ROLE SPECIALIZATION AND PLASTICITY AT THE ORIGIN OF EUSOCIALITY

The evolution of eusociality, where some individuals forfeit their own reproduction to help others, represents one of the major evolutionary transitions. The fundamental feature of eusociality is the division of labour: queens are specialist egg-layers while workers specialize on tasks such as foraging. Numerous factors that could favour helping have been identified, and its evolution can appear deceptively simple. For example, the fact that females are as closely related to their siblings as to their own offspring might suggest that just a tiny advantage over independent nesting will be enough to promote the evolution of helping. However, this implies that there was extensive pre-existing plasticity at the origin of eusociality, allowing individuals to take on roles similar to today's queens and workers. In the often-imagined scenario where a mutant offspring takes over brood provisioning, ceding egg-laying rights to a mother 'queen', the offspring could have to provision at twice the rate of an independent breeder, and the mother could have to lay twice as many eggs, to avoid selection on daughters favouring the ancestral strategy. This might be achieved if specialization frees up resources no longer utilized in performing one role, but only if there is a highly efficient trade-off between functions. A key unanswered question is therefore how efficient division of labour would be when it first evolved. Efficiency also requires tolerance and responsiveness: would ancestral females accept provisions provided by helpers, and would they adjust their own feeding effort accordingly?

The payoff through specialization could be condition-dependent. A long-standing hypothesis is that the first helpers were small females with low reproductive value that forfeited little by helping a fully fertile relative. However, the extent to which payoffs to ancestral females from providing or receiving help depend on phenotype remains unclear. Furthermore, a critical untested assumption of the subfertility hypothesis concerns the foraging ability of small/subfertile females. Such females may have low fecundity when nesting independently, but the subfertility hypothesis assumes that they will perform better with helper tasks such as provisioning.

Key objectives are to use large-scale field manipulations of the well studied non-social wasp Ammophila pubescens to for the first time:
(1) Test the benefits of role specialization: to what extent can non-social females increase their lifetime egg-laying or provisioning when forced experimentally to specialize?
(2) Test a key assumption of the subfertility hypothesis: do small females have the most to gain through specializing as provisioners?
(3) Test whether there are complementary phenotype combinations where both parties could gain by nesting together
(4) Test the tolerance and responsiveness of non-social females to received help

The overall result will be a new and exciting perspective on how trade-offs and plasticity could influence or constrain the origin of eusociality, with important implications for the magnitude of ecological and genetic advantages necessary for eusociality to be favoured by selection.

The work will benefit the international community of researchers in a variety of disciplines such as entomology, evolutionary biology, behavioural ecology and animal behaviour, including both theoreticians and empiricists, as well as those working specifically on social evolution and the evolution of animal societies. The specific research focus has been little studied, so that there is potential for a significant advancement of knowledge, in terms of both the novel approach and the new data that will be generated. There are interesting parallels between the division of labour in social insects and other taxa such as bacteria and algae.