Smaldino proposes emergent properties of human groups, arising when individuals display both differentiation and organization, constitute a novel unit of cultural selection not addressed by current evolutionary theory. We propose existing theoretical frameworks for maintenance of genetic diversity - social heterosis and social genomes - can similarly explain the appearance and maintenance of human cultural diversity (i.e., group-level traits) and collaborative interdependence.

Developmental maternal effects are a potentially important source of phenotypic variation, but they can be difficult to distinguish from other environmental factors. This is an important distinction within the context of social evolution, because if variation in offspring helping behavior is due to maternal manipulation, social selection may act on maternal phenotypes, as well as those of offspring. Factors correlated with social castes have been linked to variation in developmental nutrition, which might provide opportunity for females to manipulate the social behavior of their offspring. Megalopta genalis is a mass-provisioning facultatively eusocial sweat bee for which production of males and females in social and solitary nests is concurrent and asynchronous. Female offspring may become either gynes (reproductive dispersers) or workers (non-reproductive helpers). We predicted that if maternal manipulation plays a role in M. genalis caste determination, investment in daughters should vary more than for sons. The mass and protein content of pollen stores provided to female offspring varied significantly more than those of males, but volume and sugar content did not. Sugar content varied more among female eggs in social nests than in solitary nests. Provisions were larger, with higher nutrient content, for female eggs and in social nests. Adult females and males show different patterns of allometry, and their investment ratio ranged from 1.23 to 1.69. Adult body weight varied more for females than males, possibly reflecting increased variation in maternal investment in female offspring. These differences are consistent with a role for maternal manipulation in the social plasticity observed in M. genalis.

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 reproductive (queen) and nonreproductive (worker) castes of eusocial insect colonies are a classic example of insect polyphenism. A complementary polyphenism may also exist entirely among females in the reproductive caste. Although less studied, reproductive females may vary in behavior based on size-associated attributes leading to the production of daughter workers. We studied a bee with flexible social behavior, Megalopta genalis, to better understand the potential of this polyphenism to shape the social organization of bee colonies and, by extension, its role in the evolution of eusociality. Our experimental design reduced variation among nest foundresses in life history variables that could influence reproductive decisions, such as nesting quality and early adulthood experience. Within our study population, approximately one third of M. genalis nests were eusocial and the remaining nests never produced workers. Though they do not differ in survival, nest-founding females who do not attempt to produce workers (which we refer to as the solitary phenotype) are significantly smaller and become reproductive later than females who attempt to recruit workers (the social phenotype). Females with the social phenotype are more likely to produce additional broods but at a cost of having some of their first offspring become nonreproductive workers. The likelihood of eusocial organization varies with body size across females of the social phenotype. Thus, fitness consequences associated with size-based plasticity in foundress behavior has colony level effects on eusociality. The potential for size-based polyphenisms among reproductive females may be an important factor to consider in the evolutionary origins of eusociality. © 2012 Springer-Verlag Berlin Heidelberg.

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.