Grandparent helpers: the adaptive significance of older, postdominant helpers in the Seychelles warbler

The possibility that older, often nonreproductive, individuals may engage in kin-directed cooperative behavior has been largely overlooked in the study of cooperative breeding. Here, we describe and investigate the adaptive significance of such "grandparent" helpers in the Seychelles warbler, the first bird species in which this phenomenon has been observed. On Cousin Island, over a period of 24 years, a significant proportion (13.7%) of females, but few males (3.0%), was deposed from dominant positions. Deposed females were replaced by related females. However there was no evidence that older, senescent females were stepping aside to gain greater fitness benefits by increasing the reproductive success of their offspring, rather than breeding themselves; deposed females were not postreproductive, nor was being deposed linked to age or reproductive senescence. Of the deposed females, 68% became subordinates and helped to raise group offspring, accounting for ca. 10% of subordinates in any year. Demoted females were related (r= 0.24) to the group offspring and, consequently, could gain indirect benefits through helping. As direct benefits appeared to be limited, we suggest that indirect benefits have driven the evolution of such "grandparent helpers." This study now provides evidence for a new route to cooperative breeding in birds.     

Sex-biased preferential care in the cooperatively breeding Arabian babbler

In many social birds there are sex differences in dispersal patterns, with males commonly remaining in their natal group whereas females typically disperse at adolescence. Group members may therefore increase their fitness by preferentially caring for offspring of a particular sex according to social circumstances. Although previous studies have focussed on intragroup social factors that may affect preferential care, we propose that the relative size of neighbouring groups is of primary importance. Here we show that in the cooperatively breeding Arabian babbler (Turdoides squamiceps), parents preferentially feed male offspring when relative group size is small, and female offspring when group size is large. Unlike parents, helpers consistently favour young of the opposite sex to themselves, suggesting the risk of competition with members of the same sex for future breeding opportunities may override other considerations. These results emphasize the complexity of investment strategies in relation to social circumstances and the variable benefits of raising males vs. females in a species with sex-biased philopatry.     

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.     

Balancing contest competition,scramble competition,and social tolerance at feeding sites in wild common marmosets (Callithrix jacchus)

Models of primate sociality focus on the costs and benefits of group living and how factors such as rank, feeding competition, alliance formation, and cooperative behavior shape within‐group social relationships. We conducted a series of controlled field experiments designed to investigate how resource distribution (one or three of four reward platforms) and amount of food on a reward platform affected foraging strategies and individual feeding success in four groups of wild common marmosets (Callithrix jacchus) living in the Caatinga of northeastern Brazil. At our field site, common marmoset groups are characterized by a single breeding female who can produce twin litters twice per year, strong social cohesion, and cooperative infant care provided principally by several adult male helpers. We found that except for the dominant breeding female, rank (based on aggression) was not a strong predictor of feeding success. Although the breeding female in each group occupied the highest rank position and obtained the greatest daily feeding success, all other group members, including adults and juveniles experienced relatively equal feeding success across most experimental conditions. This was accomplished using a balance of behavioral strategies related to contest competition, scramble competition (associated with a finder's advantage), and social tolerance (sharing the same feeding platform). Based on these results, the social structure of common marmosets is best described as “single female dominance,” with the breeding female maximizing food intake needed to offset the energetic costs associated with reproductive twinning and the ability to produce two litters per year. Cooperative infant caregiving, in which the number of helpers is positively correlated with offspring survivorship, requires a set of behavioral strategies that serve to reduce contest competition and promote prosocial behaviors at feeding sites.     

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.     

