Dispersal of sibling coalitions promotes helping among immigrants in a cooperatively breeding bird

Kin selection is a major force in social evolution, but dispersal is often assumed to reduce its impact by diluting kinship. In most cooperatively breeding vertebrates, in which more than two individuals care for young, juveniles delay dispersal and become helpers in family groups. In long-tailed tits (Aegithalos caudatus), however, offspring disperse to breed and helpers are failed breeders that preferentially aid kin. Helping also occurs among immigrants, but their origins are unknown and cooperation in these cases is poorly understood. Here, we combine long-term demographic and genetic data from our study population to investigate immigration and helping in this species. We first used a novel application of parentage analysis to discriminate between immigrants and unknown philopatric recruits. We then cross-checked sibship reconstruction with pairwise relatedness estimates to show that immigrants disperse in sibling coalitions and helping among them is kin biased. These results indicate that dispersal need not preclude sociality, and dispersal of kin coalitions may help maintain kin-selected cooperation in the absence of delayed dispersal.     

Kin discrimination in cooperatively breeding long-tailed tits

Long-tailed tits Aegithalos caudatus are cooperative breeders in which helpers exhibit a kin preference in their cooperative behaviour. We investigated the mechanism through which this preference is achieved by first conducting an experiment for testing whether breeders could recognize the calls of their relatives while controlling for spatial effects. We found that there were significant differences in the responses of breeders to the vocalizations of kin and non-kin, suggesting that vocal cues may be used for kin recognition. We conducted a second experiment in order to investigate whether recognition is achieved on the basis of relatedness per se or through association. Nestlings were cross-fostered between unrelated broods in order to create broods composed of true and foster siblings. In subsequent years, survivors from experimental broods did not discriminate between true and fostered siblings when making helping decisions, indicating that recognition is learned and not genetically determined. We discuss the effectiveness of learning through association as an indirect cue to kinship.     

Schoolchildren cooperate more successfully with non-kin than with siblings

Cooperation plays a key role in the development of advanced societies and can be stabilized through shared genes (kinship) or reciprocation. In humans, cooperation among kin occurs more readily than cooperation among non-kin. In many organisms, cooperation can shift with age (e.g. helpers at the nest); however, little is known about developmental shifts between kin and non-kin cooperation in humans. Using a cooperative game, we show that 3- to 10-year-old French schoolchildren cooperated less successfully with siblings than with non-kin children, whether or not non-kin partners were friends. Furthermore, children with larger social networks cooperated better and the perception of friendship among non-friends improved after cooperating. These results contrast with the well-established preference for kin cooperation among adults and indicate that non-kin cooperation in humans might serve to forge and extend non-kin social relationships during middle childhood and create opportunities for future collaboration beyond kin. Our results suggest that the current view of cooperation in humans may only apply to adults and that future studies should focus on how and why cooperation with different classes of partners might change during development in humans across cultures as well as other long-lived organisms.     

Genetic analysis reveals diverse kin‐directed routes to helping in the rifleman Acanthisitta chloris

The social organization of cooperatively breeding species is extremely variable, with diverse social group composition and patterns of relatedness. Species that exhibit alternative routes to helping within the same population are potentially useful systems to investigate the causes and fitness consequences of diverse evolutionary pathways to cooperative behaviour. In this study, we use microsatellite markers and field observations to describe helping behaviour and patterns of relatedness in the unusual cooperative breeding system of the rifleman Acanthisitta chloris. First, we show that rifleman helpers consist of a remarkably diverse demographic, including males and females, who may be adult or juvenile, failed breeders or nonbreeders, or even successful breeders that simultaneously feed their own brood. Adult helpers mostly helped at first‐brood nests, while first‐brood juveniles assisted their parents at second broods. Second, we show that rifleman pairs are strictly sexually monogamous, and helpers did not gain any current reproductive success through helping. Third, genotyping showed that contrary to previous assumptions, helpers were closely related to the recipients of their care and preferentially directed care towards relatives over contemporaneous nests of nonrelatives. Finally, we show that variation in helper provisioning effort was attributed to age: juvenile helpers provisioned less than adults and were less responsive to the demands of a growing brood. Overall, our results show that the diverse routes to helping in this unusual species are driven by the common theme of kinship between helper and recipients, resulting in a previously underestimated potential for helpers to gain indirect fitness benefits.     

