Evolutionary routes to stable ownership.

Ownership can evolve in potentially any species. Drawing on insights from across disciplines, we distinguish between possession and ownership and present species-neutral criteria for ownership, defined as respect for possession. We use a variant of the tug-of-war evolutionary game to demonstrate how ownership can evolve in the form of a new, biologically realistic strategy, Restraint With Retaliation (RWR). In our game, resource holding potential (RHP) is assumed to be equal between interactants, and resource holding asymmetry determines whether ownership is adaptive. RWR will be evolutionarily stable when the ratio of resource holdings between interactants is relatively low, but not when this ratio is sufficiently high. We offer RWR as one evolutionary route to ownership among many, and discuss how ownership unites previously described behavioural phenomena across taxa. We propose that some but not all mechanisms of territory formation and maintenance can be considered ownership, and show that territories are not the only resources that can be owned. We argue that ownership can be a powerful cooperative solution to tragedies of the commons and problems of collective action throughout the biological world. We advance recent scholarship that has begun to investigate the biological importance of ownership, and we call for a comprehensive account of its evolutionary logic and taxonomic distribution. We propose that ownership should be considered a fundamental, unifying biological phenomenon.

Asymmetry within social groups: division of labour and intergroup competition.

Social animals vary in their ability to compete with group members over shared resources and also vary in their cooperative efforts to produce these resources. Competition among groups can promote within-group cooperation, but many existing models of intergroup cooperation do not explicitly account for observations that group members invest differentially in cooperation and that there are often within-group competitive or power asymmetries. We present a game theoretic model of intergroup competition that investigates how such asymmetries affect within-group cooperation. In this model, group members adopt one of two roles, with relative competitive efficiency and the number of individuals varying between roles. Players in each role make simultaneous, coevolving decisions. The model predicts that although intergroup competition increases cooperative contributions to group resources by both roles, contributions are predominantly from individuals in the less competitively efficient role, whereas individuals in the more competitively efficient role generally gain the larger share of these resources. When asymmetry in relative competitive efficiency is greater, a group's per capita cooperation (averaged across both roles) is higher, due to increased cooperation from the competitively inferior individuals. For extreme asymmetry in relative competitive efficiency, per capita cooperation is highest in groups with a single competitively superior individual and many competitively inferior individuals, because the latter acquiesce and invest in cooperation rather than within-group competition. These predictions are consistent with observed features of many societies, such as monogynous Hymenoptera with many workers and caste dimorphism.

Escalated conflict in a social hierarchy.

Animals that live in cooperative societies form hierarchies in which dominant individuals reap disproportionate benefits from group cooperation. The stability of these societies requires subordinates to accept their inferior status rather than engage in escalated conflict with dominants over rank. Applying the logic of animal contests to these cases predicts that escalated conflict is more likely where subordinates are reproductively suppressed, where group productivity is high, relatedness is low, and where subordinates are relatively strong. We tested these four predictions in the field on co-foundress associations of the paper wasp Polistes dominulus by inducing contests over dominance rank experimentally. Subordinates with lower levels of ovarian development, and those in larger, more productive groups, were more likely to escalate in conflict with their dominant, as predicted. Neither genetic relatedness nor relative body size had significant effects on the probability of escalation. The original dominant emerged as the winner in all except one escalated contest. The results provide the first evidence that reproductive suppression of subordinates increases the threat of escalated conflict, and hence that reproductive sharing can promote stability of the dominant-subordinate relationship.

Comparison of brain volumes between single and multiple foundresses in the paper wasp Polistes dominulus.

Queens of the paper wasp Polistes dominulus have the option to found nests in spring alone or together with other queens. In the latter case a dominance hierarchy is established among the cofoundresses with the dominant wasp getting the major share of the reproductive output of the nest. The different reproductive strategies of an individual wasp will necessitate different behaviors. We measured the volumes of brain structures as a potential indicator of differential use and elaboration of a number of brain structures. We found a significant increase in the volume of the antennal lobe in members of multiple foundress associations in comparison to single foundresses. The volume of the collar, a substructure of the calyx of the mushroom body, was also significantly larger, especially in the dominant queen of a foundress association. No significant differences between dominant or subordinate wasps in regard to volume of the measured brain substructures were found.

Signaling individual identity versus quality: a model and case studies with ruffs, queleas, and house finches.