Maintenance of Multifemale Social Organization in a Group of <Emphasis Type="Italic">Nomascus concolor</Emphasis> at Wuliang Mountain,Yunnan, China

Many short-term studies have reported groups of black crested gibbons containing ≥2 adult females (Nomascus concolor). We report the stability of multifemale groups in this species over a period of 6 yr. Our focal group and 2 neighboring groups included 2 breeding females between March 2003 and June 2009. We also habituated 1 multifemale group to observers and present detailed information concerning their social relationships over a 9-mo observation period. We investigated interindividual distances and agonistic behavior among the 5 group members. The spatial relationship between the 3 adult members (1 male, 2 females) formed an equilateral triangle. A subadult male was peripheral to the focal group, while a juvenile male maintained a closer spatial relationship with the adult members. We observed little agonistic behavior among the adult members. The close spatial relationship and lack of high rates of agonistic behavior among females suggest that the benefits of living in a multifemale group were equal to or greater than the costs for both females, given their ecological and social circumstances. The focal group occupied a large home range that was likely to provide sufficient food sources for the 2 females and their offspring. Between March 2003 and June 2009, 1 adult female gave 2 births and the other one gave 1 birth. All individuals in the focal group survived to June 2009. A long-term comparative study focused on females living in multifemale groups and females living in pair-living groups would provide insight into understanding the evolutionary mechanisms of the social system in gibbons.     

Modes of cooperation during territorial defense by African lions

Cooperation during territorial defense allows social groups of African lions to defend access to resources necessary for individual reproductive success. Some forms of cooperation will be dependent upon cognition: reciprocity places greater cognitive demands on participants than does kinship or mutualism. Lions have well-developed cognitive abilities that enable individuals to recognize and interact with others in ways that seem to enhance their inclusive fitness. Male lions appear to cooperate unconditionally, consistently responding to roaring intruders regardless of their male companions’ kinship or behavior. Female lions, however, do keep track of the past behavior of their female companions, apparently using the reliability of a companion as one means of assessing the risks posed by approaching intruders. Some “laggard” females may exploit the cooperative tendencies of “leaders” during territorial encounters. Although leader females clearly recognize laggards as such, the costs of tolerating laggards may be less than the benefits leaders gain through territorial defense behavior. Thus, although lions clearly have the cognitive ability to base cooperation on reciprocity, territorial defense cooperation appears instead to be based primarily on mutual benefits to participants for both male and female lions.     

Linear and Stable Dominance Hierarchies in Cooperative Carrion Crows

Cooperatively breeding birds typically form cohesive and stable groups that live year‐round in all purpose territories where competition for resources is likely to arise. Understanding how group members negotiate over resources is crucial because conflicts may disrupt the stability of the group and may ultimately hinder cooperation. However, social relationships within the group have been largely neglected so far. Here we investigated how cooperatively breeding carrion crows (Corvus corone corone) share a food source, by observing dyadic interactions in 29 territories that contained retained offspring of the breeding pair and/or immigrants. We found that crows formed linear and stable dominance hierarchies, which were stronger for males than females. We suggest that this difference mirrors the level of competition for resources other than food, such as reproduction and territory inheritance, which is higher in males than females. Interestingly, immigrant males dominated male offspring, suggesting that, for the resident breeder, which is the alpha member of the group, the benefits of an association with an immigrant overcome the costs of having his sons pushed down in the hierarchy. Our study uncovered the key factors that determine hierarchical relationships among cooperatively breeding crows and highlighted the need of focussing on social interactions in every context of group living to fully explain the dynamic of cooperation at the nest.     

Cooperative Breeding and Group Structure in the Lake Tanganyika Cichlid Neolamprologus savoryi

As yet, cooperative breeding has been described only for some fish species. However, evidence is accumulating that it is widespread among Lake Tanganyika cichlids. We studied the cooperative breeding system of the substrate breeding cichlid Neolamprologus savoryi. Breeding groups typically consisted of a large breeding male with one to four breeding females and three to 33 helpers (mean group size: 14.3 members). Group size was significantly related to breeding male and female body sizes, and larger males had more breeding females and larger sized male helpers. The size of the largest female in the group was positively related to the number and sizes of secondary breeding females and female helpers. In case of multiple breeding females, these females usually divided the group's territory into sub‐territories, each with its own helpers (subgroups). Interspersed between groups, independent fish were detected defending an individual shelter (4.4% of all fish). In 9% of the groups no breeding female was present. All group members participated in territory defence and maintenance, and showed submissive behaviours to larger group members. As expected, the level of between‐subgroup conflicts was high compared with the level of within‐subgroup conflicts. We compare these results with data available from other cooperatively breeding fishes.     

