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 personalities and social niche specialization in female meerkats

The social niche specialization hypothesis predicts that group‐living animals should specialize in particular social roles to avoid social conflict, resulting in alternative life‐history strategies for different roles. Social niche specialization, coupled with role‐specific life‐history trade‐offs, should thus generate between‐individual differences in behaviour that persist through time, or distinct personalities, as individuals specialize in particular nonoverlapping social roles. We tested for support for the social niche specialization hypothesis in cooperative personality traits in wild female meerkats (Suricata suricatta) that compete for access to dominant social roles. As cooperation is costly and dominance is acquired by heavier females, we predicted that females that ultimately acquired dominant roles would show noncooperative personality types early in life and before and after role acquisition. Although we found large individual differences in repeatable cooperative behaviours, there was no indication that individuals that ultimately acquired dominance differed from unsuccessful individuals in their cooperative behaviour. Early‐life behaviour did not predict social role acquisition later in life, nor was cooperative behaviour before and after role acquisition correlated in the same individuals. We suggest that female meerkats do not show social niche specialization resulting in cooperative personalities, but that they exhibit an adaptive response in personality at role acquisition.     

Variation in contributions to teaching by meerkats

Recent evidence from cooperative insect, bird and mammal societies has challenged the assumption that teaching is restricted to humans. However, little is known about the factors affecting the degree to which individuals in such societies contribute to teaching. Here, I examine variation in contributions to teaching in meerkats, where older group members teach pups to handle difficult prey. I show that investment in teaching varies with characteristics of pups, helpers, groups and ecological conditions. Although prior experience in caring for pups did not significantly influence teaching behaviour, younger helpers, which were still investing in growth, contributed less to teaching than older individuals. This suggests that, in common with other cooperative activities, contributions to teaching vary with the costs experienced by individual group members. However, in contrast to other forms of helping in meerkats, I detected no effects of nutritional state on teaching, suggesting that it carries relatively low costs. In species where individuals can potentially gain direct or indirect fitness benefits from facilitating learning in others, low costs divided among multiple group members may help tip the balance towards selection for teaching.     

Costs of cooperative behaviour in suricates (Suricata suricatta).

Functional interpretations of helping behaviour suggest that it has evolved because helpers increase their direct or indirect fitness by helping. However, recent critiques have suggested that helping may be an unselected extension of normal parental behaviour, pointing to evidence that all mature individuals commonly respond to begging young (whether they are parents, relatives or non-relatives) as well as to the lack of evidence that cooperative activities have appreciable costs to helpers. Here we provide an example of one form of cooperative behaviour that is seldom performed by parents and has substantial energetic costs to helpers. In the cooperative mongoose, Suricata suricatta, non-breeding adults commonly babysit young pups at the natal burrow for a day at a time, foregoing feeding for 24 hours. Parents rarely contribute to babysitting, and babysitting has substantial energetic costs to helpers. Members of small groups compensate for the reduced number of participants by babysitting more frequently, and neither the proportion of time that babysitters are present nor the survival of litters vary with group size.     

Behavioural tactics of breeders in cooperative meerkats

In eusocial invertebrates, queens commonly show morphological and behavioural modifications to their role as the principal breeders in their colonies. With the exception of naked mole-rats, Heterocephalus glaber, morphological modification of breeders has yet to be shown in cooperative vertebrates, but the behaviour of dominant individuals may be modified so as to maximize reproductive success. We studied the cooperative behaviour of dominant and subordinate adults in meerkats, Suricata suricatta, and found that the decision rules governing the contributions of dominant breeders differed from those of subordinate helpers. Dominant breeders contributed less than adult helpers to babysitting and pup feeding, but raised their individual contributions to pup care to a greater extent when helper:pup ratios were low. In contrast to subordinates, dominant breeders did not increase their contributions when they foraged successfully. Finally, while subordinates of both sexes assisted in rearing the young when dominants bred, dominant females contributed little when subordinates attempted to breed, and male helpers (but not females) reduced their contributions to the care of pups. Our results suggest that the division of labour between breeders and helpers in meerkats is intermediate between that of facultatively cooperative species, where parents are principally responsible for rearing young, and that of specialized eusocial species, which show a well-defined division of labour between breeders and workers.     