We develop an evolutionary model that predicts that characters selected to signal individual identity will have properties differing from those expected for indicator signals of quality. Traits signaling identity should be highly variable, often display polymodal distributions, not be condition dependent (i.e., be cheap to produce and/or maintain), not be associated with fitness differences, exhibit independent assortment of component characters, and often occur as fixed phenotypes with a high degree of genetic determination. We illustrate the existence of traits with precisely these attributes in the ornamental, conspicuously variable, and sexually dimorphic breeding plumages of ruff sandpipers Philomachus pugnax and red-billed queleas Quelea quelea. Although ruffs lek and queleas are monogamous, both species breed in high-density aggregations with high rates of social interactions (e.g., aggression and territory defense). Under these socioecological conditions, individual recognition based on visual cues may be unusually important. In contrast to these species, we also review plumage characteristics in house finches Carpodacus mexicanus, a nonterritorial, dispersed-breeding species in which plumage ornamentation is thought to signal quality. In keeping with expectations for quality signals, house finch plumage is relatively less variable, unimodally distributed, condition dependent, correlated with fitness measures, has positively correlated component characters, and is a plastic, environmentally determined trait. We briefly discuss signals of identity in other animals.

Tests of reproductive-skew models in social insects.

Reproductive-skew theory can be broadly divided into transactional models, in which reproduction is shared among group members in return for some fitness benefit, and tug-of-war models, in which reproductive sharing arises solely from an inability of each group member to fully control the others. For small-colony social insects in which complete reproductive control by a single individual is plausible, transactional-concession models account, better than any other existing model, for observed relationships between each of the dependent variables of skew, changes in reproductive partitioning over time, group size, and within-group aggression, and each of the predictor variables of genetic relatedness, ecological constraints on solitary breeding, and benefits of group living. An extension of transactional-concession models via the "workers-as-a-collective-dominant" model potentially offers new insights into some of the most striking reproductive patterns in large-colony eusocial Hymenopteran species, from the loss of worker capacity to produce female offspring to patterns of skew and aggression in polygynous societies.

Genetic support for the evolutionary theory of reproductive transactions in social wasps.

Recent evolutionary models of reproductive partitioning within animal societies (known as 'optimal skew', 'concessions' or 'transactional' models) predict that a dominant individual will often yield some fraction of the group's reproduction to a subordinate as an incentive to stay in the group and help rear the dominant's offspring. These models quantitatively predict how the magnitude of the subordinate's 'staying incentive' will vary with the genetic relatedness between dominant and subordinate, the overall expected group output and the subordinate's expected output if it breeds solitarily. We report that these predictions accord remarkably well with the observed reproductive partitioning between conesting dominant and subordinate queens in the social paper wasp Polistes fuscatus. In particular, the theory correctly predicts that (i) the dominant's share of reproduction, i.e. the skew, increases as the colony cycle progresses and (ii) the skew is positively associated both with the colony's productivity and with the relatedness between dominant and subordinate. Moreover, aggression between foundresses positively correlated with the skew, as predicted by transactional but not alternative tug-of-war models of societal evolution. Thus, our results provide the strongest (quantitative support yet for a unifying model of social evolution.

Extra-pair paternity as the result of reproductive transactions between paired mates.

Transactional ('optimal skew' or concessions') models of social evolution emphasize that dominant members of society can be favoured for donating parcels of reproduction to same-sexed subordinates in return for cooperation by the latter. We developed a mathematically similar model in which extra-pair paternity in broods receiving biparental care is viewed as emerging from a reproductive transaction between the paired mates. The model quantitatively predicted the maximum paternity that a male mate can demand before its female mate is favoured to break the pair bond and caring solitarily for a brood sired entirely by a neighbouring male. The model predicts that extra-pair paternity results when the neighbouring male is of sufficiently higher quality than the male mate. In such cases, the exact amount of extra-pair paternity will vary directly with the difference in quality between the two males and inversely with the value (fitness impact) of the male mate's parental care. Importantly, the transactional model provided a unified explanation for experimental and observational evidence that extra-pair paternity rises with decreasing quality of the male mate, increasing genetic variability among breeding males, increasing breeding density, increasing availability of food and decreasing involvement of the male mate in parental care.

Dispersal of first "workers" in social wasps: causes and implications of an alternative reproductive strategy.

Many "workers" in north temperate colonies of the eusocial paper wasp Polistes fuscatus disappear within a few days of eclosion. We provide evidence that these females are pursuing an alternative reproductive strategy, i.e., dispersing to overwinter and become nest foundresses the following spring, instead of helping to rear brood on their natal nests. A female is most likely to stay and help at the natal nest (i.e., least likely to disperse) when it is among the first workers to emerge and when it emerges on a nest with more pupae (even though worker-brood relatedness tends to be lower in such colonies). The latter cause may result from the fact that pupae-laden nests are especially likely to survive, and thus any direct or indirect reproductive payoffs for staying and working are less likely to be lost. Disappearing females are significantly smaller than predicted if dispersal tendency was independent of body size (emergence order-controlled), suggesting that the females likely to be most effective at challenging for reproductive rights within the natal colony (i.e., the largest females) are also most likely to stay. Thus, early dispersal is conditional on a female's emergence order, the maturity of its natal nest, and its body size. Finally, we present evidence that foundresses may actively limit the sizes of first-emerging females, perhaps to decrease the probability that the latter can effectively challenge foundresses for reproductive rights. The degree to which foundresses limit the size of first-emerging females accords well with the predictions of the theory of staying incentives.

