Helping in cooperatively breeding long-tailed tits: a test of Hamilton's rule

Inclusive fitness theory provides the conceptual framework for our current understanding of social evolution, and empirical studies suggest that kin selection is a critical process in the evolution of animal sociality. A key prediction of inclusive fitness theory is that altruistic behaviour evolves when the costs incurred by an altruist (c) are outweighed by the benefit to the recipient (b), weighted by the relatedness of altruist to recipient (r), i.e. Hamilton''s rule rb > c. Despite its central importance in social evolution theory, there have been relatively few empirical tests of Hamilton''s rule, and hardly any among cooperatively breeding vertebrates, leading some authors to question its utility. Here, we use data from a long-term study of cooperatively breeding long-tailed tits Aegithalos caudatus to examine whether helping behaviour satisfies Hamilton''s condition for the evolution of altruism. We show that helpers are altruistic because they incur survival costs through the provision of alloparental care for offspring. However, they also accrue substantial benefits through increased survival of related breeders and offspring, and despite the low average relatedness of helpers to recipients, these benefits of helping outweigh the costs incurred. We conclude that Hamilton''s rule for the evolution of altruistic helping behaviour is satisfied in this species.     

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.     

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.     

Resolving the evolution of sterile worker castes: a window on the advantages and disadvantages of monogamy

Many social Hymenoptera species have morphologically sterile worker castes. It is proposed that the evolutionary routes to this obligate sterility must pass through a ‘monogamy window’, because inclusive fitness favours individuals retaining their reproductive totipotency unless they can rear full siblings. Simulated evolution of sterility, however, finds that ‘point of view’ is critically important. Monogamy is facilitating if sterility is expressed altruistically (i.e. workers defer reproduction to queens), but if sterility results from manipulation by mothers or siblings, monogamy may have no effect or lessen the likelihood of sterility. Overall, the model and data from facultatively eusocial bees suggest that eusociality and sterility are more likely to originate through manipulation than by altruism, casting doubt on a mandatory role for monogamy. Simple kin selection paradigms, such as Hamilton''s rule, can also fail to account for significant evolutionary dynamics created by factors, such as population structure, group-level effects or non-random mating patterns. The easy remedy is to always validate apparently insightful predictions from Hamiltonian equations with life-history appropriate genetic models.     

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.     

Darwin's ‘one special difficulty’: celebrating Darwin 200

Darwin identified eusocial evolution, especially of complex insect societies, as a particular challenge to his theory of natural selection. A century later, Hamilton provided a framework for selection on inclusive fitness. Hamilton''s rule is robust and fertile, having generated multiple subdisciplines over the past 45 years. His suggestion that eusociality can be explained via kin selection, however, remains contentious. I review the continuing debate on the role of kin selection in eusocial evolution and suggest some lines of research that should resolve that debate.     

Beyond promiscuity: mate-choice commitments in social breeding

Obligate eusociality with distinct caste phenotypes has evolved from strictly monogamous sub-social ancestors in ants, some bees, some wasps and some termites. This implies that no lineage reached the most advanced form of social breeding, unless helpers at the nest gained indirect fitness values via siblings that were identical to direct fitness via offspring. The complete lack of re-mating promiscuity equalizes sex-specific variances in reproductive success. Later, evolutionary developments towards multiple queen-mating retained lifetime commitment between sexual partners, but reduced male variance in reproductive success relative to female''s, similar to the most advanced vertebrate cooperative breeders. Here, I (i) discuss some of the unique and highly peculiar mating system adaptations of eusocial insects; (ii) address ambiguities that remained after earlier reviews and extend the monogamy logic to the evolution of soldier castes; (iii) evaluate the evidence for indirect fitness benefits driving the dynamics of (in)vertebrate cooperative breeding, while emphasizing the fundamental differences between obligate eusociality and cooperative breeding; (iv) infer that lifetime commitment is a major driver towards higher levels of organization in bodies, colonies and mutualisms. I argue that evolutionary informative definitions of social systems that separate direct and indirect fitness benefits facilitate transparency when testing inclusive fitness theory.     

