Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.     

Experimental evidence for kin-biased helping in a cooperatively breeding vertebrate

The widespread belief that kin selection is necessary for the evolution of cooperative breeding in vertebrates has recently been questioned. These doubts have primarily arisen because of the paucity of unequivocal evidence for kin preferences in cooperative behaviour. Using the cooperative breeding system of long-tailed tits (Aegithalos caudatus) in which kin and non-kin breed within each social unit and helpers are failed breeders, we investigated whether helpers preferentially direct their care towards kin following breeding failure. First, using observational data, we show that not all failed breeders actually become helpers, but that those that do help usually do so at the nest of a close relative. Second, we confirm the importance of kinship for helping in this species by conducting a choice experiment. We show that potential helpers do not become helpers in the absence of close kin and, when given a choice between helping equidistant broods belonging to kin and non-kin within the same social unit, virtually all helped at the nest of kin. This study provides strong evidence that kinship plays an essential role in the maintenance of cooperative breeding in this species.     

Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta

Evolutionary explanations of cooperative breeding based on kin selection have predicted that the individual contributions made by different helpers to rearing young should be correlated with their degree of kinship to the litter or brood they are raising. In the cooperative mongoose or meerkat, Suricata suricatta, helpers babysit pups at the natal burrow for the first month of pup life and frequent babysitters suffer substantial weight losses over the period of babysitting. Large differences in contributions exist between helpers, which are correlated with their age, sex and weight but not with their kinship to the young they are raising. Provision of food to some group members raises the contributions of individuals to babysitting. We discuss the implications of these results for evolutionary explanations of cooperative behaviour.     

Cooperative breeding and monogamy in mammalian societies

Comparative studies of social insects and birds show that the evolution of cooperative and eusocial breeding systems has been confined to species where females mate completely or almost exclusively with a single male, indicating that high levels of average kinship between group members are necessary for the evolution of reproductive altruism. In this paper, we show that in mammals, the evolution of cooperative breeding has been restricted to socially monogamous species which currently represent 5 per cent of all mammalian species. Since extra-pair paternity is relatively uncommon in socially monogamous and cooperatively breeding mammals, our analyses support the suggestion that high levels of average kinship between group members have played an important role in the evolution of cooperative breeding in non-human mammals, as well as in birds and insects.     

Pair and group breeding behaviour of a communal gallinule,the pukeko, Porphyrio P. Melanotus

Pukeko, Porphyrio porphyrio melanotus breed as pairs or groups and the breeding behaviour of individuals in all units is described and compared. Courtship, including copulation, occurred between all adult members in a territory although male-female copulations were most frequent. Low ranking yearlings were excluded from copulation. Participation in copulation by more than two birds was common, and, along with homosexual behaviour, is believed to help synchronize sexual cycles allowing several females to lay in the same nest at the same time. Only adults incubated, while all birds in a territory assisted with chick care, the degree of participation varying with status. In pair territories, older chicks helped feed younger chicks. Stable kin groups were more coordinated and showed less competitive aggression among members than non-kin groups of unstable membership. The significance of these results is discussed and it is argued that in a situation where an adult group is necessary for the defence of a breeding territory, then it is in the interests of all these individuals to participate in all breeding activities.     

Influence of Winter Ranging Behaviour on the Social Organization of a Cooperatively Breeding Bird Species, The Apostlebird

Most cooperative breeding bird species live in family groups that are formed through the prolonged association of offspring with their parents. Research into cooperative families has in particular investigated the balance between cooperation and conflict over reproductive decisions. As a consequence of this research focus, social interactions among group members outside the breeding season are rarely studied, despite the fact that they are likely to be crucial for social decisions. We investigated the social dynamics and ranging behaviour of the family group living cooperatively breeding apostlebird ( Struthidea cinerea ) outside the breeding season. Group size changed between, but not within, the seasons, being smaller during the breeding season than in the winter season. This change in group size was a consequence of breeding groups merging after breeding, then splitting again before the next breeding season. While breeding groups used small, non-overlapping home ranges (      = 113 ha) around the nesting site, during winter groups moved up to 1200 ha (      = 598 ha), and interacted frequently with up to four other winter groups. In particular large groups often joined together during winter and spent up to 50% of their time associating with other large winter groups. This apparent fission-fusion system facilitated the exchange of group members, offering the possibility to form new breeding coalitions and new groups. The results of this study suggest that behaviour outside the breeding season can be of considerable importance to the social dynamics of both families and cooperative breeding in such systems.     