Kinship affects investment by helpers in a cooperatively breeding bird

Helping behaviour in cooperative breeding systems has been attributed to kin selection, but the relative roles of direct and indirect fitness benefits in the evolution of such systems remain a matter of debate. In theory, helpers could maximize the indirect fitness benefits of cooperation by investing more in broods with whom they are more closely related, but there is little evidence for such fine-scale adjustment in helper effort among cooperative vertebrates. In this study, we used the unusual cooperative breeding system of the long-tailed tit Aegithalos caudatus to test the hypothesis that the provisioning effort of helpers was positively correlated with their kinship to broods. We first use pedigrees and microsatellite genotypes to characterize the relatedness between helpers and breeders from a 14 year field study. We used both pedigree and genetic approaches because long-tailed tits have access to pedigree information acquired through social relationships, but any fitness consequences will be determined by genetic relatedness. We then show using both pedigrees and genetic relatedness estimates that alloparental investment by helpers increases as their relatedness to the recipients of their care increases. We conclude that kin selection has played a critical role in moulding the investment decisions of helpers in this cooperatively breeding species.     

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.     

Kin and social relationships in splendid fairy-wrens: recognition by song in a cooperative bird

Cooperatively breeding splendid fairy-wren,s Malurus splendens, were tested with songs recorded from individuals of known social and kin relationships. Both males and females sang and responded aggressively to songs of wrens from other social groups. Wrens responded similarly to songs of non-kin and songs of close kin in the absence of social familiarity with them. Breeding females responded more intensely to songs of helpers from other groups than to songs of helpers in their own group. The songs of male and female helpers elicited similar responses by breeding females. The response to other females may be associated with competition for breeding status and helpers. Two females sometimes breed in social groups with two older females; no interference was observed. Song may allow individuals to recognize other wrens in their group and to direct their behaviour towards non-dispersing relatives by location and social familiarity rather than by kinship identifiers.     

Kin Associations during Nest Founding in an Allodapine Bee Exoneura robusta: do Females Distinguish between Relatives and Familiar Nestmates?

True recognition of kin can have important fitness consequences in terms of directing altruistic behaviours toward close relatives (nepotism) and avoiding inbreeding. However, recent evidence suggests that some social insect species cannot or do not distinguish their closest relatives from among nestmates in important fitness-based contexts. Such findings are relevant to kin selection theories where individuals are expected to preferentially rear close relatives in order to gain inclusive fitness benefits. Here, allozyme markers are used to examine whether female Exoneura robusta individuals preferentially nest with their closest kin when given a choice of familiar previous nestmates. The results suggest these bees do not prefer kin over non-kin nestmates. Kin associations during nest founding in this species are probably due to philopatry and/or association with previously familiar nestmates.     

Helpers increase long-term but not short-term productivity in cooperatively breeding long-tailed tits

Helpers at the nest in the cooperative breeding system of long-tailedtits Aegithalos caudatus exhibit kin preference in their helpingbehavior. The aim of this study was to use multivariate analysesto investigate whether helpers accrue indirect fitness benefitsthrough their cooperation by increasing the productivity ofrelatives. All birds started each season breeding independentlyin pairs, but birds that failed in their own breeding attemptoften redirected their care to help another pair provision theiroffspring. About half of all broods had one or more helpers,86% of which were male. Provisioning rates increased and therewas a corresponding increase in the mass of nestlings withinbroods as the number of helpers increased. Helpers had no significantshort-term effect on productivity because nest predation, nestlingsurvival, and brood size were unaffected by the presence ofhelpers. However, in the long term helpers had a highly significanteffect on the recruitment of fledglings, the positive effectof helpers being linear within the range of helper numbers thatwe observed. We found no evidence to suggest that these resultswere confounded by the effects of individual or habitat quality.We conclude that long-tailed tits accrue indirect fitness benefitsby helping kin. Nevertheless, the inclusive fitness benefitfrom helping is substantially lower than that of independentbreeding, showing that helpers are making the best of a badjob.     

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.     

