Sexual selection and sex allocation in a simultaneous hermaphrodite

Abstract

Since Darwin’s pioneering work, sexual selection theory has become a unifying framework in evolutionary biology successfully explaining the variation in sexual dimorphism, reproductive strategies and mating systems. Although, it has long been argued that sexual selection is an important evolutionary agent in all sexually reproducing organisms, the vast majority of empirical studies on sexual selection in animals focus on separate sexed organisms. However, given that hermaphroditism is a widespread reproductive strategy among animals, empirical work on sexual selection in this group of organisms is required to evaluate the general importance of sexual selection for animals of all types of gender expression. In my PhD project, I aimed to determine the characteristics of sexual selection that operates in the outcrossing simultaneously hermaphroditic flatworm Macrostomum lignano, with a particular focus on the conditions that have been proposed to affect the sex allocation (i.e., the resource allocation to the male versus the female sex function) in simultaneous hermaphrodites. Sex allocation theory predicts that the average mating group size (i.e., the number of mating partners plus one) within a population is one of the main parameters that affect the sex allocation in simultaneous hermaphrodites. I studied the determinants of mating group size and sperm transfer success in M. lignano and found substantial between individual variation in both traits. My results suggest that mating group size is primarily affected by the number of available mating partners, but I also found that worms with relatively larger testes acquired more mates. Apart from this, I also explored the role of mate choice for its potential to restrict the number of mating partners in M. lignano. I found that sequentially mated worms copulated more frequently with well-fed worms compared to starved worms. This suggests that worms have a preference to mate more well-fed partners, presumably because well-fed partners have a higher female fecundity and therefore represent more attractive sperm recipients. Simultaneous hermaphrodites are predicted to allocate more reproductive resources into the male sex function if the mating group size increases. Until now, empirical studies testing this prediction primarily focussed on phenotypic plasticity in testis size as an estimate of male allocation. However, sperm competition theory predicts that sperm competition does not only select for larger testes but also for the production of bigger sperm. I experimentally tested for a phenotypically plastic response in sperm length to different levels of sperm competition in M. lignano. Despite that fact that my experimental manipulation of the level of sperm competition induced a phenotypically plastic response in testis size and ovary size, I found no difference in the sperm length between individuals that either experienced no or intense sperm competition. Thus, there seems to be no phenotypic plasticity in sperm length in response to the level of sperm competition in M. lignano. One crucial assumption of sexual selection theory for simultaneous hermaphrodites is that Bateman’s principle applies to this group of organisms. Consequently, the reproductive success of the female sex function is expected to be primarily limited by the resources available for egg production rather than the number of mating partners. In support of this prediction, I could demonstrate that the food availability but not the number of mating partners has an effect on the number of offspring produced by the female sex function in M. lignano. Previous research on sex allocation in simultaneous hermaphrodites mainly focused the factors that influence the resource allocation towards the male versus the female sex function, but very few attempts have been made to understand the behavioural consequences of differences in the sex allocation among individuals. I hypothesised that sex allocation has an effect on the mating behaviour in simultaneously hermaphroditic animals and predicted that individuals adopt a mating strategy that is most beneficial to the sex function that is relatively more pronounced compared to the average sex allocation in a population. An experimental test of this hypothesis revealed that more male-biased individuals mate more frequently compared to more female-biased individuals, which has been predicted if Bateman’s principle applies to M. lignano. In conclusion, my studies suggest a high potential for pre- and post-copulatory sexual selection in the simultaneously hermaphroditic flatworm M. lignano.