Evolutionary routes to non-kin cooperative breeding in birds

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.     

Genetic structure, relatedness and helping behaviour in the yellow mongoose in a farmland and a natural habitat

The yellow mongoose Cynictis penicillata is a facultatively social species and provides an opportunity to study the evolution of social behaviour. We examined genetic structure, relatedness and helping behaviour in the yellow mongoose in natural habitat in the Kalahari Desert, where the species lives in small family groups of up to four individuals and shows no cooperative breeding; and in farmland in the Western Cape Province of South Africa, where they live in larger groups of up to 13 individuals, engage in numerous social interactions and show cooperative breeding. The farmland population showed significant inbreeding, and lower genetic variability than the desert population, but there was no evidence of a recent population bottleneck. The genetic relatedness between individuals within social groups and that between future potential helpers and pups were higher in the farmland population than in the desert population. However, based on a limited sample, helping effort (in the farmland population) was not preferentially directed towards kin. Thus, the origin of helping in the farmland population is consistent with kin selection, but in the absence of kin discrimination, future research should investigate whether long-term breeding opportunities or group augmentation contribute to maintaining cooperative breeding in this population.     

The evolution of cooperative breeding through group augmentation

Some individuals (helpers) in cooperatively breeding species provide alloparental care and often suppress their own reproduction. Kin selection is clearly an important explanation for such behaviour, but a possible alternative is group augmentation where individuals survive or reproduce better in large groups and where it therefore pays to recruit new members to the group. The evolutionary stability of group augmentation is currently disputed. We model evolutionarily stable helping strategies by following the dynamics of social groups with varying degrees of subordinate help. We also distinguish between passive augmentation, where a group member benefits from the mere presence of others, and active augmentation, where their presence as such is neutral or harmful, but where helping to recruit new group members may still be beneficial if they in turn actively provide help for the current reproductives ('delayed reciprocity'). The results show that group augmentation (either passive or active) can be evolutionarily stable and explain costly helping by non-reproductive subordinates, either alone or leading to elevated help levels when acting in concert with kin selection. Group augmentation can thus potentially explain the weak relationships between relatedness and helping behaviour that are observed in some cooperatively breeding species. In some cases, the superior mutualistic performance of cooperatively behaving groups can generate an incentive to stay and help which is strong enough to make ecological constraints unnecessary for explaining the stability of cooperatively breeding groups.     

Sex-specific associative learning cues and inclusive fitness benefits in the Seychelles warbler

In cooperative breeding vertebrates, indirect fitness benefits would be maximized by subordinates that accurately assess their relatedness to group offspring and preferentially help more closely related kin. In the Seychelles warbler (Acrocephalus sechellensis), we found a positive relationship between subordinate-nestling kinship (determined using microsatellite marker genotypes) and provisioning rates, but only for female subordinates. Female subordinates that helped were significantly more related to the nestlings than were nonhelpers, and the decision to help appears to be based on associative learning cues. High levels of female infidelity means that subordinates cannot trust their legitimacy through the male line, consequently they appear to use the continued presence of the primary female, but not the primary male, as a reliable cue to determine when to feed nestlings. By using effective discrimination, female subordinates are able to maximize the indirect benefits gained within a cooperative breeding system otherwise driven primarily by direct breeding benefits.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Cooperative investment in public goods is kin directed in communal nests of social birds