Kin selection, not group augmentation, predicts helping in an obligate cooperatively breeding bird

Kin selection theory has been the central model for understanding the evolution of cooperative breeding, where non-breeders help bear the cost of rearing young. Recently, the dominance of this idea has been questioned; particularly in obligate cooperative breeders where breeding without help is uncommon and seldom successful. In such systems, the direct benefits gained through augmenting current group size have been hypothesized to provide a tractable alternative (or addition) to kin selection. However, clear empirical tests of the opposing predictions are lacking. Here, we provide convincing evidence to suggest that kin selection and not group augmentation accounts for decisions of whether, where and how often to help in an obligate cooperative breeder, the chestnut-crowned babbler (Pomatostomus ruficeps). We found no evidence that group members base helping decisions on the size of breeding units available in their social group, despite both correlational and experimental data showing substantial variation in the degree to which helpers affect productivity in units of different size. By contrast, 98 per cent of group members with kin present helped, 100 per cent directed their care towards the most related brood in the social group, and those rearing half/full-sibs helped approximately three times harder than those rearing less/non-related broods. We conclude that kin selection plays a central role in the maintenance of cooperative breeding in this species, despite the apparent importance of living in large groups.     

Fine‐scale genetic structure and helping decisions in a cooperatively breeding bird

In animal societies, characteristic demographic and dispersal patterns may lead to genetic structuring of populations, generating the potential for kin selection to operate. However, even in genetically structured populations, social interactions may still require kin discrimination for cooperative behaviour to be directed towards relatives. Here, we use molecular genetics and long‐term field data to investigate genetic structure in an adult population of long‐tailed tits Aegithalos caudatus, a cooperative breeder in which helping occurs within extended kin networks, and relate this to patterns of helping with respect to kinship. Spatial autocorrelation analyses reveal fine‐scale genetic structure within our population, such that related adults of either sex are spatially clustered following natal dispersal, with relatedness among nearby males higher than that among nearby females, as predicted by observations of male‐biased philopatry. This kin structure creates opportunities for failed breeders to gain indirect fitness benefits via redirected helping, but crucially, most close neighbours of failed breeders are unrelated and help is directed towards relatives more often than expected by indiscriminate helping. These findings are consistent with the effective kin discrimination mechanism known to exist in long‐tailed tits and support models identifying kin selection as the driver of cooperation.     

Social organization and communal breeding in the chestnut-bellied starling (Spreo pulcher)

Chestnut-bellied starlings (Spreo pulcher) live in social groups of 10–30 individuals and during their breeding seasons maintain group ranges which show little overlap with neighbouring groups. A social group may contain two to six breeding pairs, non-breeding adults of both sexes, and immatures. Each breeding female has her own nest and she alone incubates. The parents and up to 12 other starlings feed the nestlings. Individual helpers may successively or simultaneously attend the nests of different breeders. The percentage of nests attended within a group differs for helpers of different sex, age and breeding status: immatures of 1–2 years and non-breeding adult males help most and adult females least. Nests with more helpers have higher fledging success than those with fewer helpers. These results are discussed with reference to the tentative benefits of helping behaviour and kinship relationships within the social group.     

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.     

How helpers help: disentangling ecological confounds from the benefits of cooperative breeding

Evolutionary explanations for helping in cooperative breeding systems usually require a positive effect of helping on the fitness of the breeders being assisted. However, such helper effects have proven surprisingly difficult to quantify. Cockburn et al . (this issue ) apply detailed statistical analyses to long-term field data on the enigmatic superb fairy-wren. They show that it is possible to disentangle the complex web of ecological and evolutionary interactions that confound so many studies. Whilst fairy-wren helpers may not increase nest productivity, they do increase future survival of breeding females. This study points the way for future statistical explorations of long-term data in other cooperative birds and mammals.     

Mating system, philopatry and patterns of kinship in the cooperatively breeding subdesert mesite Monias benschi

In the first molecular study of a member of the threatened avian family, Mesitornithidae, we used nine polymorphic microsatellite loci to elucidate parentage, patterns of within-group kinship and occurrence of extra-group paternity in the subdesert mesite Monias benschi, of southwest Madagascar. We found this cooperatively breeding species to have a very fluid mating system. There was evidence of genetic monogamy and polygynandry: of the nine groups with multiple offspring, six contained one breeding pair with unrelated helpers and three contained multiple male and female breeders with related helpers. Although patterns of within-group kinship varied, there was a strong positive relationship between group size and relatedness, suggesting that groups form by natal philopatry. There was also a strong positive correlation between within-sex and between-sex relatedness, indicating that unlike most cooperatively breeding birds, philopatry involved both sexes. In contrast to predictions of kin selection and reproductive skew models, all monogamous groups contained unrelated individuals, while two of the three polygynandrous groups were families. Moreover, although between-group variation in seasonal reproductive success was related to within-group female relatedness, relatedness among males and between the sexes had no bearing on a group's reproductive output. While kin selection may underlie helping behaviour in females, factors such as direct long-term fitness benefits of group living probably determine helping in males. Of the 14 offspring produced by fully sampled groups, at least two were sired by males from neighbouring groups: one by a breeding male and one by a nonbreeding male, suggesting that males may augment their reproductive success through extra-group paternity.     

