Looking-glass parasites: Evolution and ecology of the Red Queen’s parasite, Atriophallophorus winterbourni (Blasco-Costa et al., 2019)

Abstract

Host-parasite interactions are an attractive subject for research on evolution, ecology and behaviour. Classic model systems of infectious disease dynamics, epidemiology and host population regulation by parasites present a diversity of examples where fundamental concepts are tested. The interaction between the New Zealand Mud Snail Potamopyrgus antipodarum (Gray, 1843) and its trematode parasite Atriophallophorus winterbourni Blasco-Costa et al., 2019 is a good example. The system has become a model for research on the maintenance of sexual reproduction in natural populations. The core of earlier research on the system is focused on the co-evolutionary interaction between the host and its parasite in natural populations. This thesis features research on the epidemiological and ecological factors that underlie these co-evolutionary dynamics between the snail and the trematode. I expand the understanding of the key players in this interaction by presenting a comprehensive, large-scale study on the phylogeography of A. winterbourni in New Zealand. This study reveals that the parasite, which was thought to be one species, in fact consists of a complex of cryptic species. These species have overlapping distributions, while showing a strong intraspecific phylogeographic structure. At the local scale, within Lake Alexandrina in New Zealand, I provide experimental evidence for behavioural manipulation by the parasite. The parasite induces migration of its snail host toward the shallow-water margin, a form of behavioural manipulation that is likely to facilitate transmission to dabbling ducks. I then show how this manipulation conceals the relationship between risk of infection and prevalence of infected hosts. Risk of exposure is key factor for understanding epidemiology and evolution of host resistance. Spatial de-coupling of risk of exposure and prevalence of infection by host manipulation therefore presents a problem for assessment of spatial structure in selection for host resistance. I therefore tested if the frequency of multiple-genotype infections within single hosts can be used to identify areas with increased risk of exposure, instead of prevalence of infection. I show that the frequency of multiple-genotype infections resolves small-scale patterns in risk of exposure. Therefore, multiple genotype-infections can function as an indicator for risk of exposure and may have applications in evolutionary or epidemiological research and disease management. Finally, I examined the mating system of A. winterbourni. Clonal replication within the snail host leads to co-transmission of numerous, clonally identical, hermaphrodite parasite individuals to the same bird host. My results suggest that this opportunity for inbreeding in infrapopulations does not lead to inbred populations. Together, the chapters in this thesis contribute to the research on the fascinating interaction between P. antipodarum and A. winterbourni, while simultaneously addressing a diverse set of questions on behavioural manipulation, epidemiology, phylogeography and mating system evolution.