigrants to other group members increases as they age. In rare cases, natal members of the community also exhibit age-related increases in relatedness. We also find large variation in the proportion of female group members who are immigrants, beyond simple traditional considerations of patrilocality or matrilocality, which raises questions about the circumstances under which this hypothesis of female competition are met. We consider possible explanations for these heterogenous results, and we address methodological considerations that merit increased attention for research on kinship and reproductive conflict in human societies. This article is part of the theme issue 'The evolution of female-biased kinship in humans and other mammals'.

Sex differences in the drivers of reproductive skew in a cooperative breeder.

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high-skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long-term genetic and observational data to examine factors affecting reproductive skew in the high-skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within-group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate-guarding and potentially reproductive restraint (for males). Ecological conditions or "outside options" affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.

Infanticide and within-clutch competition select for reproductive synchrony in a cooperative bird.

Reproduction among members of social animal groups is often highly synchronized, but neither the selective advantages nor the proximate causes of synchrony are fully understood. Here I investigate the evolution of hatching synchrony in the Greater Ani (Crotophaga major), a communally nesting bird in which several unrelated females contribute eggs to a large, shared clutch. Hatching synchrony is variable, ranging from complete synchrony to moderate asynchrony, and is determined by the onset of incubation of the communal clutch. Data from a 10-year field study indicate that individual reproductive success is highest in synchronous groups, and that nestlings that hatch in the middle of the hatching sequence are most likely to survive. Nestling mortality is high in asynchronous clutches because early-hatching nestlings are more likely to be killed by adult group members, whereas late-hatching nestlings are more likely to starve due competition with their older nest-mates. Therefore, the timing of hatching appears to be under stabilizing selection from infanticide and resource competition acting in concert. These results provide empirical support for models predicting that synchrony may evolve as an adaptive counter-strategy to infanticide, and they highlight the importance of competition in shaping the timing of reproduction in social groups.

A Simple Behavioral Model Predicts the Emergence of Complex Animal Hierarchies.

Social dominance hierarchies are widespread, but little is known about the mechanisms that produce nonlinear structures. In addition to despotic hierarchies, where a single individual dominates, shared hierarchies exist, where multiple individuals occupy a single rank. In vertebrates, these complex dominance relationships are thought to develop from interactions that require higher cognition, but similar cases of shared dominance have been found in social insects. Combining empirical observations with a modeling approach, we show that all three hierarchy structures-linear, despotic, and shared-can emerge from different combinations of simple interactions present in social insects. Our model shows that a linear hierarchy emerges when a typical winner-loser interaction (dominance biting) is present. A despotic hierarchy emerges when a policing interaction is added that results in the complete loss of dominance status for an attacked individual (physical policing). Finally, a shared hierarchy emerges with the addition of a winner-winner interaction that results in a positive outcome for both interactors (antennal dueling). Antennal dueling is an enigmatic ant behavior that has previously lacked a functional explanation. These results show how complex social traits can emerge from simple behaviors without requiring advanced cognition.

Major Hurdles for the Evolution of Sociality.

Why do most animals live solitarily, while complex social life is restricted to a few cooperatively breeding vertebrates and social insects? Here, we synthesize concepts and theories in social evolution and discuss its underlying ecological causes. Social evolution can be partitioned into (a) formation of stable social groups, (b) evolution of helping, and (c) transition to a new evolutionary level. Stable social groups rarely evolve due to competition over food and/or reproduction. Food competition is overcome in social insects with central-place foraging or bonanza-type food resources, whereas competition over reproduction commonly occurs because staying individuals are rarely sterile. Hence, the evolution of helping is shaped by direct and indirect fitness options and helping is only altruism if it reduces the helper's direct fitness. The helper's capability to gain direct fitness also creates within-colony conflict. This prevents transition to a new evolutionary level.

Elevated glucocorticoid concentrations during gestation predict reduced reproductive success in subordinate female banded mongooses.

