Infectious diseases in natural populations are important areas of research in ecology and evolution as they describe how parasites influence the host fitness. A host may undergo adaptive evolution against the parasite by acquiring either resistance or tolerance through developing intricate biochemical and molecular defence strategies. However, the knowledge about the genes associated with these traits remains limited. Furthermore, the strength of ongoing natural selection on transcript abundance has not been studied directly, despite the fact that gene regulation has a major role in adaptive evolution. In this thesis, I applied genomic and transcriptomic approaches to study the host parasite system of anadromous brown trout (Salmo trutta) infected with a myxozoan parasite, Tetracapsuloides bryosalmonae. In salmonids, T. bryosalmonae causes an emerging temperature-dependent disease, proliferative kidney disease (PKD). The parasite infects the kidney and spleen of juvenile fish, and at elevated temperatures, causes strong inflammatory response, anaemia and kidney hypertrophy.

In this thesis, I performed one of the first association mapping attempts on parasite resistance and tolerance in brown trout and demonstrated the possibilities as well as limitations of association analysis in natural populations. As there was very limited genomic information available for T. bryosalmonae, I also generated an annotated assembly of the parasite transcriptome. Furthermore, by combining -omic approaches with genetic mark-recapture and classical regression-based selection analysis, I demonstrated the effect of temperature-driven parasite-induced contemporary natural selection on transcript abundance and co-regulated gene networks in this wild vertebrate species.

I identified several promising candidate genes involved in PKD resistance and severity in brown trout. I also characterized more than three thousand transcripts of T. bryosalmonae. Among these, I also identified four novel protein drug targets, which can help in curing the infected fish. I also showed that the myxozoan parasite induces massive cell proliferation in the fish host whose variation is associated with the survival selection on the co-regulated gene networks. The directional selection on the individual transcript abundances was weak, similar to the published selection estimates on phenotypic traits. Finally, I also discovered many transcripts exhibiting widespread signal of disruptive selection, related to host immune defence, host–pathogen interactions, cellular repair and maintenance.

Overall, my thesis showcases the power of integrating ecological and genomic perspectives to gain novel insights into the functional genomic basis of resistance against a parasite, health damage (i.e., anaemia) caused by the parasite and the ongoing associated natural selection in the wild. Altogether, my thesis combines multiple levels of biological complexities and represents a significant step forward towards understanding the molecular basis of T. bryosalmonae and PKD.