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as ‘animal personality’ or a ‘behavioural syndrome’. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.     

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.     

Temporal variation in fitness payoffs promotes cooperative breeding in long-tailed tits Aegithalos caudatus

Cooperative breeding is paradoxical because some individuals forego independent reproduction and instead help others to reproduce. The ecological constraints model states that such behavior arises because of constraints on independent reproduction. Spatial variation in constraints has been shown to co-vary with the incidence of cooperative breeding in correlational and experimental studies. Here, we examine whether temporally variable ecological constraints can act in a similar way to promote cooperative breeding in the atypical system of long-tailed tits Aegithalos caudatus. In this species, individuals may switch reproductive tactics from breeding to helping within the same breeding season. Using 7 yr of field data, we show that reproductive success declined seasonally because of declines in brood size, nestling weight, and juvenile survival. The survival to breeding age of chicks from nests with helpers was higher than for chicks from nests without helpers, and since helpers usually helped at the nest of a close relative, they accrued inclusive fitness benefits. We used these data to model the expected fitness payoffs of breeding and helping at different times during the season. The model shows that late in the breeding season, the fitness payoff from a kin-directed helping tactic becomes greater than that from independent breeding. The behavioral switch predicted by the model is consistent with the observed switch from breeding to helping, which shows that cooperative breeding may evolve as a way of making the best of a bad job at the end of a temporally constrained breeding season.     

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 and helper effects in the cooperatively breeding grey-crowned babbler

Cooperative breeding, where some individuals help to raise offspring that are not their own, is a relatively rare social system in birds. We studied the breeding biology of a declining cooperative breeder, the grey-crowned babbler Pomatostomus temporalis , with the aim of isolating the social factors that affect its reproductive success. Most breeding pairs were assisted by philopatric offspring, although pairs could breed successfully without helpers. Females laid up to four clutches (usually three eggs per clutch) per season. Male (but not female) helpers increased the number of young fledged from individual nests and the likelihood of re-nesting, resulting in higher seasonal fledgling production. Helper effects on brood size and fledgling production were greater in the second year of the study, which was also characterized by higher nest failure. This suggests that helpers enhance reproduction more in poor conditions. Our study demonstrates the interacting effects of social and ecological factors on reproductive success, and that retention of offspring is not always beneficial for the breeders in cooperative species.     

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.     

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.     

Determinants of reproductive success in dominant female meerkats

1. In cooperative societies with high reproductive skew, selection on females is likely to operate principally through variation in the probability of acquiring dominant status and variation in reproductive success while dominant. Despite this, few studies of cooperative societies have investigated the factors that influence which females become dominant, and/or their reproductive output while in the dominant position. 2. Here we use long-term data from a wild meerkats population to describe variation in the breeding success of dominant female meerkats Suricata suricatta and investigate its causes. 3. Female meerkats compete intensely for breeding positions, and the probability of acquiring the breeding role depends upon a female's age in relation to competitors and her weight, both at the time of dominance acquisition and early in life. 4. Once dominant, individual differences in breeding success depend principally on the duration of dominance tenure. Females remain for longer in the dominant position if they are heavier than their competitors at the start of dominance, and if the number of adult female competitors at the start is low. 5. Female breeding success is also affected by variation in fecundity and pup survival, both of which increase with group size. After controlling for these effects, female body weight has a positive influence on breeding rate and litter size, while the number of adult female competitors reduces litter survival. 6. These findings suggest that selection for body weight and competitive ability will be high in female meerkats, which may moderate their investment in cooperative activities. We suggest that similar consequences of competition may occur among females in other cooperative societies where the benefits of attaining dominance status are high.     