Ploidy of the eusocial beetle Austroplatypus incompertus (Schedl) (Coleoptera, Curculionidae) and implications for the evolution of eusociality

In the hymenopterans, haplodiploidy, leading to high-genetic relatedness amongst full sisters has been regarded as critical to kin selection and inclusive fitness hypotheses that explain the evolution of eusociality and altruistic behaviours. Recent evidence for independent origins of eusociality in phylogenetically diverse taxa has led to the controversy regarding the general importance of relatedness to eusociality and its evolution. Here, we developed a highly polymorphic microsatellite marker to test whether the eusocial ambrosia beetle Austroplatypus incompertus (Schedl) is haplodiploid or diplodiploid. We found that both males and females of A. incompertus are diploid, signifying that altruistic behaviour resulting from relatedness asymmetries did not play a role in the evolution of eusocialty in this species. This provides additional evidence against the haplodiploidy hypothesis and implicates alternative hypotheses for the evolution of eusociality.     

A GENERAL MODEL FOR KIN SELECTION

Inclusive fitness theory is central to our understanding of the evolution of social behavior. By showing the importance of genetic transmission through nondescendent relatives, it helps to explain the evolution of reproductively altruistic behaviors, such as those observed in the social insects. Inclusive fitness thinking is quantified by Hamilton's rule, but Hamilton's rule has often been criticized for being inexact or insufficiently general. Here I show how adopting a genic perspective yields a very general version that remains pleasingly simple and transparent.     

Deleterious mutation and the evolution of eusociality

Abstract.— Certain arguments concerning the evolution of eusociality form a classic example of the application of the principles of kin selection. These arguments center on the different degrees of relatedness of potential beneficiaries of an individual's efforts, for example a female's higher relatedness to her sisters than to her daughters in a haplodiploid system. This type of reasoning is insufficient to account for the evolution and maintainence of sexual reproduction, because parthenogenic females produce offspring that are more closely related to them than are offspring produced sexually. Among the forces invoked to explain sexual reproduction is deleterious mutation. This factor can be shown to favor eusociality as well, because siblings produced by helping carry fewer deleterious alleles on average than would offspring. The strength of this effect depends on the genomewide deleterious mutation rate, U, and on the selection coefficient, s, associated with deleterious alleles. For small s, the effect depends approximately on the product Us. This phenomenon illustrates that an assumption implicit in some analyses–that the relatedness of an individual to an actor is all that matters to its value to that actor–can fail for the evolution of eusociality as it does for the evolution of sex.     

How multiple mating by females affects sexual selection

Multiple mating by females is widely thought to encourage post-mating sexual selection and enhance female fitness. We show that whether polyandrous mating has these effects depends on two conditions. Condition 1 is the pattern of sperm utilization by females; specifically, whether, among females, male mating number, m (i.e. the number of times a male mates with one or more females) covaries with male offspring number, o. Polyandrous mating enhances sexual selection only when males who are successful at multiple mating also sire most or all of each of their mates'' offspring, i.e. only when Cov_♂(m,o), is positive. Condition 2 is the pattern of female reproductive life-history; specifically, whether female mating number, m, covaries with female offspring number, o. Only semelparity does not erode sexual selection, whereas iteroparity (i.e. when Cov_♀(m,o), is positive) always increases the variance in offspring numbers among females, which always decreases the intensity of sexual selection on males. To document the covariance between mating number and offspring number for each sex, it is necessary to assign progeny to all parents, as well as identify mating and non-mating individuals. To document significant fitness gains by females through iteroparity, it is necessary to determine the relative magnitudes of male as well as female contributions to the total variance in relative fitness. We show how such data can be collected, how often they are collected, and we explain the circumstances in which selection favouring multiple mating by females can be strong or weak.     

Hamilton's rule,inclusive fitness maximization,and the goal of individual behaviour in symmetric two‐player games

Hamilton's original work on inclusive fitness theory assumed additivity of costs and benefits. Recently, it has been argued that an exact version of Hamilton's rule for the spread of a pro‐social allele (rb > c) holds under nonadditive pay‐offs, so long as the cost and benefit terms are defined as partial regression coefficients rather than pay‐off parameters. This article examines whether one of the key components of Hamilton's original theory can be preserved when the rule is generalized to the nonadditive case in this way, namely that evolved organisms will behave as if trying to maximize their inclusive fitness in social encounters.     