Dominant females in social species have been hypothesized to reduce the reproductive success of their subordinates by inducing elevated circulating glucocorticoid (GC) concentrations. However, this 'stress-related suppression' hypothesis has received little support in cooperatively breeding species, despite evident reproductive skews among females. We tested this hypothesis in the banded mongoose (Mungos mungo), a cooperative mammal in which multiple females conceive and carry to term in each communal breeding attempt. As predicted, lower ranked females had lower reproductive success, even among females that carried to term. While there were no rank-related differences in faecal glucocorticoid (fGC) concentrations prior to gestation or in the first trimester, lower ranked females had significantly higher fGC concentrations than higher ranked females in the second and third trimesters. Finally, females with higher fGC concentrations during the third trimester lost a greater proportion of their gestated young prior to their emergence from the burrow. Together, our results are consistent with a role for rank-related maternal stress in generating reproductive skew among females in this cooperative breeder. While studies of reproductive skew frequently consider the possibility that rank-related stress reduces the conception rates of subordinates, our findings highlight the possibility of detrimental effects on reproductive outcomes even after pregnancies have become established.

Agonistic reciprocity is associated with reduced male reproductive success within haremic social networks.

While individual variation in social behaviour is ubiquitous and causes social groups to differ in structure, how these structural differences affect fitness remains largely unknown. We used social network analysis of replicate bluebanded goby (Lythrypnus dalli) harems to identify the reproductive correlates of social network structure. In stable groups, we quantified agonistic behaviour, reproduction and steroid hormones, which can both affect and respond to social/reproductive cues. We identified distinct, optimal social structures associated with different reproductive measures. Male hatching success (HS) was negatively associated with agonistic reciprocity, a network structure that describes whether subordinates 'reciprocated' agonism received from dominants. Egg laying was associated with the individual network positions of the male and dominant female. Thus, males face a trade-off between promoting structures that facilitate egg laying versus HS. Whether this reproductive conflict is avoidable remains to be determined. We also identified different social and/or reproductive roles for 11-ketotestosterone, 17ß-oestradiol and cortisol, suggesting that specific neuroendocrine mechanisms may underlie connections between network structure and fitness. This is one of the first investigations of the reproductive and neuroendocrine correlates of social behaviour and network structure in replicate, naturalistic social groups and supports network structure as an important target for natural selection.

The evolution of prolonged life after reproduction.

Why females of some species cease ovulation before the end of their natural lifespan is a longstanding evolutionary puzzle. For many species in captivity, post-reproductive life is simply an epiphenomenon of lengthened lifespan. Yet in natural populations of humans as well as some cetaceans and insects, reproductive senescence occurs much faster than somatic aging and females exhibit prolonged post-reproductive lifespans (PRLSs). Determining the mechanisms and functions that underpin PRLSs has proved a significant challenge. Here we bring together both classic and modern hypotheses proposed to explain PRLSs and discuss their application to both human and nonhuman animals. By taking an integrative and broad taxonomic approach we highlight the need to consider multiple interacting explanations for the evolution of PRLSs.

The origin and evolution of social insect queen pheromones: Novel hypotheses and outstanding problems.

Queen pheromones, which signal the presence of a fertile queen and induce daughter workers to remain sterile, are considered to play a key role in regulating the reproductive division of labor of insect societies. Although queen pheromones were long thought to be highly taxon-specific, recent studies have shown that structurally related long-chain hydrocarbons act as conserved queen signals across several independently evolved lineages of social insects. These results imply that social insect queen pheromones are very ancient and likely derived from an ancestral signalling system that was already present in their common solitary ancestors. Based on these new insights, we here review the literature and speculate on what signal precursors social insect queen pheromones may have evolved from. Furthermore, we provide compelling evidence that these pheromones should best be seen as honest signals of fertility as opposed to suppressive agents that chemically sterilize the workers against their own best interests.

Partial ovary development is widespread in honey bees and comparable to other eusocial bees and wasps.

Honey bee workers have few opportunities for direct reproduction because their ovary development is chemically suppressed by queens and worker-laid eggs are destroyed by workers. While workers with fully developed ovaries are rare in honey bee colonies, we show that partial ovary development is common. Across nine studies, an average of 6% to 43% of workers had partially developed ovaries in queenright colonies with naturally mated queens. This shift by workers toward potential future reproduction is linked to lower productivity, which suggests that even small investments in reproductive physiology by selfish workers reduce cooperation below a theoretical maximum. Furthermore, comparisons across 26 species of bees and wasps revealed that the level of partial ovary development in honey bees is similar to that of other eusocial Hymenoptera where there is reproductive conflict among colony members. Natural variation in the extent of partial ovary development in honey bee colonies calls for an exploration of the genetic and ecological factors that modulate shifts in cooperation within animal societies.

Costly reproductive competition between females in a monogamous cooperatively breeding bird.

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.