Elevated prolactin levels immediately precede decisions to babysit by male meerkat helpers

Recent studies suggest that decisions to care for the offspring of others in societies of cooperative vertebrates may have a hormonal basis. The crucial question of whether changes in hormone levels immediately precede or merely follow bouts of offspring care, however, remains largely unanswered. Here, we show that in wild groups of cooperatively breeding meerkats, male helpers that decided to babysit for the day had significantly higher levels of prolactin, coupled with lower levels of cortisol, before initiating a babysitting session compared with similarly aged individuals that decided to forage. In addition, these hormonal differences disappeared over the course of the day, suggesting that hormone levels changed in a fundamentally different way in meerkats that babysat versus those that foraged. In contrast, long-term contributions to babysitting were not significantly associated with plasma levels of prolactin, cortisol, or testosterone in individual male helpers. Our results show, for the first time, that elevated levels of prolactin may immediately precede bouts of helping behavior but differ from recent findings on the same study population in which plasma levels of cortisol, but not prolactin, were significantly and positively associated with rates of pup feeding by male helpers. Together, these results lend significant weight to the idea that decisions to help in cooperative vertebrates have a hormonal basis, although different hormones appear to be associated with different types of care.     

Helpers in a cooperatively breeding cichlid stay and pay or disperse and breed, depending on ecological constraints

The theory of family-group dynamics predicts that group structure, helping behaviour and social interactions among group members should vary with the opportunities of subordinates to breed independently. We investigated experimentally whether unrelated mature helpers in the cooperatively breeding cichlid Neolamprologus pulcher reduce costly social and cooperative behaviour and choose to disperse and breed independently when offered vacant breeding sites. As predicted by the ecological constraints hypothesis,when breeding substrate was available, (i) helpers spent more time in dispersal areas and it was mainly large helpers that left the group to breed independently; (ii) all helpers invested less in costly submissive behaviours towards other group members and large helpers reduced help, supporting the 'pay-to-stay' hypothesis; and (iii) large helpers, particularly those that dispersed and bred, increased more in body mass in the treatment than those without breeding options, suggesting status-dependent strategic growth of helpers.We conclude that helpers of N. pulcher decide whether to stay and pay or disperse and breed in response to constraints on independent breeding.     

Facultative sex ratio adjustment by western bluebird mothers with stay-at-home helpers-at-the-nest

Although population sex ratios rarely deviate from unity, the sex ratio of individual mothers should be labile, allowing them to bias their sex ratios in favour of the more successful sex when they can expect a difference in the mean reproductive value of their daughters and sons. Just how mothers should bias sex allocation is particularly complicated in cooperative breeders, because the adaptive sex ratio may be influenced by conflicting impacts of helpers on their parents' fitness via ‘local resource enhancement’ and ‘local resource competition’. In western bluebirds, Sialia mexicana, breeding-age helpers-at-the-nest are exclusively male and increase their parents' nesting success in the current year. As such, they are viewed as helpers, not hinderers, even though by failing to gain a breeding position they reduce their parents' annual inclusive fitness below that of parents with a breeding son. In this study, I tested the hypothesis that nonbreeding, stay-at-home helpers indicate poor breeding prospects for locally competing sons, and investigated one prediction of this hypothesis that such helpers also indicate a tendency for parents to produce substandard sons. A female removal experiment showed that female mates were in short supply. Pairs had daughter-biased broods when they had a stay-at-home helper son that failed to get a mate in the first place, but not when they had a helper that had been breeding on his own, but returned home to help sometime after his mother finished laying her eggs. Stay-at-home sons were not developmentally delayed relative to breeders of the same cohort, suggesting that helpers may not be inferior to breeders. Although the population sex ratio fluctuates about unity, a multiyear data set showed a negative relationship between the frequency of helping and the annual brood sex ratio for the population. These results suggest that local resource competition outweighs local resource enhancement in driving individual and population sex ratio variation in western bluebirds, a pattern that would not be predicted based on the simple question of whether helpers help or hinder at the nest.     

