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Two of John et al.'s examples of proxy failures in ecological situations are not failures: Runaway sexual selection and marsupial neonate competition. Instead, more appropriate ecological examples may be paternal genetic kin recognition and warning coloration. These differ in proxy effectiveness and failure in ways that illustrate the importance of "costs" in the evolution of ecological proxy traits.

Eusocial Hymenoptera are often characterized by having facultatively or obligately sterile worker castes. However, findings across an increasing number of species are that some workers are non-natal-they have 'drifted' away from where they were born and raised. Moreover, drifters are often indistinguishable from natal workers in the work and benefits provided to joined groups. This seems an evolutionary paradox of providing benefits to potentially unrelated individuals over close kin. Rather than being mistakes, drifting is proposed to be adaptive if joiners either gain inclusive fitness by preferentially moving to other kin groups or through generalized reciprocity in which exchanging workers across groups raises group-level genetic diversity and creates social heterosis. It is unclear, however, if reciprocity is unlikely because of a susceptibility to cheating. In resolving this question, a series of evolutionary simulations show: (1) Reciprocity can persist under a range of genetic assumptions and scenarios of cheating, (2) cheating almost always evolves, but can be expressed in a variety of ways that are not always predictable, (3) the inclusive fitness hypothesis is equally or more susceptible to cheating. Moreover, existing data in Hymenoptera (although not extensive) are more consistent with generalized reciprocity. This supports a hypothesis that drifting, as a phenomenon, may more often reflect maximization of group and parental fitness rather than fitness gains for the individual drifters.

Parents often face an investment trade-off between either producing many small or fewer large offspring. When environments vary predictably, the fittest parental solution matches available resources by varying only number of offspring and never optimal individual size. However when mismatches occur often between parental expectations and true resource levels, dynamic models like multifaceted parental investment (MFPI) and parental optimism (PO) both predict offspring size can vary significantly. MFPI is a "realist" strategy: parents assume future environments of average richness. When resources exceed expectations and it is too late to add more offspring, the best-case solution increases investment per individual. Brood size distributions therefore track the degree of mismatch from right-skewed around an optimal size (slight underestimation of resources) to left-skewed around a maximal size (gross underestimation). Conversely, PO is an "optimist" strategy: parents assume maximally good resource futures and match numbers to that situation. Normal or lean years do not affect "core" brood as costs primarily fall on excess "marginal" siblings who die or experience stunted growth (producing left-skewed distributions). Investment patterns supportive of both MFPI and PO models have been observed in nature, but studies that directly manipulate food resources to test predictions are lacking. Ant colonies produce many offspring per reproductive cycle and are amenable to experimental manipulation in ways that can differentiate between MFPI and PO investment strategies. Colonies in a natural population of a harvester ant (Pogonomyrmex salinus) were protein-supplemented over 2 years, and mature sexual offspring were collected annually prior to their nuptial flight. Several results support either MFPI or PO in terms of patterns in offspring size distributions and how protein differentially affected male and female production. Unpredicted by either model, however, is that supplementation affected distributions more strongly across years than within (e.g., small females are significantly rarer in the year after colonies receive protein). Parental investment strategies in P. salinus vary dynamically across years and conditions. Finding that past conditions can more strongly affect reproductive decisions than current ones, however, is not addressed by models of parental investment.

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.

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.

The role of the ant colony largely consists of non-reproductive tasks, such as foraging, tending brood, and defense. However, workers are vitally linked to reproduction through their provisioning of sexual offspring, which are produced annually to mate and initiate new colonies. Gynes (future queens) have size-associated variation in colony founding strategy (claustrality), with each strategy requiring different energetic investments from their natal colony. We compared the per capita production cost required for semi-claustral, facultative, and claustral gynes across four species of Pogonomyrmex harvester ants. We found that the claustral founding strategy is markedly expensive, costing approximately 70% more energy than that of the semi-claustral strategy. Relative to males, claustral gynes also had the largest differential investment and smallest size variation. We applied these investment costs to a model by Brown and Bonhoeffer (2003) that predicts founding strategy based on investment cost and foraging survivorship. The model predicts that non-claustral foundresses must survive the foraging period with a probability of 30-36% in order for a foraging strategy to be selectively favored. These results highlight the importance of incorporating resource investment at the colony level when investigating the evolution of colony founding strategies in ants.

