It is generally accepted that from a theoretical perspective, haplodiploidy should facilitate the evolution of eusociality. However, the "haplodiploidy hypothesis" rests on theoretical arguments that were made before recent advances in our empirical understanding of sex allocation and the route by which eusociality evolved. Here we show that several possible promoters of the haplodiploidy effect would have been unimportant on the route to eusociality, because they involve traits that evolved only after eusociality had become established. We then focus on two biological mechanisms that could have played a role: split sex ratios as a result of either queen virginity or queen replacement. We find that these mechanisms can lead haplodiploidy to facilitating the evolution of helping but that their importance varies from appreciable to negligible, depending on the assumptions. Furthermore, under certain conditions, haplodiploidy can even inhibit the evolution of helping. In contrast, we find that the level of promiscuity has a strong and consistently negative influence on selection for helping. Consequently, from a relatedness perspective, monogamy is likely to have been a more important driver of eusociality than the haplodiploidy effect.

Malaria parasites must undergo a round of sexual reproduction in the blood meal of a mosquito vector to be transmitted between hosts. Developing a transmission-blocking intervention to prevent parasites from mating is a major goal of biomedicine, but its effectiveness could be compromised if parasites can compensate by simply adjusting their sex allocation strategies. Recently, the application of evolutionary theory for sex allocation has been supported by experiments demonstrating that malaria parasites adjust their sex ratios in response to infection genetic diversity, precisely as predicted. Theory also predicts that parasites should adjust sex allocation in response to host immunity. Whilst data are supportive, the assumptions underlying this prediction – that host immune responses have differential effects on the mating ability of males and females – have not yet been tested. Here, we combine experimental work with theoretical models in order to investigate whether the development and fertility of male and female parasites is affected by innate immune factors and develop new theory to predict how parasites' sex allocation strategies should evolve in response to the observed effects. Specifically, we demonstrate that reactive nitrogen species impair gametogenesis of males only, but reduce the fertility of both male and female gametes. In contrast, tumour necrosis factor-α does not influence gametogenesis in either sex but impairs zygote development. Therefore, our experiments demonstrate that immune factors have complex effects on each sex, ranging from reducing the ability of gametocytes to develop into gametes, to affecting the viability of offspring. We incorporate these results into theory to predict how the evolutionary trajectories of parasite sex ratio strategies are shaped by sex differences in gamete production, fertility and offspring development. We show that medical interventions targeting offspring development are more likely to be ‘evolution-proof’ than interventions directed at killing males or females. Given the drive to develop medical interventions that interfere with parasite mating, our data and theoretical models have important implications. Malaria and related parasites cause some of the most serious infectious diseases of humans, domestic animals and wildlife. To be transmitted, these parasites produce male and female sexual stages that differentiate into gametes and mate when taken up in a mosquito blood meal. Despite the need to develop a transmission-blocking intervention, remarkably little is understood about the evolution of parasite mating strategies. However, recent research demonstrates that producing the right ratio of male to female stages is central to mating success. Evolutionary theory predicts that sex ratios are adjusted in line with a variety of factors that affect mating success, including host immunity. We test this theory by investigating whether ubiquitous immune factors differentially affect the production and fertility of males and females. Our experiments demonstrate that immune factors have complex, sex-specific effects, from reducing gamete production to affecting offspring viability. We use these results to generate theory predicting how such effects shape the evolutionary trajectories of parasite sex ratio strategies. Given the drive to develop medical interventions that prevent transmission by blocking parasite mating, our results have important implications. Specifically, we suggest that medical interventions targeting offspring development are more likely to be ‘evolution-proof’ than interventions with sex-specific effects.

There is much interest in understanding how population demography impacts upon social evolution. Here, we consider the impact of rate and pattern of dispersal upon a classic social evolutionary trait – the sex ratio. We recover existing analytical results for individual dispersal, and we extend these to allow for budding dispersal. In particular, while a cancelling of relatedness and kin competition effects means that the sex ratio is unaffected by the rate of individual dispersal, we find that a decoupling of relatedness and kin competition means that budding dispersal favours increasingly female‐biased sex ratios. More generally, our analysis illustrates the relative ease with which biological problems involving class structure can be solved using a kin selection approach to social evolution theory.