Reproductive success depends on the quality of helpers in the endangered,cooperative El Oro parakeet (Pyrrhura orcesi)

In cooperative species, helping behaviour and reproductive success can be correlated, but understanding this correlation is often impaired by the difficulty to correctly infer causation. While helpers can incur costs by participating in brood care, it is yet unclear if their help depends on their individual quality. We address these questions in the previously unknown cooperative breeding system of the endangered El Oro parakeet (Pyrrhura orcesi). Specifically, we ask (i) whether breeders benefit directly from helpers by an enhanced reproductive success and if so, (ii) whether the amount of this potential benefit is regulated by the quality of contributing group members. Groups consist of a dominant breeding pair accompanied by helpers, but cooperation is not obligate. Microsatellite heterozygosity was used to assess individual quality; its suitability as indicator of quality was reflected in the positive relationship between offspring heterozygosity and recruitment into the population. The reproductive success of breeding pairs depended on helper (genetic) quality and the number of helpers. This relationship occurred on two different levels: clutch size and fledging success, indicating (i) that females profit from high‐quality helpers and probably adjust clutch size accordingly and (ii) that the helpers increase fledging success. Congruently, we found that offspring body condition is positively affected by helper quality, which is most probably explained by the increased feeding rates when helpers are present. We suggest a causal link between cooperation and reproductive success in this frugivorous, endangered parakeet. Further, helper (genetic) quality can be a relevant factor for determining reproductive fitness in cooperative species, particularly in small and bottlenecked populations.     

Dispersal costs set the scene for helping in an atypical avian cooperative breeder

The ecological constraints hypothesis is suggested to explain the evolution of cooperative breeding in birds. This hypothesis predicts that the scene for cooperative breeding is set when ecological factors constrain offspring from dispersal. This prediction was tested in the atypical cooperative breeding system of the long-tailed tit, Aegithalos caudatus, by comparing the degree of philopatry and cooperation in an isolated and a contiguous site whilst experimentally controlling for confounding aspects of reproduction. No difference was found between the two sites in the survival of offspring but a greater proportion were found to remain philopatric in the isolated site. This difference was caused by greater philopatry of normally dispersive females suggesting, as predicted, that dispersal costs were greater from this site. Furthermore, a greater proportion of males and females cooperated following breeding failure in the isolated site than in the contiguous site. Thus, as has been suggested for typical avian cooperative breeders, dispersal costs, relative to philopatric benefits, appear to set the scene for cooperative breeding in long-tailed tits.     

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.     

Why aren’t we all hutterites?

In this paper I explore the psychology of ritual performance and present a simple graphical model that clarifies several issues in William Irons’s theory of religion as a “hard-to-fake” sign of commitment. Irons posits that religious behaviors or rituals serve as costly signals of an individual’s commitment to a religious group. Increased commitment among members of a religious group may facilitate intra-group cooperation, which is argued to be the primary adaptive benefit of religion. Here I propose a proximate explanation for how individuals are able to pay the short-term costs of ritual performance to achieve the long-term fitness benefits offered by religious groups. The model addresses three significant problems raised by Irons’s theory. First, the model explains why potential free-riders do not join religious groups even when there are significant net benefits that members of religious groups can achieve. Second, the model clarifies how costly a ritual must be to achieve stability and prevent potential free-riders from joining the religious group. Third, the model suggests why religious groups may require adherents to perform private rituals that are not observed by others. Several hypotheses generated from the model are also discussed. Richard Sosis is an assistant professor of anthropology at the University of Connecticut. His research interests include the evolution of cooperation, utopian societies, and the behavioral ecology of religion. In collaboration with Bradley Ruffle (Ben Gurion University) he is currently investigating the impact of privatization and religiosity on intra-group trust within Israeli Kibbutzim.     