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.

Social castes of eusocial insects may have arisen through an evolutionary modification of an ancestral reproductive ground plan, such that some adults emerge from development physiologically primed to specialize on reproduction (queens) and others on maternal care expressed as allo-maternal behaviour (workers). This hypothesis predicts that variation in reproductive physiology should emerge from ontogeny and underlie division of labour. To test these predictions, we identified physiological links to division of labour in a facultatively eusocial sweat bee, Megalopta genalis. Queens are larger, have larger ovaries and have higher vitellogenin titres than workers. We then compared queens and workers with their solitary counterparts-solitary reproductive females and dispersing nest foundresses-to investigate physiological variation as a factor in caste evolution. Within dyads, body size and ovary development were the best predictors of behavioural class. Queens and dispersers are larger, with larger ovaries than their solitary counterparts. Finally, we raised bees in social isolation to investigate the influence of ontogeny on physiological variation. Body size and ovary development among isolated females were highly variable, and linked to differences in vitellogenin titres. As these are key physiological predictors of social caste, our results provide evidence for developmental caste-biasing in a facultatively eusocial bee.

Social Hymenoptera have played a leading role in development and testing of kin selection theory. Inclusive fitness models, following from Hamilton's rule, successfully predict major life history characteristics, such as biased sex investment ratios and conflict over parentage of male offspring. However, kin selection models poorly predict patterns of caste-biasing nepotism and reproductive skew within groups unless kin recognition constraints or group-level selection is also invoked. These successes and failures mirror the underlying kin recognition mechanisms. With reliable environmental cues, such as the sex of offspring or the origin of male eggs, predictions are supported. When only genetic recognition cues are potentially available, predictions are not supported. Mathematical simulations demonstrate that these differing mechanisms for determining kinship produce very different patterns of behavior. Decisions based on environmental cues for relatedness result in a robust mixture of cooperation and noncooperation depending on whether or not Hamilton's rule is met. In contrast, cooperation evolves under a wider range of conditions and to higher frequencies with genetic kin recognition as shared greenbeard traits. This "excess of niceness" matches the existing patterns in caste bias and reproductive skew; individuals often help others at an apparent cost to their inclusive fitness. The results further imply a potential for greenbeard-type kin recognition to create arbitrary runaway social selection for shared genetic traits. Suggestive examples in social evolution may be alloparental care and unicoloniality in ants. Differences in kin recognition mechanisms also can have consequences for maintenance of advantageous genetic diversity within populations.

A major evolutionary question is how reproductive sharing arises in cooperatively breeding species despite the inherent reproductive conflicts in social groups. Reproductive skew theory offers one potential solution: each group member gains or is allotted inclusive fitness equal to or exceeding their expectation from reproducing on their own. Unfortunately, a multitude of skew models with conflicting predictions has led to confusion in both testing and evaluating skew theory. The confusion arises partly because one set of models (the 'transactional' type) answer the ultimate evolutionary question of what ranges of reproductive skew can yield fitness-enhancing solutions for all group members. The second set of models ('compromise') give an evolutionarily proximate, game-theoretic evolutionarily stable state (ESS) solution that determines reproductive shares based on relative competitive abilities. However, several predictions arising from compromise models require a linear payoff to increased competition and do not hold with non-linear payoffs. Given that for most species it may be very difficult or impossible to determine the true relationship between effort devoted to competition and reproductive share gained, compromise models are much less predictive than previously appreciated. Almost all skew models make one quantitative prediction (e.g. realized skew must fall within ranges predicted by transactional models), and two qualitative predictions (e.g. variation in relatedness or competitive ability across groups affects skew). A thorough review of the data finds that these three predictions are relatively rarely supported. As a general rule, therefore, the evolution of cooperative breeding appears not to be dependent on the ability of group members to monitor relatedness or competitive ability in order to adjust their behaviour dynamically to gain reproductive share. Although reproductive skew theory fails to predict within-group dynamics consistently, it does better at predicting quantitative differences in skew across populations or species. This suggests that kin selection can play a significant role in the evolution of sociality. To advance our understanding of reproductive skew will require focusing on a broader array of factors, such as the frequency of mistaken identity, delayed fitness payoffs, and selection pressures arising from across-group competition. We furthermore suggest a novel approach to investigate the sharing of reproduction that focuses on the underlying genetics of skew. A quantitative genetics approach allows the partitioning of variance in reproductive share itself or that of traits closely associated with skew into genetic and non-genetic sources. Thus, we can determine the heritability of reproductive share and infer whether it actually is the focus of natural selection. We view the 'animal model' as the most promising empirical method where the genetics of reproductive share can be directly analyzed in wild populations. In the quest to assess whether skew theory can provide a framework for understanding the evolution of sociality, quantitative genetics will be a central tool in future research.

