Relatedness,Conflict, and the Evolution of Eusociality

The evolution of sterile worker castes in eusocial insects was a major problem in evolutionary theory until Hamilton developed a method called inclusive fitness. He used it to show that sterile castes could evolve via kin selection, in which a gene for altruistic sterility is favored when the altruism sufficiently benefits relatives carrying the gene. Inclusive fitness theory is well supported empirically and has been applied to many other areas, but a recent paper argued that the general method of inclusive fitness was wrong and advocated an alternative population genetic method. The claim of these authors was bolstered by a new model of the evolution of eusociality with novel conclusions that appeared to overturn some major results from inclusive fitness. Here we report an expanded examination of this kind of model for the evolution of eusociality and show that all three of its apparently novel conclusions are essentially false. Contrary to their claims, genetic relatedness is important and causal, workers are agents that can evolve to be in conflict with the queen, and eusociality is not so difficult to evolve. The misleading conclusions all resulted not from incorrect math but from overgeneralizing from narrow assumptions or parameter values. For example, all of their models implicitly assumed high relatedness, but modifying the model to allow lower relatedness shows that relatedness is essential and causal in the evolution of eusociality. Their modeling strategy, properly applied, actually confirms major insights of inclusive fitness studies of kin selection. This broad agreement of different models shows that social evolution theory, rather than being in turmoil, is supported by multiple theoretical approaches. It also suggests that extensive prior work using inclusive fitness, from microbial interactions to human evolution, should be considered robust unless shown otherwise.     

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.     

A conceptual model for the origin of worker behaviour and adaptation of eusociality

In a model based on the wasp family Vespidae, the origin of worker behaviour, which constitutes the eusociality threshold, is not based on relatedness, therefore the origin of eusociality does not depend on inclusive fitness, and workers at the eusociality threshold are not altruistic. Instead, incipient workers and queens behave selfishly and are subject to direct natural selection. Beyond the eusociality threshold, relatedness enables 'soft inheritance' as the framework for initial adaptations of eusociality. At the threshold of irreversibility, queen and worker castes become fixed in advanced eusociality. Transitions from solitary to facultative, facultative to primitive, and primitive to advanced eusociality occur via exaptation, phenotypic accommodation and genetic assimilation. Multilevel selection characterizes the solitary to highly eusocial transition, but components of multilevel selection vary across levels of eusociality. Roles of behavioural flexibility and developmental plasticity in the evolutionary process equal or exceed those of genotype.     

Sex ratios and the evolution of eusociality in the hymenoptera

The potential role of sex ratio biassing in the evolution of worker behaviour in male-haploid hymenopteran insects is examined using a deterministic genetic model. The model is based on a bivoltine life cycle with annual colonies and it assumes five gene loci, each of them controlling a specific feature of the life cycle (particularly brood sex ratios). The hypothetical gene controlling worker behaviour is assumed to be expressed either in the mothers (parental manipulation models) or in the female offspring (offspring altruism models). The threshold of the worker efficiency required for the worker behaviour to evolve is 0.5 under parental manipulation and 1.0 under offspring altruism when the sex ratios are not skewed. Worker evolution by offspring altruism can evolve more easily if the first workers initially raise mainly female brood. With such a sex ratio bias, the threshold of worker efficiency allowing eusociality to evolve drops below 1.0, even close to 0.8. Worker evolution is also favoured by the elimination of males from the first of the two annually occurring offspring generations. It is concluded that the male-haploid sex determination can, through the control of sex ratios, play a significant role in the evolution of eusociality in hymenopteran insects.     

Dufour’s gland secretion,sterility and foraging behavior: Correlated behavior traits in bumblebee workers

Bombus terrestris colonies go through two major phases: the “pre-competition phase” in which the queen is the sole reproducer and aggression is rare, and the “competition phase” in which workers aggressively compete over reproduction. Conflicts over reproduction are partially regulated by a group of octyl esters that are produced in Dufour’s gland of reproductively subordinate workers and protect them from being aggressed. However, workers possess octyl esters even before overt aggression occurs, raising the question of why produce the ester-signal before it is functionally necessary?In most insect societies, foragers show reduced aggression and low dominance rank. We hypothesize that ester production in B. terrestris is not only correlated with sterility but also with foraging, signaling cooperative behavior by subordinate workers. Such a signal helps to maintain social organization, reduce the cost of fights between reproductives and helpers, and increase colony productivity, enabling subordinates to gain greater inclusive fitness. We demonstrate that foragers produce larger amounts of esters compared to non-foragers, and that their amounts positively correlate with foraging efforts. We further suggest that task performance, potential fecundity, and aggression are interlinked, and that worker–worker interactions are involved in regulating foraging behavior.B. terrestris, being an intermediate phase between primitive and derived eusocial insects, provides an excellent model for understanding the evolution of early phases of eusociality. Our results, combined with those in primitively eusocial wasps, suggest that at early stages of social evolution, reproduction was regulated by a “primordial division of labor”, that comprised foragers and reproducers, which further evolved to a more complex division of labor, a hallmark of eusociality.     