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.     

Cortisol levels are positively associated with pup-feeding rates in male meerkats

In societies of cooperative vertebrates, individual differences in contributions to offspring care are commonly substantial. Recent attempts to explain the causes of this variation have focused on correlations between contributions to care and the protein hormone prolactin, or the steroid hormone testosterone. However, such studies have seldom considered the importance of other hormones or controlled for non-hormonal factors that are correlative with both individual hormone levels and contributions to care. Using multivariate statistics, we show that hormone levels explain significant variation in contributions to pup-feeding by male meerkats, even after controlling for non-hormonal effects. However, long-term contributions to pup provisioning were significantly and positively correlated with plasma levels of cortisol rather than prolactin, while plasma levels of testosterone were not related to individual patterns of pup-feeding. Furthermore, a playback experiment that used pup begging calls to increase the feeding rates of male helpers gave rise to parallel increases in plasma cortisol levels, whilst prolactin and testosterone levels remained unchanged. Our findings confirm that hormones can explain significant amounts of variation in contributions to offspring feeding, and that cortisol, not prolactin, is the hormone most strongly associated with pup-feeding in cooperative male meerkats.     

The evolutionary ecology of alternative migratory tactics in salmonid fishes

Extensive individual variation in spatial behaviour is a common feature among species that exhibit migratory life cycles. Nowhere is this more evident than in salmonid fishes; individual fish may complete their entire life cycle in freshwater streams, others may migrate variable distances at sea and yet others limit their migrations to larger rivers or lakes before returning to freshwater streams to spawn. This review presents evidence that individual variation in migratory behaviour and physiology in salmonid fishes is controlled by developmental thresholds and that part of the variation in proximal traits activating the development of alternative migratory tactics is genetically based. We summarize evidence that alternative migratory tactics co‐exist within populations and that all individuals may potentially adopt any of the alternative phenotypes. Even though intra‐specific genetic divergence of migratory tactics is uncommon, it may occur if female competition for oviposition sites results in spawning segregation of alternative phenotypes. Because of their polygenic nature, alternative migratory tactics are considered as threshold traits. Threshold traits have two characteristics: an underlying 'liability' trait that varies in a continuous fashion, and a threshold value which is responsible for the discreetness observed in phenotypic distribution. We review evidence demonstrating that body size is an adequate proxy for the liability trait controlling the decision to migrate, but that the same phenotypic outcome (anadromy or residency) may be reached by different developmental pathways. The evidence suggesting a significant heritable component in the development of alternative migratory tactics is subsequently reviewed, leading us to conclude that alternative migratory tactics have considerable potential to respond to selection and evolve. We review what is known about the proximal physiological mechanisms mediating the translation of the continuous value of the liability trait into a discontinuous migratory tactic. We conclude by identifying several avenues for future research, including testing the frequency‐dependent selection hypothesis, establishing the relative importance of adaptive phenotypic plasticity in explaining some geographic gradients in migratory behaviour and identifying the physiological and genetic basis of the switching mechanisms responsible for alternative migratory tactics.     

Consistent individual differences in cooperative behaviour in meerkats (Suricata suricatta)

Although recent models for the evolution of personality, using game theory and life‐history theory, predict that individuals should differ consistently in their cooperative behaviour, consistent individual differences in cooperative behaviour have rarely been documented. In this study, we used a long‐term data set on wild meerkats to quantify the repeatability of two types of cooperative care (babysitting and provisioning) within individuals and examined how repeatability varied across age, sex and status categories. Contributions to babysitting and provisioning were significantly repeatable and positively correlated within individuals, with provisioning more repeatable than babysitting. While repeatability of provisioning was relatively invariant across categories of individuals, repeatability of babysitting increased with age and was higher for subordinates than dominants. These results provide support for theoretical predictions that life‐history trade‐offs favour the evolution of consistent individual differences in cooperative behaviour and raise questions about why some individuals consistently help more than others across a suite of cooperative behaviours.