Ecology and Evolution of Invasive Pacific Oysters in Response to Pathogen Infection and Rising Temperatures
Nature is a highly complex system that is subject to competition from several factors, which can be of physical, chemical, biotic but also anthropogenic origin. Nevertheless, we commonly consider only a few of those factors in our experiments. However, to understand the bigger picture, we have to test the synchronous effects of multiple factors. One great opportunity to do so comes from the direct interplay between bioinvasions and climate change. Bioinvasions constitute a natural experiment in evolution: when invasive species colonize new habitats they experience strong selection pressures from novel abiotic and biotic stressors. For a successful invasion, adaptation to those stressors is essential for survival. Additional threats may result from current climate change scenarios that further challenge the adaptive potential of invaders. Major threats of global change, such as emerging diseases are caused directly and indirectly by rising temperatures. A combined approach addressing direct effects of global change on host-parasite interactions of invasive species has rarely been taken. However, there is growing evidence that such multiple factors interact in complex ways. Furthermore, the way invasive species cope with novel parasites is still a black box. Using invasive Pacific oysters Crassostrea gigas and their opportunistic pathogens of the genus Vibrio as model organisms, this thesis addresses the evolution of an invasive species to novel sympatric parasites and combines this with additional challenges imposed by rising temperatures that are expected to occur in the habitat. C. gigas independently invaded and successfully colonized the Southern and the Northern area of the European Wadden Sea. The successful invasion of C. gigas‘ is mainly attributed to a lack of natural enemies and high propagule pressure. While Southern populations have occasionally been subjected to extensive mortalities resulting from a complex interaction of high temperatures, oyster genetics and parasite infections, Northern populations have been spared from this fate so far. Those differences in invasion and disease selection history were the starting point of my thesis. Based on a set of controlled infection experiments at contemporary and future water temperatures, I demonstrated that invasive oysters have the potential to adapt rapidly to novel sympatric Vibrio spp. (Chapter III). By using lab-bred hybrids of the two invasion waves, I determined that the rapid adaptation is facilitated by dominant inheritance of disease resistance alleles. This adds a further factor, apart from lack of natural enemies and high propagule pressure in explaining C. gigas‘ enormous invasion success: rapid adaptation to enemy shifts. This adaptation to sympatric pathogens could only be observed at high temperatures (21°C in contrast to 17°C). Indeed, I could show that Vibrio infection and temperature add additively to disease outbreaks in adults (Chapter I). At high temperatures adult oysters have a reduced ability to clear out infectious strains efficiently (Chapter I), while simultaneously the likelihood of encountering pathogenic strains from the surrounding environment correlates positively with temperature (Chapter II). However, in contrast to adults, susceptibility to disease of larvae was reduced at high temperatures, i.e. 23°C in contrast to 19°C (Chapter IV). I assume, that nowadays, selection is less pronounced on adults when average water temperatures remain below 20°C. However, if average summer temperatures will rise as predicted by global change scenarios, selection pressure on adult oysters will increase while simultaneously decrease on larvae by favoring successful recruitment and disease resistance (Chapter IV). Such opposing temperature-mediated effects between life-stages will play a major role in determining this species‘ persistence in the invaded area in the face of global warming. In summary, by studying the evolution of an invasive species to novel parasites in the context of climate change I unveiled another facet explaining the outstanding success of C. gigas‘ invasion in the European Wadden sea: rapid adaptation to enemy shift. In concert with this finding, I suggest, that in the context of rising temperatures, the persistence of C. gigas underlies on the one hand the opposite response of temperature-mediated infection outcome between larvae and adults, and on the other hand the equilibrium between the rate of rising temperatures and the rate at which the populations will be able to catch up.