Mechanisms of social regulation change across colony development in an ant

Background  

Mutual policing is an important mechanism for reducing conflict in cooperative groups. In societies of ants, bees, and wasps, mutual policing of worker reproduction can evolve when workers are more closely related to the queen's sons than to the sons of workers or when the costs of worker reproduction lower the inclusive fitness of workers. During colony growth, relatedness within the colony remains the same, but the costs of worker reproduction may change. The costs of worker reproduction are predicted to be greatest in incipient colonies. If the costs associated with worker reproduction outweigh the individual direct benefits to workers, policing mechanisms as found in larger colonies may be absent in incipient colonies.     

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.     

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.     

The evolution of extreme altruism and inequality in insect societies

In eusocial organisms, some individuals specialize in reproduction and others in altruistic helping. The evolution of eusociality is, therefore, also the evolution of remarkable inequality. For example, a colony of honeybees (Apis mellifera) may contain 50 000 females all of whom can lay eggs. But 100 per cent of the females and 99.9 per cent of the males are offspring of the queen. How did such extremes evolve? Phylogenetic analyses show that high relatedness was almost certainly necessary for the origin of eusociality. However, even the highest family levels of kinship are insufficient to cause the extreme inequality seen in e.g. honeybees via ‘voluntary altruism’. ‘Enforced altruism’ is needed, i.e. social pressures that deter individuals from attempting to reproduce. Coercion acts at two stages in an individual''s life cycle. Queens are typically larger so larvae can be coerced into developing into workers by being given less food. Workers are coerced into working by ‘policing’, in which workers or the queen eat worker-laid eggs or aggress fertile workers. In some cases, individuals rebel, such as when stingless bee larvae develop into dwarf queens. The incentive to rebel is strong as an individual is the most closely related to its own offspring. However, because individuals gain inclusive fitness by rearing relatives, there is also a strong incentive to ‘acquiesce’ to social coercion. In a queenright honeybee colony, the policing of worker-laid eggs is very effective, which results in most workers working instead of attempting to reproduce. Thus, extreme altruism is due to both kinship and coercion. Altruism is frequently seen as a Darwinian puzzle but was not a puzzle that troubled Darwin. Darwin saw his difficulty in explaining how individuals that did not reproduce could evolve, given that natural selection was based on the accumulation of small heritable changes. The recognition that altruism is an evolutionary puzzle, and the solution was to wait another 100 years for William Hamilton.     

The evolutionary origin and elaboration of sociality in the aculeate Hymenoptera: maternal effects, sib-social effects, and heterochrony

We discuss the evolutionary origin and elaboration of sociality using an indirect genetic effects perspective. Indirect genetic effects models simultaneously consider zygotic genes, genes expressed in social partners (especially mothers and siblings), and the interactions between them. Incorporation of these diverse genetic effects should lead to more realistic models of social evolution. We first review haplodiploidy as a factor that promotes the evolution of eusociality. Social insect biologists have doubted the importance of relatedness asymmetry caused by haplodiploidy and focused on other predisposing factors such as maternal care. However; indirect effects theory shows that maternal care evolves more readily in haplodiploids, especially with inbreeding and despite multiple mating. Because extended maternal care is believed to be a precondition for the evolution of eusociality, the evolutionary bias towards maternal care in haplodiploids may result in a further bias towards eusociality in these groups. Next, we compare kin selection and parental manipulation and then briefly review additional hypotheses for the evolutionary origin of eusociality. We present a verbal model for the evolutionary origin and elaboration of sib-social care from maternal care based on the modification of the timing of expression of maternal care behaviors. Specifically, heterochrony genes cause maternal care behaviors to be expressed prereproductively towards siblings instead of postreproductively towards offspring. Our review demonstrates that both maternal effect genes (expressed in a parental manipulation manner) and direct effect zygotic genes (expressed in an offspring control manner) are likely involved in the evolution of eusociality. We conclude by describing theoretical and empirical advances with indirect genetic effects and sociogenomics, and we provide specific quantitative genetic and genomic predictions from our heterochrony model for the evolutionary origin and elaboration of eusociality.     

