The definition of eusociality

We describe more precise definitions for the term "eusociality"and other social systems. Our criterion for eusociality is thepresence of castes, which are groups of individuals that becomeirreversibly behaviorally distinct at some point prior to reproductivematurity. Eusocial societies are characterized by two traits:(1) helping by individuals of the less-reproductive caste, and(2) either behavioral totipotency of only the more reproductivecaste (facultative eusociality) or totipotency of neither caste(obligate eusociality). We define "cooperative breeding" asalloparental care without castes. Cooperatively breeding societiesmay comprise two types, semisocial (distribution of lifetimereproductive success bimodal), and quasisocial (distributionof lifetime reproductive success unimodal), but this hypothesisrequires empirical analysis. Our definitions conceptually unifystudies of arthropod and vertebrate sociality.     

Kin selection versus sexual selection: why the ends do not meet

I redevelop the hypothesis that lifetime monogamy is a fundamental condition for the evolution of eusocial lineages with permanent non-reproductive castes, and that later elaborations--such as multiply-mated queens and multi-queen colonies--arose without the re-mating promiscuity that characterizes non-social and cooperative breeding. Sexually selected traits in eusocial lineages are therefore peculiar, and their evolution constrained. Indirect (inclusive) fitness benefits in cooperatively breeding vertebrates appear to be negatively correlated with promiscuity, corroborating that kin selection and sexual selection tend to generally exclude each other. The monogamy window required for transitions from solitary and cooperative breeding towards eusociality implies that the relatedness and benefit-cost variables of Hamilton's rule do not vary at random, but occur in distinct and only partly overlapping combinations in cooperative, eusocial, and derived eusocial breeding systems.     

Forum: The eusociality continuum

Eusocial societies are traditionally characterized by a reproductivedivision of labor, an overlap of generations, and cooperativecare of the breeders' young. Eusociality was once thought tooccur only in termites, ants, and some bee and wasp species,but striking evolutionary convergences have recently becomeapparent between the societies of these insects and those ofcooperatively breeding birds and mammals. These parallels haveblurred distinctions between cooperative breeding and eusociality,leading to calls for either drastically restricting or expandingusage of these terms. We favor the latter approach. Cooperativebreeding and eusociality are not discrete phenomena, but ratherform a continuum of fundamentally similar social systems whosemain differences lie in the distribution of lifetime reproductivesuccess among group members. Therefore we propose to array vertebrateand invertebrate cooperative breeders along a common axis, representinga standardized measure of reproductive variance, and to dropsuch (loaded) terms as "primitive" and "advanced" eusociality.The terminology we propose unites all occurrences of alloparentalhelping of kin under a single theoretical umbrella (e.g., Hamilton'srule). Thus, cooperatively breeding vertebrates can be regardedas eusocial, just as eusocial invertebrates are cooperativebreeders. We believe this integrated approach will foster potentiallyrevealing cross-taxon comparisons, which are essential to understandingsocial evolution in birds, mammals, and insects.     

Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus)

The evolutionary maintenance of cooperative breeding systems is thought to be a function of relative costs and benefits to breeders, helpers and juveniles. Beneficial effects of helpers on early-life survivorship and performance have been established in several species, but lifetime fitness benefits and/or costs of being helped remain unclear, particularly for long-lived species. We tested for effects of helpers on early- and late-life traits in a population of reintroduced red wolves (Canis rufus), while controlling for ecological variables such as home-range size and population density. We found that the presence of helpers in family groups was positively correlated with pup mass and survival at low population density, but negatively correlated with mass/size at high density, with no relation to survival. Interestingly, mass/size differences persisted into adulthood for both sexes. While the presence of helpers did not advance age at first reproduction for pups of either sex, females appeared to garner long-term fitness benefits from helpers through later age at last reproduction, longer reproductive lifespan and a greater number of lifetime reproductive events, which translated to higher lifetime reproductive success. In contrast, males with helpers exhibited diminished lifetime reproductive performance. Our findings suggest that while helper presence may have beneficial short-term effects in some ecological contexts, it may also incur long-term sex-dependent costs with critical ramifications for lifetime fitness.     

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.     

Female mating decisions: maximizing fitness?

