Evolutionary responses to the independent and interacting action of sexual selection and population spatial structureinsights from experimental evolution in a species with sexual conflict

Abstract

Sexual selection is widely accepted as one of the most potent forces driving the evolution of numerous behavioural, ecological and physiological traits involved in sexual interactions, and consequently, as a force with critical implications for population viability and for evolutionary processes such as reproductive isolation and speciation. An increasing body of research studies in the last decades have proved that sexual selection operates not only before copulation (pre-copulatory sexual selection) but also after mating (post-copulatory sexual selection). Female multiple mating behaviour (polyandry) opens the gates for sexual selection to operate after copulation through mechanisms such as sperm competition cryptic female choice, and post-copulatory sexually antagonistic selection resulting from differences in the evolutionary interests of the two sexes (sexual conflict).Bearing in mind the costs that mating entails for the organisms, specially for females, the causes underlying the origin and maintenance of polyandry have remained an evolutionary conundrum. It has been hypothesized that polyandry may be a side effect of the selection acting on males to be more competitive and successful in the face of strong competition for access to females. On the other hand, polyandry may also have an adaptive origin rooted on the direct (material) and/or indirect (genetic) benefits that females may accrue through multiple mating with different males. Many of the hypotheses related to the benefits of multiple mating are based on the existence of reliable female mate choice. Notwithstanding, assessing the quality of potential mates and making a good choice can be difficult under some circumstances. Polyandry has been also hypothesized to work as a bet-hedging strategy spreading the risk of mating with unsuitable (e.g., infertile, or genetically incompatible) mates. By sampling more males, polyandrous females may minimize the consequences of assessment errors in mate choice, reducing the risk for of complete reproductive failure for females, preventing inbreeding depression and extinction. This may be highly relevant under certain ecological and demographical conditions, for example in small populations in which stochastic changes may have a deep impact and where sexual selection cannot operate effectively. Interestingly, recent theoretical findings suggest that mating system evolution, and the influence of mating system, and therefore sexual selection, on population persistence over time are closely related to the level of population subdivision. However, while population spatial structure is accepted as an important factor mediating critical features of population dynamics as well as population viability and the population’s probability of extinction, we know very little about the implications of population spatial subdivision for sexual selection and sexual conflict dynamics, and empirical studies into the connections between population spatial structure and sexual selection are lacking. This thesis was aimed to address this gap of knowledge. To this purpose, we used the seed beetle Callosobruchus maculatus, a model for the study of sexual selection and sexual conflict, in combination with experimental evolution, one of the most powerful methodological approaches in the study of evolution, to gain insights into the independent and interactive effects of mating system and population spatial structure selection treatments on the evolution of sexual selection and sexual conflict dynamics. The main results of the research in this thesis inform that, in some cases, population spatial structure is able to reverse the evolutionary pattern imposed by sexual selection in undivided populations. These results may have far-reaching implications for the conservation of species whose populations are small or fragmented. In addition, our findings suggest that sexual conflict in C. maculatus is not as clear-cut as previously thought and that the reproductive outcomes of mating events depend on a delicate balance between benefits and costs accrued through sexual interactions.