Diversity of avian haemosporidian parasites : Host specificity, genetic structure and infection patterns

Sammanfattning: Parasites live on or inside their hosts and usually cause fitness loss, sometimes even lead to outbreaks of emerging infectious disease. Understanding how a parasite can infect its hosts (i.e., host specificity of the parasite) is important to both basic studies on disease evolution and the whole ecosystem health.In this thesis, I use avian haemosporidians, a group of species-rich protozoans as a model system to study host specificity of parasites, because of their high diversity in geographical distributions and host ranges.Studying host specificity of avian haemosporidians is facing two main challenges. First, it is essential to have a method that accurately defines the species limits of the parasites, which cannot be done by current identification methods. In some cases, a presumed generalist parasite that appears to infect multiple host species may have already adapted separately to different hosts, with the consequences that gene flow is restricted between them, and thus should be considered as reproductively isolated parasite species. In order to detect these cryptic species, reliable molecular markers are required. But genomic sequencing of avian haemosporidians is challenging since they coexist with hosts whose genome size is 50 times larger, causing an excessive amount of contamination in the yielded sequences. Second, the measurement of host specificity is in itself a complicated exercise. To assess host specificity of a parasite, one must consider the parasite’s ability to infect its host and reproduce in the host. The associations between a parasite and its hosts may vary with biotic and abiotic environmental factors, therefore the overall infection patterns of all potential hosts should be analysed, which was not reported in previous haemosporidian studies.In this thesis, my aim is to answer these two open questions for better understanding host specificity with a set of case studies. In Paper I a cost-effective protocol was developed to obtain multiple nuclear gene sequences throughout the genome of avian haemosporidians from DNA extracted from wild-infected bird blood without any special treatment. Based on analyses of multiple nuclear genes, the phylogenetic structures were investigated respectively for a group of sympatric parasites that present similar morphological characters in Paper II, and allopatric parasites with identical mitochondrial gene sequences in Paper III, to clarify if they should be considered as the same species or several different but cryptic species. I then tested the infection patterns of three generalist parasites in a natural community in Paper IV and found that generalist parasites are not equally adapted to all species in their host ranges but better to a smaller subset of hosts. In Paper V I further investigated the seasonal dynamics of parasite infection patterns and found that infections peaked during the main nesting season in adults and a few weeks later in juveniles, as soon as they started to be captured. Juveniles must become infected already as nestlings, thereafter the infection intensities decrease along the development of their immune systems.In summary, the findings in this study have provided new insights for further studies on host specificity of avian haemosporidians, with newly developed approaches to define the species limits and to investigate the infection patterns of parasites.