Sexual selection theory assumes that maximizing fitness is the ultimate goal in every mating decision. Fitness can be maximized directly by increasing the number of offspring (direct benefits) or indirectly by maximizing offspring's lifetime reproductive success (indirect benefits). Whereas there is considerable evidence in the literature for the influence of mating decisions on direct benefits, indirect benefits have been more elusive. Here, we review the variables that influence mating decisions made by females of freshwater fish and how these affect their fitness directly, as well as indirectly. Females enhance their fitness by matching their mating decisions to current environmental conditions, using a wide range of pre- and post-copulation mechanisms that enable them to maximize benefits from mating. Male sexual traits and courtship displays are signals used by females as a way of assessing male quality in terms of both direct and indirect benefits. Polyandry is very common among freshwater fish species, and indirect benefits have been hypothesized as drivers of its predominance. Despite intensive theoretical work, and multiple suggestions of the effects of indirect benefits, to date no study has been able to demonstrate experimentally the existence of indirect benefits in freshwater fish species. Additionally, most studies of direct benefits measure short-term benefits of mating decisions. In both cases, lifetime reproductive success is not assessed. Therefore, we are led to conclude that evidence as to whether female mating decisions result in direct and/or indirect benefits in freshwater fish species is still lacking. These results should be considered in light of the ongoing debate about the significance of indirect benefits in female mating decisions.     

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.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Attractive males do not sire superior daughters

Much of the recent work on the evolution of female choice has focused on the relative influence of direct and indirect benefits, and particularly whether direct costs can be offset by indirect benefits. Studies investigating whether attractive males benefit females by increasing the viability of their offspring often report mating advantages to sons consistent with the Fisher process, while detecting no or weak viability benefits. One potential reason for this is that sons may trade-off viability benefits with investment in costly traits that enhance mating success, leading to the suggestion that viability benefits may be better detected by examining daughters’ fitness. Here we investigate the relationship between male attractiveness and daughters’ fitness in Drosophila simulans. We measured daughter (and dam) lifetime reproductive success and longevity. We found no evidence that attractive males sire high fitness daughters. Additionally, neither daughters nor dams gained direct benefits from mating with attractive males. However, aspects of daughters’ fitness were related to dam characters.     

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.     

Male‐induced costs of mating for females compensated by offspring viability benefits in an insect

Sexual conflict facilitates the evolution of traits that increase the reproductive success of males at the expense of components of female fitness. Theory suggests that indirect benefits are unlikely to offset the direct costs to females from antagonistic male adaptations, but empirical studies examining the net fitness pay‐offs of the interaction between the sexes are scarce. Here, we investigate whether matings with males that invest intrinsically more into accessory gland tissue undermine female lifetime reproductive success (LRS) in the cricket Teleogryllus oceanicus. We found that females incur a longevity cost of mating that is proportional to the partner’s absolute investment into the production of accessory gland products. However, male accessory gland weight positively influences embryo survival, and harmful ejaculate‐induced effects are cancelled out when these are put in the context of female LRS. The direct costs of mating with males that sire offspring with higher viability are thus compensated by direct and possibly indirect genetic benefits in this species.     

Policing and punishment across the domains of social evolution

Several decades of research in humans, other vertebrates, and social insects have offered fascinating insights into the dynamics of punishment (and its subset, policing), but authors have only rarely addressed whether there are fundamental joint principles underlying the maintenance of these behaviors. Here we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punishing roles in animal societies. We apply our scheme to societies of eusocial Hymenoptera and nonhuman vertebrate social breeders, and we outline potential extensions for understanding conflict regulation among cells in metazoan bodies and unrelated individuals in human societies. We highlight that: 1) no social unit is expected to express punishment behavior unless it collects positive inclusive fitness benefits that surpass alternative benefits of bystanding; 2) punishment with public good benefits can be maintained through either direct fitness benefits (coercion) or indirect fitness benefits (correction) or both; 3) differences across social systems in the distributions of power, relatedness, and reproductive options drive variation in the extent to which individuals actively punish; and 4) inclusive fitness logic captures many punishment‐relevant evolutionary and ecological variables in a single framework that appears to apply across very different types of social arrangements. Synthesis Researchers have long observed that individuals in animal societies punish (and by extension, police) each other, but they have rarely investigated whether general principles underlie this behavior across social arrangements. In this paper, we present a punisher/bystander approach rooted in inclusive fitness logic to predict which individuals should take on punisher roles in animal societies. We apply the approach to eusocial insects and cooperatively breeding vertebrates and outline extensions towards the control of cancer cell lineages and punishment in human groups. We highlight how variation in specific social variables may drive differences in punishing/policing across the social domains.     