Hamilton's rule meets the Hamiltonian: kin selection on dynamic characters

Many biological characters of interest are temporal sequences of decisions. The evolution of such characters is often modelled using dynamic optimization methods such as the maximum principle. A quantity central to these analyses is the ''Hamiltonian'' function, named after the mathematician William R. Hamilton. On the other hand, evolutionary models in which individuals interact with relatives are usually based on Hamilton''s rule, named after the evolutionary biologist William D. Hamilton. In this article we present a generalized maximum principle that includes the effects of interactions among relatives and we show that a time-dependent (dynamic) version of Hamilton''s rule holds involving the Hamiltonian. This result brings together the power and generality of both the maximum principle and Hamilton''s rule thereby providing a natural framework for understanding the evolution of ''dynamic'' characters under kin selection.     

Characterisation of ionisations that influence the redox potential of mitochondrial cytochrome c and photosynthetic bacterial cytochromes c2

Several cytochromes c₂ from the Rhodospirillaceae show a pH dependence of redox potential in the physiological pH range which can be described by equations involving an ionisation in the oxidised form (pK_o) and one in the reduced form (pK_r). These cytochromes fall into one of two groups according to the degree of separation of pK_o and pK_r. In group A, represented here by the Rhodomicrobium vannielii cytochrome c₂, the separation is approx. one pH unit and the ionisation is that of a haem propionic acid. Members of this group are unique among both cytochromes c₂ and mitochondrial cytochromes c in lacking the conserved residue Arg-38. We propose that the role of Arg-38 is to lower the pK of the nearby propionic acid, so that it lies out of the physiological pH range. Substitution of this residue by an uncharged amino acid leads to a raised pK for the propionic acid. In group B, represented here by Rhodopseudomonas viridis cytochrome c₂, the separation between pK_o and pK_r is approx. 0.4 pH unit and the ionisable group is a histidine at position 39. This was established by NMR spectroscopy and confirmed by chemical modification. Only a few other members of the cytochrome c₂/mitochondrial cytochrome c family have a histidine at this position and of these, both Crithidia cytochrome c-557 and yeast cytochrome c were found to have a pH-dependent redox potential similar to that of Rps. viridis cytochrome c₂. Using Coulomb's law, it was found that the energy required to separate pK_o and pK_r could be accounted for by simple electrostatic interactions between the haem iron and the ionisable group.     

Estimation of effective population size in continuously distributed populations: there goes the neighborhood

Use of genetic methods to estimate effective population size (N_e) is rapidly increasing, but all approaches make simplifying assumptions unlikely to be met in real populations. In particular, all assume a single, unstructured population, and none has been evaluated for use with continuously distributed species. We simulated continuous populations with local mating structure, as envisioned by Wright''s concept of neighborhood size (NS), and evaluated performance of a single-sample estimator based on linkage disequilibrium (LD), which provides an estimate of the effective number of parents that produced the sample (N_b). Results illustrate the interacting effects of two phenomena, drift and mixture, that contribute to LD. Samples from areas equal to or smaller than a breeding window produced estimates close to the NS. As the sampling window increased in size to encompass multiple genetic neighborhoods, mixture LD from a two-locus Wahlund effect overwhelmed the reduction in drift LD from incorporating offspring from more parents. As a consequence, never approached the global N_e, even when the geographic scale of sampling was large. Results indicate that caution is needed in applying standard methods for estimating effective size to continuously distributed populations.     

