Maternal manipulation of offspring size can trigger the evolution of eusociality in promiscuous species.

Eusocial organisms typically live in colonies with one reproductive queen supported by thousands of sterile workers. It is widely believed that monogamous mating is a precondition for the evolution of eusociality. Here, we present a theoretical model that simulates a realistic scenario for the evolution of eusociality. In the model, mothers can evolve control over resource allocation to offspring, affecting offspring's body size. The offspring can evolve body-size-dependent dispersal, by which they disperse to breed or stay at the nest as helpers. We demonstrate that eusociality can evolve even if mothers are not strictly monogamous, provided that they can constrain their offspring's reproduction through manipulation. We also observe the evolution of social polymorphism with small individuals that help and larger individuals that disperse to breed. Our model unifies the traditional kin selection and maternal manipulation explanations for the evolution of eusociality and demonstrates that-contrary to current consensus belief-eusociality can evolve despite highly promiscuous mating.

Coevolution of larval signalling and worker response can trigger developmental caste determination in social insects.

Eusocial insects belong to distinct queen and worker castes, which, in turn, can be divided into several morphologically specialized castes of workers. Caste determination typically occurs by differential nutrition of developing larvae. We present a model for the coevolution of larval signalling and worker task allocation-both modelled by flexible smooth reaction norms-to investigate the evolution of caste determination mechanisms and worker polymorphism. In our model, larvae evolve to signal their nutritional state to workers. The workers evolve to allocate time to foraging for resources versus feeding the brood, conditional on the larval signals and their body size. Worker polymorphism evolves under accelerating foraging returns of increasing body size, which causes selection to favour large foraging and small nursing workers. Worker castes emerge because larvae evolve to amplify their signals after obtaining some food, which causes them to receive more food, while the other larvae remain unfed. This leads to symmetry-breaking among the larvae, which are either well-nourished or malnourished, thus emerging as small or large workers. Our model demonstrates the evolution of nutrition-dependent caste determination and worker polymorphism by a self-reinforcement mechanism that evolves from the interplay of larval signalling and worker response to the signals.

The evolution of ageing in cooperative breeders.

Cooperatively breeding animals live longer than their solitary counterparts. This has been suggested for birds, mole rats, and social insects. A common explanation for these long lifespans is that cooperative breeding evolves more readily in long-lived species because lower mortality reduces the rate of territory turnover and thus leads to a limitation of breeding territories. Here, we reverse this argument and show that-rather than being a cause for its evolution-long lifespans are an evolutionary consequence of cooperative breeding. In evolutionary individual-based simulations, we show that natural selection favors a delayed onset of senescence in cooperative breeders, relative to solitary breeders, because cooperative breeders have a delayed age of first reproduction as helpers wait in a reproductive queue to obtain breeder status. Especially long lifespans evolve in cooperative breeders in which queue positions depend on the helpers' age rank among the helpers within the breeding territory. Furthermore, we show that lower genetic relatedness among group members leads to the evolution of longer lifespans. This is because selection against higher mortality is weaker when mortality reduces competition for breeding between relatives. Our results link the evolutionary theory of ageing with kin selection theory, demonstrating that the evolution of ageing in cooperative breeders is driven by the timing of reproduction and kin structure within breeding territories.

Resource sharing is sufficient for the emergence of division of labour.

Division of labour occurs in a broad range of organisms. Yet, how division of labour can emerge in the absence of pre-existing interindividual differences is poorly understood. Using a simple but realistic model, we show that in a group of initially identical individuals, division of labour emerges spontaneously if returning foragers share part of their resources with other group members. In the absence of resource sharing, individuals follow an activity schedule of alternating between foraging and other tasks. If non-foraging individuals are fed by other individuals, their alternating activity schedule becomes interrupted, leading to task specialisation and the emergence of division of labour. Furthermore, nutritional differences between individuals reinforce division of labour. Such differences can be caused by increased metabolic rates during foraging or by dominance interactions during resource sharing. Our model proposes a plausible mechanism for the self-organised emergence of division of labour in animal groups of initially identical individuals. This mechanism could also play a role for the emergence of division of labour during the major evolutionary transitions to eusociality and multicellularity.

Antagonistic pleiotropy and the evolution of extraordinary lifespans in eusocial organisms.

Queens of eusocial species live extraordinarily long compared to their workers. So far, it has been argued that these lifespan divergences are readily explained by the classical evolutionary theory of ageing. As workers predominantly perform risky tasks, such as foraging and nest defense, and queens stay in the well-protected nests, selection against harmful genetic mutations expressed in old age should be weaker in workers than in queens due to caste differences in extrinsic mortality risk, and thus, lead to the evolution of longer queen and shorter worker lifespans. However, these arguments have not been supported by formal models. Here, we present a model for the evolution of caste-specific ageing in social insects, based on Williams' antagonistic pleiotropy theory of ageing. In individual-based simulations, we assume that mutations with antagonistic fitness effects can act within castes, that is, mutations in early life are accompanied by an antagonistic effect acting in later life, or between castes, where antagonistic effects emerge due to caste antagonism or indirect genetic effects between castes. In monogynous social insect species with sterile workers, large lifespan divergences between castes evolved under all different scenarios of antagonistic effects, but regardless of the degree of caste-specific extrinsic mortality. Mutations with antagonistic fitness effects within castes reduced lifespans of both castes, while mutations with between-caste antagonistic effects decreased worker lifespans more than queen lifespans, and consequently increased lifespan divergences. Our results challenge the central explanatory role of extrinsic mortality for caste-specific ageing in eusocial organisms and suggest that antagonistic pleiotropy affects castes differently due to reproductive monopolization by queens, hence, reproductive division of labor. Finally, these findings provide new insights into the evolution of tissue-specific ageing in multicellular organisms in general.