Stable eusociality via maternal manipulation when resistance is costless

In many eusocial species, queens use pheromones to influence offspring to express worker phenotypes. Although evidence suggests that queen pheromones are honest signals of the queen's reproductive health, here I show that queen's honest signalling can result from ancestral maternal manipulation. I develop a mathematical model to study the coevolution of maternal manipulation, offspring resistance to manipulation and maternal resource allocation. I assume that (i) maternal manipulation causes offspring to be workers against offspring's interests; (ii) offspring can resist at no direct cost, as is thought to be the case with pheromonal manipulation; and (iii) the mother chooses how much resource to allocate to fertility and maternal care. In the coevolution of these traits, I find that maternal care decreases, thereby increasing the benefit that offspring obtain from help, which in the long run eliminates selection for resistance. Consequently, ancestral maternal manipulation yields stable eusociality despite costless resistance. Additionally, ancestral manipulation in the long run becomes honest signalling that induces offspring to help. These results indicate that both eusociality and its commonly associated queen honest signalling can be likely to originate from ancestral manipulation.     

Cannibalistic siblicide in praying mantis nymphs (Miomantis caffra)

Inclusive fitness theory predicts that cannibalism should be more likely to arise if close relatives can be avoided, suggesting that cannibalistic species will possess mechanisms for minimizing predation on kin. Juvenile Miomantis caffra are good candidates for the possession of such traits because; (1) groups of siblings hatch together into the same locale, (2) they are aggressive hunters, and (3) they are strongly cannibalistic. In this study, the possibility of kin recognition or avoidance in M. caffra is investigated by laboratory comparison of cannibalism rates between groups of differing relatedness. In order to examine the likelihood of encounters between early instar siblings, the extent of dispersal away from the ootheca in the days following hatching is also observed. Nymphs did not rapidly disperse after hatching, so the chances of full siblings encountering one another in the wild appear to be high. Despite this, cannibalism was equally high in groups of full siblings and groups of mixed parenthood. We suggest that for M. caffra, a generalist ambush predator, the benefits of indiscriminate aggression may outweigh any inclusive fitness benefits that would be gained from kin discrimination.     

The validity and value of inclusive fitness theory

Social evolution is a central topic in evolutionary biology, with the evolution of eusociality (societies with altruistic, non-reproductive helpers) representing a long-standing evolutionary conundrum. Recent critiques have questioned the validity of the leading theory for explaining social evolution and eusociality, namely inclusive fitness (kin selection) theory. I review recent and past literature to argue that these critiques do not succeed. Inclusive fitness theory has added fundamental insights to natural selection theory. These are the realization that selection on a gene for social behaviour depends on its effects on co-bearers, the explanation of social behaviours as unalike as altruism and selfishness using the same underlying parameters, and the explanation of within-group conflict in terms of non-coinciding inclusive fitness optima. A proposed alternative theory for eusocial evolution assumes mistakenly that workers' interests are subordinate to the queen's, contains no new elements and fails to make novel predictions. The haplodiploidy hypothesis has yet to be rigorously tested and positive relatedness within diploid eusocial societies supports inclusive fitness theory. The theory has made unique, falsifiable predictions that have been confirmed, and its evidence base is extensive and robust. Hence, inclusive fitness theory deserves to keep its position as the leading theory for social evolution.     

Kin recognition in Rana cascadae tadpoles: maternal and paternal effects

Cascades frog (Rana cascadae) tadpoles preferentially associate with full siblings over half sibling and half siblings over non-siblings when reared with siblings or as isolates. These tadpoles can use cues of maternal or paternal origin in distinguishing siblings from non-siblings, but maternal cues are preferred over paternal cues. This suggests that a hierarchy of cue importance may exist. Our results are consistent with both a phenotypic matching and a genetic recognition system of kin recognition. Thus, both learned and innate components may play a role in R. cascadae sibling recognition. Kin recognition may facilitate preferential treatment of kin, such as cooperation in food finding or in warning against predators, and therefore those individuals behaving altruistically in kin groups can increase their inclusive fitness.     

Frequency of social nesting in the sweat bee Megalopta genalis (Halictidae) does not vary across a rainfall gradient, despite disparity in brood production and body size

Local environmental conditions can facilitate or preclude the development of eusocial colonies in insects that facultatively express behavioural-caste polyphenism. To explore how environmental variability relates to the expression of social behaviour, we collected 120 nests of the facultatively social sweat bee, Megalopta genalis (Halictidae: Augochlorini), along a nearly twofold rainfall gradient in central Panama. Brood rearing activity of bees in seasonal neotropical forests should track flowering phenologies, which are typically set by rainfall and phylogenetic patterns. Nests were collected at roughly similar times of year from three sites comprising wet, moist and dry lowland tropical forests. There were significant differences in ovarian development, brood production and body size across sites for some comparisons, but no effect on the proportion of social colonies collected at each site. Results show that phenotypes of M. genalis relevant to social behaviour (ovarian development, brood production, body size) may be responsive to variation in local environment over distances of <20 km.     

