Abstract
Explaining the origin of eusociality, with strict division of labour between workers and reproductives, remains one of evolutionary biology’s greatest challenges. Specific combinations of genetic, behavioural and demographic traits in Hymenoptera are thought to explain their relatively high frequency of eusociality, but quantitative models integrating such preadaptations are lacking. Here we use mathematical models to show that the joint evolution of helping behaviour and maternal sex ratio adjustment can synergistically trigger both a behavioural change from solitary to eusocial breeding, and a demographic change from a life cycle with two reproductive broods to a life cycle in which an unmated cohort of female workers precedes a final generation of dispersing reproductives. Specific suits of preadaptations are particularly favourable to the evolution of eusociality: lifetime monogamy, bivoltinism with male generation overlap, hibernation of mated females and haplodiploidy with maternal sex ratio adjustment. The joint effects of these preadaptations may explain the abundance of eusociality in the Hymenoptera and its virtual absence in other haplodiploid lineages.
Highlights
Explaining the origin of eusociality, with strict division of labour between workers and reproductives, remains one of evolutionary biology’s greatest challenges
The female hibernation life cycle is a common feature of Halictine bees[30], bumblebees[31,32], Vespine and Polistes wasps[33], where despite large diversity in life history and social behaviour, life cycles usually start with a solitary mated female or occasionally groups of mated females
In primitively eusocial Halictines, despite workers keeping the potential to reproduce, the life cycle resembles the one described by our model: colonies first produce a female-biased helper brood followed by a reproductive brood at the end of the season
Summary
Explaining the origin of eusociality, with strict division of labour between workers and reproductives, remains one of evolutionary biology’s greatest challenges. Maternal manipulation of offspring sex ratios and bivoltinism, several additional factors have been proposed to bias the odds in favour of eusociality, such as specific life cycle structures, ecological conditions[16,17] and last but not least a monogamous mating system[18,19,20]. It is unknown how these factors jointly affect the evolution of reproductive altruism, and in particular whether they act synergistically in promoting it. We show that sex ratio evolution causes the production of a first brood of unmated workers before a brood of reproductives, leading to a univoltine life cycle reminiscent of annual colonies of bumblebees and vespine (yellowjacket) wasps that produce workers in the spring and early summer and a final brood of reproductive at the end of the season
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