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.     

Extrapair paternity, inclusive fitness, and within-group benefits of helping in western bluebirds

In central coastal California, USA, 3–16% of western bluebird ( Sialia mexicana ) pairs have adult male helpers at the nest. Demographic data on a colour-ringed population over a 13-year period indicate that helpers gain a small indirect fitness benefit through increases in the number of young fledged from nests of close kin. A small proportion of adult helpers (16%) that were able to breed and help simultaneously had higher annual inclusive fitness than males that only bred. These males comprised such a minor proportion of helpers that the mean fitness of helpers was still lower than the mean fitness of independent breeders. We used DNA fingerprinting to determine whether extrapair fertilizations alter within-group benefits enough to tip the balance in favour of helping behaviour. Overall, 19% of 207 offspring were sired by males other than their social father and extrapair fertilizations occurred in 45% of 51 nests. Intraspecific brood parasitism was rare so that mean mother-nestling relatedness approximated the expected value of 0.5. Extrapair paternity reduced putative father-offspring relatedness to 0.38. Mean helper-nestling relatedness was 0.41 for helpers assisting one or both parents and 0.28 for helpers aiding their brothers. Helpers rarely sired offspring in the nests at which they helped. Helping was not conditional on paternity and helpers were not significantly more closely related to offspring in their parents' nests than to offspring in their own nests. Although helpers may derive extracurricular benefits if helping increases their own or their father's opportunities for extrapair fertilizations, within-nest inclusive fitness benefits of helping do not compensate males for failing to breed. Breeding failure and constraints on breeding are the most likely explanations for why most helpers help.     

Helper contributions in the cooperatively breeding laughing kookaburra: feeding young is no laughing matter

I studied the contributions of individuals to incubation and nestling feeding in a population of cooperatively breeding laughing kookaburras, Dacelo novaeguineae. In most cooperatively breeding birds where nest success is limited by nestling starvation, related helpers increase the overall level of provisioning to the nest, thus boosting the production of nondescendent kin. However, although partial brood loss is the largest cause of lost productivity in kookaburra nests, additional helpers failed to increase overall provisioning. Instead, all group members, but especially helpers, reduced their feeding contributions as group size increased. Breeders and helpers reduced the size of prey delivered, and helpers also reduced the number of feeding visits. An important benefit of helping in kookaburras may be to allow all group members to reduce their effort. Within groups, contributions to care depended on status, sex, group size and the brood size. Breeding males delivered the most food. Breeding females provisioned less than their partner, but their effort was comparable to that of male helpers. Female helpers contributed the least food. Incubation effort followed similar patterns. The relatedness of helpers to the brood had no impact on their provisioning. Across all group sizes, helpers generally brought larger items to the nest than breeders. Copyright 2000 The Association for the Study of Animal Behaviour.     

No Evidence for Enforced Alloparental Care in a Cooperatively Breeding Parrot

In cooperatively breeding species, in which non‐breeding helpers assist in rearing the offspring of breeding individuals, conflicts of interest commonly occur between breeders and helpers over their respective contributions to offspring care. During such conflicts, breeders might use aggressive behavior to enforce contributions of helpers to offspring care, especially if helpers are not related to the breeders and their offspring and thus do not stand to gain indirect fitness benefits by helping. Using a combination of behavioral and genetic data, we investigated in the cooperatively breeding El Oro parakeet Pyrrhura orcesi (i) whether breeders are commonly dominant over helpers, (ii) whether they use aggressive behavior toward helpers to enforce offspring provisioning, and (iii) whether the relatedness of helpers to the nestlings affects the frequency of—or the reaction of helpers to—such aggressions. Even though breeders were generally dominant over helpers, we found no evidence for the enforcement of alloparental care. This finding was independent of the relatedness between helpers and nestlings, even though distantly related helpers overall contributed little to offspring care. We suggest that the inability of breeders to properly assess the work rates of their helpers at least partly explains the absence of enforcement. More generally, our results add to a body of evidence suggesting that enforcement might be an exceptional rather than a general mechanism underlying the expression of alloparental care in cooperatively breeding species.