Hamilton's rule and the causes of social evolution

Hamilton''s rule is a central theorem of inclusive fitness (kin selection) theory and predicts that social behaviour evolves under specific combinations of relatedness, benefit and cost. This review provides evidence for Hamilton''s rule by presenting novel syntheses of results from two kinds of study in diverse taxa, including cooperatively breeding birds and mammals and eusocial insects. These are, first, studies that empirically parametrize Hamilton''s rule in natural populations and, second, comparative phylogenetic analyses of the genetic, life-history and ecological correlates of sociality. Studies parametrizing Hamilton''s rule are not rare and demonstrate quantitatively that (i) altruism (net loss of direct fitness) occurs even when sociality is facultative, (ii) in most cases, altruism is under positive selection via indirect fitness benefits that exceed direct fitness costs and (iii) social behaviour commonly generates indirect benefits by enhancing the productivity or survivorship of kin. Comparative phylogenetic analyses show that cooperative breeding and eusociality are promoted by (i) high relatedness and monogamy and, potentially, by (ii) life-history factors facilitating family structure and high benefits of helping and (iii) ecological factors generating low costs of social behaviour. Overall, the focal studies strongly confirm the predictions of Hamilton''s rule regarding conditions for social evolution and their causes.     

Lifetime monogamy and the evolution of eusociality

All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton''s rule (br_s > r_oc), but implies that relatedness cancels out of the equation because average relatedness to siblings (r_s) and offspring (r_o) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton''s rule.     

Quantitative genetic versions of Hamilton's rule with empirical applications

Hamilton''s theory of inclusive fitness revolutionized our understanding of the evolution of social interactions. Surprisingly, an incorporation of Hamilton''s perspective into the quantitative genetic theory of phenotypic evolution has been slow, despite the popularity of quantitative genetics in evolutionary studies. Here, we discuss several versions of Hamilton''s rule for social evolution from a quantitative genetic perspective, emphasizing its utility in empirical applications. Although evolutionary quantitative genetics offers methods to measure each of the critical parameters of Hamilton''s rule, empirical work has lagged behind theory. In particular, we lack studies of selection on altruistic traits in the wild. Fitness costs and benefits of altruism can be estimated using a simple extension of phenotypic selection analysis that incorporates the traits of social interactants. We also discuss the importance of considering the genetic influence of the social environment, or indirect genetic effects (IGEs), in the context of Hamilton''s rule. Research in social evolution has generated an extensive body of empirical work focusing—with good reason—almost solely on relatedness. We argue that quantifying the roles of social and non-social components of selection and IGEs, in addition to relatedness, is now timely and should provide unique additional insights into social evolution.     

Parent—offspring conflict: the full-sib—half-sib fallacy

R. L. Trivers used Hamilton''s rule regarding the evolution of altruistic behaviour to demonstrate the occurrence of parent–offspring conflict and concluded that this would be more severe when future offspring were half siblings rather than full siblings of the offspring currently receiving investment. Here we show that Trivers'' formulation applies in a limited range of circumstances and offer an alternative formulation that is universally applicable. Under this formulation the optimal investment from the offspring''s point of view in species with uniparental care and, hence, the extent of parent–offspring conflict depends on the cost of the caring parent''s investment to the future fitness of the non-caring parent.     

Helpers at the nest improve late-life offspring performance: evidence from a long-term study and a cross-foster experiment

Background

Conditions during an individual''s rearing period can have far reaching consequences for its survival and reproduction later in life. Conditions typically vary due to variation in parental quality and/or the environment, but in cooperative breeders the presence of helpers adds an important component to this. Determining the causal effect of helpers on offspring fitness is difficult, since high-quality breeders or territories are likely to produce high-quality offspring, but are also more likely to have helpers because of past reproductive success. This problem is best resolved by comparing the effect of both helping and non-helping subordinates on offspring fitness, however species in which both type of subordinates commonly occur are rare.