TRAIT MAPPING AND SALIENCE IN THE EVOLUTION OF EUSOCIAL VESPID WASPS

The multiple independent origins of eusociality in the insect order Hymenoptera are clustered in only four of more than 80 families, and those four families are two pairs of closely related taxa in a single part of the order. Therefore, although ordinal-level characteristics can contribute to hymenopteran eusocial evolution, more important roles have been played by traits of infraordinal taxa that contain the eusocial forms. Many factors have been proposed and discussed, but assessments of traits' salience to eusocial evolution have heretofore not been joined to phylogenetics. In the present analysis, cladograms of superfamilies and families of Hymenoptera and of the family Vespidae are used to ordinate the appearance of traits that play roles in vespid eusociality. Proximity of traits' first appearance to the origin of eusocial Vespidae is taken as one measure of traits' salience to vespid eusocial evolution. Traits that subtend only eusocial taxa and that are uniquely associated with eusociality have foundations in more general traits that subtend more inclusive taxa. No single trait is uniquely causative of vespid eusocial evolution. High-salience traits that closely subtend vespid eusociality include nesting, oviposition into an empty nest cell, progressive provisioning of larvae, adult nourishment during larval provision malaxation, and inequitable food distribution among nestmates. The threshold characteristic of Polistes-grade eusociality is life-long alloparental brood care by first female offspring who remain, uninseminated, at their natal nest. Traits directly associated with occurrence of such workers are larva-adult trophallaxis, which can foster relatively low larval nourishment early in a colony cycle, and protogyny and direct larval development, which combine to yield restricted mating opportunities for female offspring that are the first to emerge in the colony cycle. Trait mapping suggests no role for asymmetry of relatedness due to haplodiploidy, but it suggests high salience for haplodiploidy as a mechanism enabling the production of all-female clutches of first offspring.     

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.     

Neutron scattering studies of subcomponent C1q of first component C1 of human complement and its association with subunit C1r2C1s2 within C1

Neutron scattering studies are reported on subcomponent C1q of component C1 of human complement, and on C1, the complex of C1q with subunit C1r₂C1s₂. For C1q, the molecular weight was determined as 460,000. The radius of gyration at infinite contrast R_c is 12.8 nm. The R_c values for the proteolytically cleaved forms of C1q, namely the heads and the stalks, are 1.5 to 2 nm and 11 nm, respectively, and thus the axis-to-arm angle of C1q is estimated at 45 °. Neutron data for subunit C1r₂C1s₂ are published elsewhere. The neutron data on C1 lead to an R_c value of 12.6 nm for proenzymic C1 and a molecular weight of 820,000. The wideangle scattering curve of C1q exhibits a minimum at Q = 0.28 nm^?1 and a maximum at 0.39 nm^?1; on the addition of C1r₂C1s₂, this minimum disappears. The neutron data on C1 indicate that C1q and C1r₂C1s₂ have complexed with a large conformational change in one or both parts. No conformational changes can be detected on the activation of C1 by this method.     

Kinship,parental manipulation and evolutionary origins of eusociality

One of the hallmarks of eusociality is that workers forego their own reproduction to assist their mother in raising siblings. This seemingly altruistic behaviour may benefit workers if gains in indirect fitness from rearing siblings outweigh the loss of direct fitness. If worker presence is advantageous to mothers, however, eusociality may evolve without net benefits to workers. Indirect fitness benefits are often cited as evidence for the importance of inclusive fitness in eusociality, but have rarely been measured in natural populations. We compared inclusive fitness of alternative social strategies in the tropical sweat bee, Megalopta genalis, for which eusociality is optional. Our results show that workers have significantly lower inclusive fitness than females that found their own nests. In mathematical simulations based on M. genalis field data, eusociality cannot evolve with reduced intra-nest relatedness. The simulated distribution of alternative social strategies matched observed distributions of M. genalis social strategies when helping behaviour was simulated as the result of maternal manipulation, but not as worker altruism. Thus, eusociality in M. genalis is best explained through kin selection, but the underlying mechanism is likely maternal manipulation.     

Identification of o-phenylenediamine polymerization product catalyzed by cytochrome c

The hydrogen peroxide (H₂O₂) and cytochrome c-dependent oxidation of o-phenylenediamine (o-PD) was investigated by spectrophotometry and electrochemistry. The results indicated that o-PD underwent facile catalytic oxidation in the presence of cytochrome c, and that the degradation of cytochrome c by hydrogen peroxide can also be partly prevented in the presence of o-PD. The hydroxyl radical scavengers (mannitol and sodium benzoate) and oxo-heme species scavenger (uric acid) do not inhibit the oxidation, which implies that the hydroxylation of o-PD may not be involved in its oxidation. Combining with the results of the mass spectrum, elemental analysis, nuclear magnetic resonance and Fourier transform infrared spectrum of the isolated product, a conceivable structure of the product was suggested.