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.     

Optimal colony fissioning in social insects: testing an inclusive fitness model with honey bees

In most species of social insects, when a queen departs from her parental nest to found a new colony, she leaves on her own. In some species, however, the departing queen leaves accompanied by a portion of the parental colony’s workers and there is a permanent fissioning of the worker force. Little is known about how the adult workers in colonies of fissioning species distribute themselves between the old and the new colonies. We examined this problem, building on Bulmer’s (J Theor Biol 100: 329–339, 1983) model for the optimal splitting of a colony’s adult workforce during colony reproduction. We first created an inclusive fitness model of optimal colony fissioning that applies to species in which fissioning gives rise to two autonomous colonies. The model predicts the optimal “swarm fraction”, which we define as the proportion of the adult workers in a fissioning colony that join the departing queen. We then tested the model by comparing the predicted and observed swarm fractions in honey bees. We found a close match between predicted (0.76–0.77) and observed (0.72 ± 0.04) swarm fractions. Evidently, worker honey bees distribute themselves between the old and new colonies in a way that jointly maximizes the inclusive fitness of each worker. We conclude by discussing additional ways to test the model.     

The evolution of queen control over worker reproduction in the social Hymenoptera

A trademark of eusocial insect species is reproductive division of labor, in which workers forego their own reproduction while the queen produces almost all offspring. The presence of the queen is key for maintaining social harmony, but the specific role of the queen in the evolution of eusociality remains unclear. A long‐discussed scenario is that a queen either behaviorally or chemically sterilizes her workers. However, the demographic and ecological conditions that enable such manipulation are still debated. We study a simple model of evolutionary dynamics based on haplodiploid genetics. Our model is set in the commonly observed case where workers have lost the ability to lay female (diploid) eggs by mating, but retain the ability to lay male (haploid) eggs. We consider a mutation that acts in a queen, causing her to control the reproductive behavior of her workers. Our mathematical analysis yields precise conditions for the evolutionary emergence and stability of queen‐induced worker sterility. These conditions do not depend on the queen's mating frequency. We find that queen control is always established if it increases colony reproductive efficiency, but can evolve even if it decreases colony efficiency. We further derive the conditions under which queen control is evolutionarily stable against invasion by mutant workers who have recovered the ability to lay male eggs.     

Nestmate recognition in the stingless bee Melipona panamica (Apidae, Meliponini)

Summary: Nestmate recognition was studied in the Neotropical stingless bee Melipona panamica, a species in which workers "sneak" their own reproductive eggs into 1 % of brood cells. We manipulated four factors that could influence individual recognition cues: the mother queen, the environment during the immature stage, the environment during the early adult stage, and worker age. We also simulated the action of natural enemies on colonies tested for discrimination of such worker characteristics. All factors that we tested affected responses of the discriminating workers, which could recognize sisters, nieces and unrelated workers. Previous exposure of unrelated callow bees to the odor of the host nest greatly increased chances of acceptance by the host colony. Probability of acceptance decreased, however, with increasing age of introduced bees or increasing disturbance of the host colony. These complexities in patterns of nestmate recognition and nest defense are adequately explained from the standpoint of inclusive fitness of the discriminating workers. Differences in nestmate recognition and worker egg laying among Meliponini are also discussed.     

Vitellogenin and vitellogenin receptor gene expression is associated with male and female parenting in a subsocial insect

Complex social behaviour in Hymenoptera has been hypothesized to evolve by co-opting reproductive pathways (the ovarian ground plan hypothesis, OGPH) and gene networks (the reproductive ground plan hypothesis, RGPH). In support of these hypotheses, in eusocial Hymenoptera where there is reproductive division of labour, the yolk precursor protein vitellogenin (Vg) influences the expression of worker social behaviour. We suggest that co-opting genes involved in reproduction may occur more generally than just in the evolution of eusociality; i.e. underlie earlier stages of social evolution such as the evolution of parental care, given that reproduction and parental care rarely overlap. We therefore examined vitellogenin (vg) gene expression associated with parental care in the subsocial beetle Nicrophorus vespilloides. We found a significant reduction in the expression of vg and its receptor, vgr, in head tissue during active parental care, and confirmed that the receptor is expressed in the brains of both sexes. Ours is the first study to show that vgr is expressed in the brain of a non-eusocial insect. Given the association between behaviour and gene expression in both sexes, and the presence of vitellogenin receptors in the brain, we suggest that Vg was co-opted early in the evolution of sociality to have a regulatory function. This extends the association of Vg in parenting to subsocial species and outside of the Hymenoptera, and supports the hypothesis that the OGPH is general and that heterochrony in gene expression is important in the evolution of social behaviour and precedes subsequent evolutionary specialization of social roles.