Methodology/Principal Findings

We used multi-state capture-recapture models on 20 years of data to investigate the effect of rearing conditions on survival and recruitment in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis), with both helping and non-helping subordinates. The number of helpers in the rearing territory, but not territory quality, group- or brood size, was positively associated with survival of offspring in their first year, and later in life. This was not a result of group size itself since the number of non-helpers was not associated with offspring survival. Furthermore, a nestling cross-foster experiment showed that the number of helpers on the pre-foster territory was not associated with offspring survival, indicating that offspring from territories with helpers do not differ in (genetic) quality.

Conclusions/Significance

Our results suggest that the presence of helpers not only increase survival of offspring in their first year of life, but also subsequent adult survival, and therefore have important fitness consequences later in life. This means that when calculating the fitness benefits of helping not only short-term but also the late-life benefits have to be taken into account to fully understand the evolution of cooperative breeding.     

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.     

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.     

Lower group productivity under kin-selected reproductive altruism

Abstract Hamilton's rule provides the foundation for understanding the genetic evolution of social behavior, showing that altruism is favored by increased relatedness and increased productivity of altruists. But how likely is it that a new altruistic mutation will satisfy Hamilton's rule by increasing the reproductive efficiency of the group? Altruism per se does not improve efficiency, and hence we would not expect a typical altruistic mutation to increase the mean productivity of the population. We examined the conditions under which a mutation causing reproductive altruism can spread when it does not increase productivity. We considered a population divided into temporary groups of genetically similar individuals (typically family groups). We show that the spread of altruism requires a pleiotropic link between altruism and enhanced productivity in diploid organisms, but not in haplodiploid organisms such as Hymenoptera. This result provides a novel biological understanding of the barrier to the spread of reproductive altruism in diploids. In haplodiploid organisms, altruism within families that lowers productivity may spread, provided daughters sacrifice their own reproduction to raise full‐sisters. We verified our results using three single‐locus genetic models that explore a range of the possible reproductive costs of helping. The advantage of female‐to‐female altruism in haplodiploids is a well‐known prediction of Hamilton's rule, but its importance in relaxing the linkage between altruism and efficiency has not been explored. We discuss the possible role of such unproductive altruism in the origins of sociality. We also note that each model predicts a large region of parameter space were polymorphism between altruism and selfishness is maintained, a pattern independent of dominance.     

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.     

Broodcare helpers in the cichlid fish Lamprologus brichardi: Their costs and benefits

‘Helping’ in birds and mammals involves seemingly altruistic behaviour. In the cichlid fish Lamprologus birchardi helpers are usually young of former broods staying in their parents' territories and participating in all kinds of parental duties (Broodcare, territory maintenance and defence). The discovery of helpers in fish offered the chance of attempting an extensive analysis of potential costs and benefits influencing the evolution of helpers in a vertebrate. Three factors proved to be of major importance in the cost-benefit analysis of helping as opposed to leaving for family-independent nonreproductive aggregations. Due to investment and to their rank within a family's hierarchy, helpers grow at a slower rate than non-helpers. This cost is compensated for by (i) a lower mortality risk to helpers caused by their access to a defended shelter and by protection afforded by bigger family members, and (ii) a positive contribution by helpers to the future reproductive success of their parents: females with helpers produce bigger clutches and consequently more free-swimming fry (=siblings). Other variables, such as the helpers' influence on the relative breeding success of their parents, broodcare experience through helping, the chances of territory take-over, parasitism of parents' reproduction and cannibalism are of minor importance. Similar social organizations in other fish are discussed with respect to their ecology and are compared with cooperatively breeding birds and mammals.     