Costs and benefits of reproduction in predaceous ladybird: Effect of multiple matings on reproduction and offspring development

A few matings are sufficient for females to maximize their reproductive success, while male fitness usually increases with an increase in the number of matings. However, females of a majority of insects mate multiple times. This presents an evolutionary puzzle and brings an understanding that some benefits are associated with it. Therefore, to understand the costs and benefits of multiple matings, we performed an experimental study in a ladybird beetle, Anegleis cardoni and observed reproductive performance and longevity of adults as direct benefits and offspring development and survival as indirect benefits. This is the first time that the effect of multiple matings is being evaluated on offspring development and survival in a ladybird beetle. Results clearly reveal that females directly benefit from multiple matings in terms of increased lifetime fecundity and egg viability, but their longevity decreases with increased number of matings. Best-fit curves on lifetime fecundity and percent egg viability revealed that maximum fecundity and egg viability were both attained after 17 matings. Developmental duration of offspring decreased and their survival increased with an increase in number of matings. Developmental duration was shortest after 20 matings and longest after a single mating.     

Sex differences in relationships between habitat use and reproductive performance in Soay sheep (Ovis aries)

The role of habitat use in generating individual variation in fitness has rarely been examined empirically in natural populations of long‐lived mammals, particularly for both sexes simultaneously. This is the case despite the increase in studies attempting to understand evolutionary change in such populations. Using data from the St. Kilda Soay sheep population, we quantified the association between lifetime reproductive performance (lifetime breeding and reproductive success) and the proportion of the home range covered by a key grass species, H. lanatus, for 490 females and 304 males. Increased H. lanatus cover was associated only with increased female lifetime reproductive success, but increased lifetime breeding success for both sexes, arising through increased male longevity and increased female fecundity. This work suggests that improved understanding of the causes and consequences of fitness differences will likely require us to better account for habitat‐derived individual variation, and to do so for the sexes appropriately.     

Subordinate superb fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males

Explanations of cooperative breeding have largely focused on the indirect benefits philopatric offspring gain from investing in kin. However, recent molecular studies have revealed that in many species subordinates provision unrelated offspring. This has led to the re-evaluation of the direct and indirect benefits of helping behaviour. In this study, we used microsatellite genotyping to assess the extra-group reproductive success of subordinate superb fairy-wrens (Malurus cyaneus), a species with extremely high rates of extra-group paternity. Extra-group subordinate males sired 10.2% (193 out of 1895) of all offspring sampled between 1993 and 2000 and 21.4% (193 out of 901) of all illegitimate offspring sired by known males. The extra-group success of subordinates was greatly influenced by the attractiveness of their dominant male. Subordinates of attractive dominants sired more extra-group young than did average dominants. Evidence suggests that mate choice in superb fairy-wrens is error-prone and subordinates can gain direct reproductive benefits through parasitizing the reproductive success of attractive dominants.     

Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers

Abstract.— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis . A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.     

Living with strangers: direct benefits favour non-kin cooperation in a communally nesting bird

The greater ani (Crotophaga major), a Neotropical cuckoo, exhibits an unusual breeding system in which several socially monogamous pairs lay eggs in a single nest and contribute care to the communal clutch. Cooperative nesting is costly-females compete for reproduction by ejecting each other's eggs-but the potential direct or indirect fitness benefits that might accrue to group members have not been identified. In this study, I used molecular genotyping to quantify patterns of genetic relatedness and individual reproductive success within social groups in a single colour-banded population. Microsatellite analysis of 122 individuals in 49 groups revealed that group members are not genetic relatives. Group size was strongly correlated with individual reproductive success: solitary pairs were extremely rare and never successful, and nests attended by two pairs were significantly more likely to be depredated than were nests attended by three pairs. Egg loss, a consequence of reproductive competition, was greater in large groups and disproportionately affected females that initiated laying. However, early-laying females compensated for egg losses by laying larger clutches, and female group members switched positions in the laying order across nesting attempts. The greater ani, therefore, appears to be one of the few species in which cooperative breeding among unrelated individuals is favoured by direct, shared benefits that outweigh the substantial costs of reproductive competition.     