Reproductive bribing and policing as evolutionary mechanisms for the suppression of within-group selfishness.

We show that a new, simple, and robust general mechanism for the social suppression of within-group selfishness follows from Hamilton's rule applied in a multilevel selection approach to asymmetrical, two-person groups: If it pays a group member to behave selfishly (i.e., increase its share of the group's reproduction, at the expense of group productivity), then its partner will virtually always be favored to provide a reproductive "bribe" sufficient to remove the incentive for the selfish behavior. The magnitude of the bribe will vary directly with the number of offspring (or other close kin) potentially gained by the selfish individual and inversely with both the relatedness r between the interactants and the loss in group productivity because of selfishness. This bribe principle greatly extends the scope for cooperation within groups. Reproductive bribing is more likely to be favored over social policing for dominants rather than subordinates and as intragroup relatedness increases. Finally, analysis of the difference between the group optimum for an individual's behavior and the individual's inclusive fitness optimum reveals a paradoxical feedback loop by which bribing and policing, while nullifying particular selfish acts, automatically widen the separation of individual and group optima for other behaviors (i.e., resolution of one conflict intensifies others).

Partitioning of reproduction in animal societies.

A key feature differentiating cooperative animal societies Is the apportionment of reproduction among individuals. Only recently have studies started to focus on intraspecific variability in the distribution of reproduction within animal societies, and the available data suggest that this variability might be greater than previously suspected. How can one account for intra-and interspecific variability in partitioning of reproduction? This Is one of the most intriguing problems in the study of social behaviour, and understanding the factors underlying this variability is one of the keys to understanding the properties of complex animal societies.

Opportunistic adoption of orphaned nests in paper wasps as an alternative reproductive strategy.

Adoption of abandoned or orphaned nests by adult females occurs commonly during the colony-founding period of the primitively eusocial paper wasp, Polistes dominulus. Our evidence indicates that adoption reflects: (1) 'making the best of a bad situation,' for queens who have lost their nests; (2) subordinates leaving multiple-foundress associations; and (3) possibly, a 'sit-and-wait' strategy, in which non-nesting females wait for nests to be orphaned. A 'it-and-wait strategy' implies that wasps facultatively delay personal reproduction rather than that the delay in reproduction is due to physiological constraints (sensu Gadagkar, 1991a). Orphaned nests with related brood are not more attractive than those bearing unrelated brood, suggesting that nest-adoption has not evolved primarily as a strategy to rescue non-descendant kin. Instead, all wasps tend to adopt nests that theoretically maximize their selfish genetic interests: the most attractive nests were large combs at an advanced stage of development. These nests can produce more workers and are closer to worker emergence, at which time colony survival per unit time dramatically rises. The primary proximate cue for adoption seems to be whether nests contain later-instar larvae or pupae. Since developmental stage of brood correlates with nest size, preferred nests thus tend to be relatively mature and large.

Queen activation of lazy workers in colonies of the eusocial naked mole-rat.

Evolutionary conflicts of interest are expected to arise in genetically diverse social groups. In eusocial insect societies, a potential conflict exists between the queen and her workers over how active the workers should be, and evidence exists that queen aggression increases activity levels of her lazier workers. Here I provide evidence that queen aggression (shoving) in laboratory colonies of the eusocial mammal, the naked mole-rat (Heterocephalus glaber), is a convergently evolved manifestation of queen-worker conflict over worker activity. Queen-initiated shoves activate inherently lazy workers, which tend to be larger and/or less related to the queen than are infrequently shoved, industrious workers. In addition, queen removal selectively depresses the activity of workers that are larger and less related to her. Finally, queen shoving and worker inactivity are pronounced when colonies are satiated but not when colonies are hungry, indicating that the underlying 'work-conflict' is highly context-specific.

DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat.

Using the technique of DNA fingerprinting, we investigated the genetic structure within and among four wild-caught colonies (n = 50 individuals) of a eusocial mammal, the naked mole-rat (Heterocephalus glaber; Rodentia: Bathyergidae). We found that DNA fingerprints of colony-mates were strikingly similar and that between colonies they were much more alike than fingerprints of non-kin in other free-living vertebrates. Extreme genetic similarity within colonies is due to close genetic relationship (mean relatedness estimate +/- SE, r = 0.81 +/- 0.10), which apparently results from consanguineous mating. The inbreeding coefficient (F = 0.45 +/- 0.18) is the highest yet recorded among wild mammals. The genetic structure of naked mole-rat colonies lends support to kin selection and ecological constraints models for the evolution of cooperative breeding and eusociality.