The tragedy of the commons predicts social collapse when public goods are jointly exploited by individuals attempting to maximize their fitness at the expense of other social group members. However, animal societies have evolved many times despite this vulnerability to exploitation by selfish individuals. Kin selection offers a solution to this social dilemma, but in large social groups mean relatedness is often low. Sociable weavers (Philetairus socius) live in large colonies that share the benefits of a massive communal nest, which requires individual investment for construction and maintenance. Here, we show that despite low mean kinship within colonies, relatives are spatially and socially clustered and that nest‐building males have higher local relatedness to other colony members than do non‐building males. Alternative hypotheses received little support, so we conclude that the benefits of the public good are shared with kin and that cooperative investment is, despite the large size and low relatedness of these communities, kin directed.     

Evolutionary ecology meets wildlife management: artificial group augmentation in the re-introduction of endangered African wild dogs (Lycaon pictus)

As an alternative to kin selection, group augmentation theory provides a framework for evolutionary mechanisms maintaining cooperative breeding when individual fitness is positively related to group size. It is expected that a cooperator group would accept or adopt unrelated foreigners when it is below a critical threshold size and group members could thus benefit from recruiting additional helpers. In re-introduction attempts, this would allow for a group to be augmented artificially before release, which would enhance its chance to establish itself successfully in the release area. This possibility was tested using endangered African wild dogs Lycaon pictus studied in Hluhluwe-iMfolozi Park, South Africa. Here, we report on the first successful artificial integration of an unrelated adult female with her three male pups into an existing pack. In addition, post-release monitoring data are presented, including how a yearling male displaced the dominant male that adopted him as a pup, adding to the controversy over the evolutionary stability of group augmentation as a route to cooperative breeding. This study thus demonstrates how theory from evolutionary ecology can be applied to practical wildlife management, and vice versa.     

Bell miner provisioning calls are more similar among relatives and are used by helpers at the nest to bias their effort towards kin

Kin selection predicts that helpers in cooperative systems should preferentially aid relatives to maximize fitness. In family-based groups, this can be accomplished simply by assisting all group members. In more complex societies, where large numbers of kin and non-kin regularly interact, more sophisticated kin-recognition mechanisms are needed. Bell miners (Manorina melanophrys) are just such a system where individuals regularly interact with both kin and non-kin within large colonies. Despite this complexity, individual helpers of both sexes facultatively work harder when provisioning the young of closer genetic relatedness. We investigated the mechanism by which such adaptive discrimination occurs by assessing genetic kinship influences on the structure of more than 1900 provisioning vocalizations of 185 miners. These 'mew' calls showed a significant, positive linear increase in call similarity with increasing genetic relatedness, most especially in comparisons between male helpers and the breeding male. Furthermore, individual helping effort was more heavily influenced by call similarity to breeding males than to genetic relatedness, as predicted if call similarity is indeed the rule-of-thumb used to discriminate kin in this system. Individual mew call structure appeared to be inflexible and innate, providing an effective mechanism by which helpers can assess their relatedness to any individual. This provides, to our knowledge, the first example of a mechanism for fine-scale kin discrimination in a complex avian society.     

The evolution of cooperative breeding in the African cichlid fish,Neolamprologus pulcher