Bateman's Principle in Cooperatively Breeding Vertebrates: The Effects of Non-breeding Alloparents on Variability in Female and Male Reproductive Success

The sex-specific slopes of Bateman's gradients have importantimplications for understanding animal mating systems, includingpatterns of sexual selection and reproductive competition. Intersexualdifferences in the fitness benefits derived from mating withmultiple partners are expected to yield distinct patterns ofreproductive success for males and females, with variance indirect fitness predicted to be greater among males. These analysesassume that typically all adults are reproductive and that failureto produce offspring is non-adaptive. Among some species ofcooperatively breeding birds and mammals, however, non-breedingadult alloparents are common and may comprise the majority ofindividuals in social groups. The presence of a large numberof non-breeding adults, particularly when coupled with greatersocial suppression of reproduction among females, may alterthe relative variance in direct fitness between the sexes, therebygenerating an apparent contradiction to Bateman's Paradigm.To explore quantitatively the effects of non-breeding alloparentson variance in reproductive success, we used genetic estimatesof parentage and reproductive success drawn from the literatureto calculate the relative variability in direct fitness forfemales and males in alloparental and "other" societies of birdsand mammals. Our analyses indicate that in mammals and, to alesser extent, in birds, variability in direct fitness is greateramong females in species characterized by the presence of non-breedingalloparents. These data suggest that social interactions, includingsocial suppression of reproduction, are powerful determinantsof individual direct fitness that may modify sex-specific patternsof reproductive variance from those described by Bateman.     

Male Seychelles warblers use territory budding to maximize lifetime fitness in a saturated environment

In cooperatively breeding species, helping at the nest and buddingoff part of the natal territory have been advanced as strategiesto increase fitness in an environment that is saturated withterritories. The importance of helping or territory buddingas a determinant of lifetime reproductive success (LRS) hasbeen debated because the potential benefits of both strategiescould not be separated. Here we test the causes and the immediateand future fitness consequences of single dispersal decisionstaken by male Seychelles warblers (Acrocephalus sechellensis).Males breeding in high-quality territories (high food abundance)have significantly higher LRS than similar-aged males buddingoff part of the parental territory. Initially, budders havea low reproductive success (because of limited food resourcesor absence of a breeding partner). However, they have a longlife span and inherit high-quality territories through sitedominance, by which they gain higher LRS than breeders on low-qualityterritories, helpers, or floaters. Experimental creation ofmale breeding territory vacancies showed that most young malesbecame budders because of intense competition for high-quality territories. The translocation of warblers to the previouslyunoccupied Aride Island shows that males behave according tothe expected fitness benefits of each dispersal strategy. Inthe absence of competition for territories on Aride, all youngmales bred in high-quality territories. However, after saturationof high-quality habitat with territories, most males becamebudders rather than breeders on low-quality habitat, helpers,or floaters.     

Invasion fitness,inclusive fitness,and reproductive numbers in heterogeneous populations

How should fitness be measured to determine which phenotype or “strategy” is uninvadable when evolution occurs in a group‐structured population subject to local demographic and environmental heterogeneity? Several fitness measures, such as basic reproductive number, lifetime dispersal success of a local lineage, or inclusive fitness have been proposed to address this question, but the relationships between them and their generality remains unclear. Here, we ascertain uninvadability (all mutant strategies always go extinct) in terms of the asymptotic per capita number of mutant copies produced by a mutant lineage arising as a single copy in a resident population (“invasion fitness”). We show that from invasion fitness uninvadability is equivalently characterized by at least three conceptually distinct fitness measures: (i) lineage fitness, giving the average individual fitness of a randomly sampled mutant lineage member; (ii) inclusive fitness, giving a reproductive value weighted average of the direct fitness costs and relatedness weighted indirect fitness benefits accruing to a randomly sampled mutant lineage member; and (iii) basic reproductive number (and variations thereof) giving lifetime success of a lineage in a single group, and which is an invasion fitness proxy. Our analysis connects approaches that have been deemed different, generalizes the exact version of inclusive fitness to class‐structured populations, and provides a biological interpretation of natural selection on a mutant allele under arbitrary strength of selection.