Investment and relatedness: A cost/benefit analysis of breeding and helping in the pied kingfisher (Ceryle rudis)

Helping at the nest in birds is often termed altruism. However, so far, no study has ever demonstrated high costs to a helper's own lifetime reproductive success (=direct fitness), nor its compensation through benefits from relatives other than its own offspring (=indirect fitness). In this paper on pied kingfishers (Ceryle rudis) the relationship between investment, relatedness and inclusive fitness (expressed in terms of genetic equivalents) is investigated for breeding males, and males that help either relatives (=primary helpers) or strangers (=secondary helpers). With respect to guarding nests against predators and feeding young, primary helpers invest as much as breeders, but secondary helpers contribute significantly less. These differences in status and investment (measured in energy expenditure) affect the birds' future to such an extent that primary helpers have a lower chance of surviving and mating than secondary helpers. However, their costs in direct fitness are compensated by pronounced benefits to indirect fitness, resulting from improved survival of siblings and parents. An attempt is made to calculate the inclusive fitness of birds following different strategies over a 2-year period. It is concluded that (a) breeding is superior to helping and helping superior to doing nothing and (b) that kin-selection must be invoked to explain why surplus males choose the more costly primary helper strategy instead of the cheaper secondary helper strategy. Alternative explanations, including group selection, parental manipulation and reciprocity, are discussed.     

A quantitative test of Hamilton's rule for the evolution of altruism

The evolution of altruism is a fundamental and enduring puzzle in biology. In a seminal paper Hamilton showed that altruism can be selected for when rb - c > 0, where c is the fitness cost to the altruist, b is the fitness benefit to the beneficiary, and r is their genetic relatedness. While many studies have provided qualitative support for Hamilton's rule, quantitative tests have not yet been possible due to the difficulty of quantifying the costs and benefits of helping acts. Here we use a simulated system of foraging robots to experimentally manipulate the costs and benefits of helping and determine the conditions under which altruism evolves. By conducting experimental evolution over hundreds of generations of selection in populations with different c/b ratios, we show that Hamilton's rule always accurately predicts the minimum relatedness necessary for altruism to evolve. This high accuracy is remarkable given the presence of pleiotropic and epistatic effects as well as mutations with strong effects on behavior and fitness (effects not directly taken into account in Hamilton's original 1964 rule). In addition to providing the first quantitative test of Hamilton's rule in a system with a complex mapping between genotype and phenotype, these experiments demonstrate the wide applicability of kin selection theory.     

Genetic relatedness in groups is sex-specific and declines with age of helpers in a cooperatively breeding cichlid

Kin selection can explain the evolution of cooperative breeding and the distribution of relatives within a population may influence the benefits of cooperative behaviour. We provide genetic data on relatedness in the cooperatively breeding cichlid Neolamprologus pulcher. Helper to breeder relatedness decreased steeply with increasing helper age, particularly to the breeding males. Helper to helper relatedness was age‐assortative and also declined with age. These patterns of relatedness could be attributed to territory take‐overs by outsiders when breeders had disappeared (more in breeding males), between‐group dispersal of helpers and reproductive parasitism. In six of 31 groups females inherited the breeding position of their mother or sister. These matrilines were more likely to occur in large groups. We conclude that the relative fitness benefits of helping gained through kin selection vs. those gained through direct selection depend on helper age and sex.     

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.     

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.     

Development of microsatellite markers in the grey‐crowned babbler (Pomatostomus temporalis)

The grey‐crowned babbler (Pomatostomus temporalis) is a cooperative breeding bird species in which nonbreeding helpers of both sexes care for the young of breeding individuals. To measure the genetic relatedness between breeders and their offspring and helpers, we developed nine microsatellite markers. Most of the loci were highly polymorphic. These loci will be useful in understanding the evolution and maintenance of cooperative breeding and helping behaviour in this species.     