Grooming relationships between breeding females and adult group members in cooperatively breeding moustached tamarins (Saguinus mystax)

Grooming is the most common form of affiliative behavior in primates that apart from hygienic and hedonistic benefits offers important social benefits for the performing individuals. This study examined grooming behavior in a cooperatively breeding primate species, characterized by single female breeding per group, polyandrous matings, dizygotic twinning, delayed offspring dispersal, and intensive helping behavior. In this system, breeding females profit from the presence of helpers but also helpers profit from staying in a group and assisting in infant care due to the accumulation of direct and indirect fitness benefits. We examined grooming relationships of breeding females with three classes of partners (breeding males, potentially breeding males, (sub)adult non-breeding offspring) during three reproductive phases (post-partum ovarian inactivity, ovarian activity, pregnancy) in two groups of wild moustached tamarins (Saguinus mystax). We investigated whether grooming can be used to regulate group size by either "pay-for-help" or "pay-to-stay" mechanisms. Grooming of breeding females with breeding males and non-breeding offspring was more intense and more balanced than with potentially breeding males, and most grooming occurred during the breeding females' pregnancies. Grooming was skewed toward more investment by the breeding females with breeding males during the phases of ovarian activity, and with potentially breeding males during pregnancies. Our results suggest that grooming might be a mechanism used by female moustached tamarins to induce mate association with the breeding male, and to induce certain individuals to stay in the group and help with infant care.     

Reproductive promiscuity in the splendid fairy-wren: effects of group size and auxiliary reproduction

Extrapair fertilizations complicate our understanding of cooperativebreeding in a number of ways. For example, auxiliaries may reducethe costs of seeking extrapair fertilizations for breeding malesor females, and auxiliary males may themselves seek copulationswith the breeding female in their own group. We employed microsatellitemarkers to examine patterns of parentage in the cooperativelybreeding splendid fairy-wren (Malurus splendens melanotus).Our study population exhibited a relatively high level of extrapairpaternity (42% of 386 offspring) with considerable annual variation(range = 24–52%). Across years the proportion of offspringsired by extrapair males was significantly correlated with theaverage number of auxiliaries per group. Furthermore, the proportionof extrapair young within a brood was related to group composition;groups with multiple auxiliaries were twice as likely as groupswith zero or one auxiliary to contain extrapair young. Mostoffspring were sired by dominant breeding males, but auxiliarymales sired approximately 25% of all extrapair young (10% ofall offspring), and about half of these were cases in whichthe auxiliary male sired offspring in his own group. Within-groupsirings by auxiliary males were most common after replacementof the breeding female, and they also appeared to be more likelywhen the auxiliary was not related to the breeding male. Thus,the presence of auxiliary males increased the likelihood thatfemales would produce extrapair young, and although incest avoidancemechanisms usually prevent within-group copulations by auxiliarymales, a conflict of interest among group males arises whena new female joins the group.     

Consequences of fluctuating group size for the evolution of cooperation

Studies of cooperation have traditionally focused on discrete games such as the well-known prisoner’s dilemma, in which players choose between two pure strategies: cooperation and defection. Increasingly, however, cooperation is being studied in continuous games that feature a continuum of strategies determining the level of cooperative investment. For the continuous snowdrift game, it has been shown that a gradually evolving monomorphic population may undergo evolutionary branching, resulting in the emergence of a defector strategy that coexists with a cooperator strategy. This phenomenon has been dubbed the ‘tragedy of the commune’. Here we study the effects of fluctuating group size on the tragedy of the commune and derive analytical conditions for evolutionary branching. Our results show that the effects of fluctuating group size on evolutionary dynamics critically depend on the structure of payoff functions. For games with additively separable benefits and costs, fluctuations in group size make evolutionary branching less likely, and sufficiently large fluctuations in group size can always turn an evolutionary branching point into a locally evolutionarily stable strategy. For games with multiplicatively separable benefits and costs, fluctuations in group size can either prevent or induce the tragedy of the commune. For games with general interactions between benefits and costs, we derive a general classification scheme based on second derivatives of the payoff function, to elucidate when fluctuations in group size help or hinder cooperation.     