The conundrum of why subordinate individuals assist dominants at the expense of their own direct reproduction has received much theoretical and empirical attention over the last 50 years. During this time, birds and mammals have taken centre stage as model vertebrate systems for exploring why helpers help. However, fish have great potential for enhancing our understanding of the generality and adaptiveness of helping behaviour because of the ease with which they can be experimentally manipulated under controlled laboratory and field conditions. In particular, the freshwater African cichlid, Neolamprologus pulcher, has emerged as a promising model species for investigating the evolution of cooperative breeding, with 64 papers published on this species over the past 27 years. Here we clarify current knowledge pertaining to the costs and benefits of helping in N. pulcher by critically assessing the existing empirical evidence. We then provide a comprehensive examination of the evidence pertaining to four key hypotheses for why helpers might help: (1) kin selection; (2) pay‐to‐stay; (3) signals of prestige; and (4) group augmentation. For each hypothesis, we outline the underlying theory, address the appropriateness of N. pulcher as a model species and describe the key predictions and associated empirical tests. For N. pulcher, we demonstrate that the kin selection and group augmentation hypotheses have received partial support. One of the key predictions of the pay‐to‐stay hypothesis has failed to receive any support despite numerous laboratory and field studies; thus as it stands, the evidence for this hypothesis is weak. There have been no empirical investigations addressing the key predictions of the signals of prestige hypothesis. By outlining the key predictions of the various hypotheses, and highlighting how many of these remain to be tested explicitly, our review can be regarded as a roadmap in which potential paths for future empirical research into the evolution of cooperative breeding are proposed. Overall, we clarify what is currently known about cooperative breeding in N. pulcher, address discrepancies among studies, caution against incorrect inferences that have been drawn over the years and suggest promising avenues for future research in fishes and other taxonomic groups.     

Cooperation‐mediated plasticity in dispersal and colonization

Kin selection theory predicts that costly cooperative behaviors evolve most readily when directed toward kin. Dispersal plays a controversial role in the evolution of cooperation: dispersal decreases local population relatedness and thus opposes the evolution of cooperation, but limited dispersal increases kin competition and can negate the benefits of cooperation. Theoretical work has suggested that plasticity of dispersal, where individuals can adjust their dispersal decisions according to the social context, might help resolve this paradox and promote the evolution of cooperation. Here, we experimentally tested the hypothesis that conditional dispersal decisions are mediated by a cooperative strategy: we quantified the density‐dependent dispersal decisions and subsequent colonization efficiency from single cells or groups of cells among six genetic strains of the unicellular Tetrahymena thermophila that differ in their aggregation level (high, medium, and low), a behavior associated with cooperation strategy. We found that the plastic reaction norms of dispersal rate relative to density differed according to aggregation level: highly aggregative genotypes showed negative density‐dependent dispersal, whereas low‐aggregation genotypes showed maximum dispersal rates at intermediate density, and medium‐aggregation genotypes showed density‐independent dispersal with intermediate dispersal rate. Dispersers from highly aggregative genotypes had specialized long‐distance dispersal phenotypes, contrary to low‐aggregation genotypes; medium‐aggregation genotypes showing intermediate dispersal phenotype. Moreover, highly aggregation genotypes showed evidence for beneficial kin‐cooperation during dispersal. Our experimental results should help to resolve the evolutionary conflict between cooperation and dispersal: cooperative individuals are expected to avoid kin‐competition by dispersing long distances, but maintain the benefits of cooperation by dispersing in small groups.     

Efficiency of selection for body weight in a cooperative village breeding program of Menz sheep under smallholder farming system

We evaluated the efficiency of selection for body weight in a cooperative village breeding program for Menz sheep of Ethiopia under smallholder farming system. The design of the program involved organizing villagers in a cooperative breeding group to implement selective breeding of their sheep. The program was jump-started through a one-time provision of elite rams from a central nucleus flock, but subsequent replacement rams were selected from within the village flocks. We also evaluated body weight trends in a village where cooperative breeding was not implemented and individual farmers managed their flocks under traditional breeding practices. Under traditional breeding practices, genetic progress over 8 years either stagnated or declined in all the weights recorded. In the cooperative villages, selection differentials of 2.44 and 2.45 kg were achieved in 2010 and 2011 selection seasons, respectively. Birth weight, 3-month weight and 6-month weight increased, respectively, by 0.49, 2.29 and 2.46 kg in the third-generation lambs over the base generation. Improved rams supplied from the central nucleus flock gave an initial genetic lift of 14.4% in the 6-month weight. This was higher than the gain achieved from selection in the village flocks, which was 5.2%. Our results showed that village-based genetic improvement in body weights under smallholder conditions could be feasible if appropriate designs are adopted and that commencing with elite central nucleus rams help jump-start village-based programs.     

