Sexual selection in a transparent worm : insights from fluorescent sperm

Abstract

Sexual selection is a potent source of selection underlying the evolution of sexual dimorphism, reproductive strategies and mating systems. Although sexual selection was initially thought to occur exclusively at the pre-copulatory stage (e.g., contests among males, and female mate choice), it can also continue after copulation through sperm competition and/or cryptic female choice. However, the study of these post-copulatory processes remains challenging because they occur internally and so are often difficult to observe. During my PhD project, I used the simultaneously hermaphroditic flatworm Macrostomum lignano to study sexual selection, with a special focus on distinguishing the processes occurring at the pre- and post-copulatory stage of sexual selection. Mating is not necessarily a harmonious union, instead partners are expected to allocate their mating resources strategically over different mating opportunities to maximise their own fitness. My results suggests that virgin pairs have a greater mating propensity, presumably because they want to obtain sperm to fertilise their own eggs and have more sperm ready to give away. Moreover, in several species sperm donors have been shown to transfer accessory gland secretions along with sperm, which can manipulate the partners to increase donor's fitness. I speculate that this may also be the case in M. lignano as sperm recipients behave differently after mating with virgins, which likely transfer more accessory gland secretions. Progress in understanding post-copulatory processes of sexual selection greatly depends upon the development of techniques that facilitate the observation of internal processes. The unique opportunity to track sperm under competitive conditions inside the female reproductive tract in vivo has become possible thanks to a transgenic line ubiquitously expressing green fluorescent protein (GFP): fluorescent sperm in a transparent worm. I tested and validated the reliability of the GFP-techniques in M. lignano, from which I could take advantage to reach novel findings. Although sexual selection is recognised be composed of pre- and post-copulatory episodes of selection, few studies provide a quantitative understanding of the relative importance of the different episodes of selection. My results suggest that in M. lignano a large part of the variance observed in male reproductive success arises from two post-copulatory episodes of selection, sperm-transfer efficiency and sperm-fertilising efficiency. Moreover, individuals with bigger testis gain higher paternity share, presumably because they transfer more sperm per copulation. These two findings disagree with the view that sexual selection mainly arises from differences in mating success. Instead, the results suggest that in this study system the post-copulatory episodes of selection are very important, and that the success of these episodes likely depends upon the sperm production rate. Simultaneous hermaphrodites need to decide how they allocate their resources towards their own male and female sex functions. A fundamental theory is that this trade-off depends on the number of mating partners (i.e., mating group size). In particular, sex allocation theory predicts that individuals should allocate more energy towards their female function in small mating groups. When the mating group size increases, the intensity of sperm competition increases and so individuals are expected to increase their investment towards their male function. This is fully supported by my results, which represents the most direct test of this basic theory to date. In conclusion, the simultaneous hermaphrodite Macrostomum lignano is a powerful model organism to study sexual selection and sex allocation. My studies took advantage of several of its features to provide novel insights in fundamental topics such as the operation of sexual selection along episodes of selection and sex allocation in simultaneous hermaphrodites. Overall, my PhD works suggest that the post-copulatory episodes of sexual selection may be important agents of selection.