Models of reproductive skew assume reproductive shares are either conceded, competed over, or both. Previous mathematical evaluations found that simultaneous concessions and contests are evolutionarily unstable. Recently, Shen and Reeve (2010) challenged these conclusions and developed a series of sub-models they argued to be a unified approach to reproductive skew: the general bordered tug-of-war (BTOW). However, BTOW fails as a general model for two reasons: (1) the BTOW strategy cannot invade populations where individuals either only compete for or only concede reproductive shares and (2) contrary to Shen and Reeve's assertion, BTOW populations are easily invaded by strategies with fewer or no concessions, but competing at lower levels. The failure of BTOW as a general model has major implications for interpreting experiments on reproductive skew. A large number of studies have measured the effects of genetic relatedness and competitive ability on reproductive skew, with a great majority finding no significant correlation between variation in within-group relatedness or competitive ability and across-group differences in skew. No model of reproductive skew except one variant of the BTOW predicts such results. With the rejection of BTOW as a valid general model, it is clear that these results are contradictory to reproductive skew theory rather than supportive of it.

Cooperative breeding often results in unequal reproduction between dominant and subordinate group members. Transactional skew models attempt to predict how unequal reproduction can be before the groups themselves become unstable. A number of variants of transactional models have been developed, with a key difference being whether reproduction is controlled by one party or contested by all. It is shown here that ESS solutions for all situations of contested control over reproduction are given by the original tug-of-war model (TOW). Several interesting results follow. First, TOW can escalate enough to destabilize some types of groups. Particularly vulnerable are those that have low relatedness and gain little from cooperative breeding relative to solitary reproduction. Second, TOW can drastically reduce group productivity and especially the inclusive fitness of dominant individuals. Third, these results contrast strongly with those from variants of TOW models that include concessions to maintain group stability. Such models are shown to be special cases of the general and simpler TOW framework, and to have assumptions that may be biologically suspect. Finally, the overall analysis suggests that there is no mechanism within existing TOW framework that will prevent a costly struggle for reproductive control. Because social species rarely exhibit the high levels of aggression predicted by TOW models, alternative evolutionary mechanisms are considered that can limit conflict and produce more mutually beneficial outcomes. The further development of alternative models to predict patterns of reproductive skew are highly recommended.

In many eusocial Hymenoptera, workers prevent each other from producing male offspring by destroying worker-laid eggs. Kin selection theory predicts that such 'worker policing' behaviour can evolve by increasing the average relatedness between workers and their male brood. Alternatively, if worker-laid eggs are of low relative viability, their replacement would increase the developmental reliability of the brood. Less colony investment in terms of time and resources would be lost on poor males. This gain is independent of the relatedness of the males. Unfortunately, both nepotistic and group efficiency benefits can simultaneously accrue with the replacement of worker-laid eggs. Therefore, worker behaviour towards eggs cannot completely resolve whether both processes have been equally evolutionarily important. Adequate resolution requires the presentation of worker-produced brood of various ages. The stage at which brood are replaced can discriminate whether worker policing occurs owing to a preference for closer genetic kin, a preference for the more reliable brood or both.

Ants are social and are haplodiploid. This combination may allow the evolution of a variety of unusual genetic pathways to achieve reproductive success. These include hybridizing across species, differential use of sperm to create a hybrid worker population, and reproductively isolated gene pools that depend on each other for their survival. Although there are demonstrable costs for colony development and reproduction, these phenomena may nevertheless be relatively common in nature. The specific ecological advantages that favor the evolution of these reproductive modes remain to be discovered.