Dispersal in Kin Coalition Throughout the Non‐Breeding Season to Facilitate Fine‐Scale Genetic Structure in the Breeding Season: Evidence From a Small Passerine

Evidence shows that social cooperation among kin may evolve even in birds with extensive dispersal. In such cases, maintaining kinship during dispersal is essential to the subsequent expression of kin cooperation. This hypothesis has not been examined for most bird species. We addressed it in the ground tit (Parus humilis), a passerine where kin frequently interact in terms of cooperative polygamy and extra‐pair mating despite fast annual turnover of the breeding population. Pedigree and genotype data showed that while groups varied in composition throughout the non‐breeding season due to continual individual emigration and immigration, they always contained kin coalitions consisting of either local or immigrant individuals of different age and sexes. The first‐order kin coalitions, according to the information from local individuals, stemmed from single‐family lineages (siblings and their parents), and the lower‐order ones from neighbouring, related family lineages that merged after fledging. It was probable that immigrants had formed kin coalitions in similar ways before dispersing. Groups broke up in the breeding season. Pairing between unrelated individuals from different coalitions within a group was more likely, whereas related individuals from the same coalition tended to nest near each other. The resulting fine‐scale population genetic structure is expected to facilitate breeding interactions among kin. Our findings give clues to understanding the evolution of social cooperation in relation to dispersal.     

Multiple benefits drive helping behavior in a cooperatively breeding bird: an integrated analysis

Several hypotheses exist to explain the seemingly altruistic helping behavior of cooperative breeders, although the general utility of these hypotheses remains unclear. While the potential importance of inclusive fitness benefits (kin selection) is traditionally widely appreciated, it is increasingly recognized that direct benefits may be more important than assumed. We use an integrative two-step framework to assess support for current hypotheses in purple-crowned fairy wrens, a species where subordinates vary in relatedness to breeders and helping increases productivity. After establishing that assumptions of pay-to-stay and social prestige hypotheses (predicting that helping functions as "paying rent" to stay on the territory or as a signal of individual quality, respectively) were not met and that parentage by subordinates is extremely rare, we tested whether subordinates adjusted nestling feeding rates following the predictions of the kin selection and group augmentation hypotheses. Benefits of kin selection result from investment in relatives, and group augmentation benefits accrue when subordinates invest more in their own future helpers, for example, when they have a better chance of inheriting the breeding position. We found that subordinates fed siblings more than unrelated nestlings, indicating that kin selection could facilitate cooperation. Moreover, the effect of relatedness on feeding effort varied depending on the probability of inheriting a breeding position, suggesting that active group augmentation can explain investment by unrelated subordinates. This statistical interaction would have gone undetected had we not considered both factors simultaneously, illustrating that a focus on single hypotheses could lead to underestimation of their importance in explaining cooperative breeding.     

Population dynamics of obligate cooperators

Obligate cooperative breeding species demonstrate a high rate of group extinction, which may be due to the existence of a critical number of helpers below which the group cannot subsist. Through a simple model, we study the population dynamics of obligate cooperative breeding species, taking into account the existence of a lower threshold below which the instantaneous growth rate becomes negative. The model successively incorporates (i) a distinction between species that need helpers for reproduction, survival or both, (ii) the existence of a migration rate accounting for dispersal, and (iii) stochastic mortality to simulate the effects of random catastrophic events. Our results suggest that the need for a minimum number of helpers increases the risk of extinction for obligate cooperative breeding species. The constraint imposed by this threshold is higher when helpers are needed for reproduction only or for both reproduction and survival. By driving them below this lower threshold, stochastic mortality of lower amplitude and/or lower frequency than for non-cooperative breeders may be sufficient to cause the extinction of obligate cooperative breeding groups. Migration may have a buffering effect only for groups where immigration is higher than emigration; otherwise (when immigrants from nearby groups are not available) it lowers the difference between actual group size and critical threshold, thereby constituting a higher constraint.