Nepotistic cooperation in non-human primate groups

Darwin was struck by the many similarities between humans and other primates and believed that these similarities were the product of common ancestry. He would be even more impressed by the similarities if he had known what we have learned about primates over the last 50 years. Genetic kinship has emerged as the primary organizing force in the evolution of primate social organization and the patterning of social behaviour in non-human primate groups. There are pronounced nepotistic biases across the primate order, from tiny grey mouse lemurs (Microcebus murinus) that forage alone at night but cluster with relatives to sleep during the day, to cooperatively breeding marmosets that rely on closely related helpers to rear their young, rhesus macaque (Macaca mulatta) females who acquire their mother''s rank and form strict matrilineal dominance hierarchies, male howler monkeys that help their sons maintain access to groups of females and male chimpanzees (Pan troglodytes) that form lasting relationships with their brothers. As more evidence of nepotism has accumulated, important questions about the evolutionary processes underlying these kin biases have been raised. Although kin selection predicts that altruism will be biased in favour of relatives, it is difficult to assess whether primates actually conform to predictions derived from Hamilton''s rule: br > c. In addition, other mechanisms, including contingent reciprocity and mutualism, could contribute to the nepotistic biases observed in non-human primate groups. There are good reasons to suspect that these processes may complement the effects of kin selection and amplify the extent of nepotistic biases in behaviour.     

Cooperation between non-relatives in a primitively eusocial paper wasp,Polistes dominula

In cooperatively breeding vertebrates, the existence of individuals that help to raise the offspring of non-relatives is well established, but unrelated helpers are less well known in the social insects. Eusocial insect groups overwhelmingly consist of close relatives, so populations where unrelated helpers are common are intriguing. Here, we focus on Polistes dominula—the best-studied primitively eusocial wasp, and a species in which nesting with non-relatives is not only present but frequent. We address two major questions: why individuals should choose to nest with non-relatives, and why such individuals participate in the costly rearing of unrelated offspring. Polistes dominula foundresses produce more offspring of their own as subordinates than when they nest independently, providing a potential explanation for co-founding by non-relatives. There is some evidence that unrelated subordinates tailor their behaviour towards direct fitness, while the role of recognition errors in generating unrelated co-foundresses is less clear. Remarkably, the remote but potentially highly rewarding chance of inheriting the dominant position appears to strongly influence behaviour, suggesting that primitively eusocial insects may have much more in common with their social vertebrate counterparts than has commonly been thought.     

Kinship between parents reduces offspring fitness in a natural population of Rhododendron brachycarpum

Background and Aims

A reduction in offspring fitness resulting from mating between neighbours is interpreted as biparental inbreeding depression. However, little is known about the relationship between the parents'' genetic relatedness and biparental inbreeding depression in their progeny in natural populations. This study assesses the effect of kinship between parents on the fitness of their progeny and the extent of spatial genetic structure in a natural population of Rhododendron brachycarpum.

Methods

Kinship coefficients between 11 858 pairs of plants among a natural population of 154 R. brachycarpum plants were estimated a priori using six microsatellite markers. Plants were genotyped, and pairs were selected from among 60 plants to vary the kinship from full-sib to unrelated. After a hand-pollination experiment among the 60 plants, offspring fitness was measured at the stages of seed maturation (i.e. ripening) under natural conditions, and seed germination and seedling survival under greenhouse conditions. In addition, spatial autocorrelation was used to assess the population''s genetic structure.

Key Results

Offspring fitness decreased significantly with increasing kinship between parents. However, the magnitude and timing of this effect differed among the life-cycle stages. Measures of inbreeding depression were 0·891 at seed maturation, 0·122 (but not significant) at seed germination and 0·506 at seedling survival. The local population spatial structure was significant, and the physical distance between parents mediated the level of inbreeding between them.

Conclusions

The level of inbreeding between individuals determines offspring fitness in R. brachycarpum, especially during seed maturation. Genetic relatedness between parents caused inbreeding depression in their progeny. Therefore, biparental inbreeding contributes little to reproduction and instead acts as a selection force that promotes outcrossing, as offspring of more distant (less related) parents survive better.     

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.