Influences of Relatedness,Food Deprivation,and Sex on Adult Behaviors in the Group‐living Insect Forficula auricularia

The evolution of group living is generally associated with the emergence of social behaviors that ensure fitness benefits to group members. However, the expression of these behaviors may depend on group composition, which can vary over time with respect to sex, starvation status, and relatedness. Here, we investigated (1) whether adults of the group‐living European earwig, Forficula auricularia, show cooperative behaviors toward conspecifics and (2) whether sex, food availability, and relatedness shape the nature and frequency of these behaviors. We conducted a full‐factorial experiment using 108 unisexual pairs of adults, in which we manipulated these three factors and video‐recorded the earwig behaviors for 45 min. Our results revealed that adults mostly expressed self‐directed and aggressive behaviors. Nevertheless, they also showed allogrooming, a social behavior that offers scope for cooperation. Pairs of males displayed longer bouts of aggression and allogrooming (when it occurred) than pairs of females. Food deprivation had no effect on male behaviors, but females spent less time self‐grooming and walking when they were food deprived. Finally, low relatedness between adults did not influence any of the measured behaviors, but exacerbated frass production, possibly due to social stress. Overall, these results indicate the limited role of cooperation among F. auricularia adults during their group‐living phase.     

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.     

Temporal environmental variability drives the evolution of cooperative breeding in birds

Many vertebrates breed in cooperative groups in which more than two members provide care for young. Studies of cooperative breeding behavior within species have long highlighted the importance of environmental factors in mediating the paradox of why some such individuals delay independent breeding to help raise the offspring of others. In contrast, studies involving comparisons among species have not shown a similarly clear evolutionary-scale relationship between the interspecific incidence of cooperative breeding and any environmental factors. Here, we use a phylogenetically controlled comparative analysis of a complete, socially diverse group of birds-45 species of African starlings-to show that cooperative breeding is positively associated with living in semiarid savanna habitats and with temporal variability in rainfall. Savanna habitats are not only highly seasonal, but also temporally variable and unpredictable, and this temporal variability directly influences individual reproductive decisions in starlings and helps explain interspecific patterns of sociality. Cooperative breeding is likely to be adaptive in temporally variable environments because it allows for both reproduction in harsh years and sustained breeding during benign years. This "temporal variability" hypothesis might help explain the phylogenetic and geographic concentrations of cooperatively breeding vertebrates in savanna-like habitats and other temporally variable environments worldwide.     

Partner switching can favour cooperation in a biological market

Intraspecific cooperation and interspecific mutualisms can be promoted by mechanisms that reduce the frequency with which cooperative organisms are exploited by unhelpful partners. One such mechanism consists of changing partners after interacting with an uncooperative individual. I used McNamara et al.'s (Nature, 451, 2008, 189) partner switching model as a framework to examine whether this mechanism can select for increased cooperative investment by house sparrows (Passer domesticus) collaborating to rear offspring; previous research on this species has shown that substantial cooperative investments by both pair members are required to achieve high pay‐offs from collaborating. I found that the poorer the outcome of a breeding attempt relative to the number of eggs the female invested, the greater the likelihood of partner switching. The incidence of partner switching changed seasonally, with peak switching coinciding with an increase in the number of alternative partners available to females. After females switched partners, their breeding outcomes rose to match those of females that remained with the same partner; this was not the case for males that switched partners. Consistent with the model's prediction, males in stable partnerships achieved over 25% higher than average reproductive success, which was attributable to both persistently good breeding outcomes and their older partners' high fecundity. These results provide empirical support for the hypothesis that partner switching favours increased cooperative investment levels, and they demonstrate that variation in the relative value of by‐product benefits can enhance that process.