Understanding how individual parasite traits contribute to overall fitness, and how they are modulated by both external and host environment, is crucial for predicting disease outcome. Fungal (chytrid) parasites of phytoplankton are important yet poorly studied pathogens with the potential to modulate the abundance and composition of phytoplankton communities and to drive their evolution. Here, we studied life-history traits of a chytrid parasite infecting the planktonic, bloom-forming cyanobacterium Planktothrix spp. under host genotype and thermal variation. When expressing parasite fitness in terms of transmission success, disease outcome was largely modulated by temperature alone. Yet, a closer examination of individual parasite traits linked to different infection phases, such as (i) the establishment of the infection (i.e. intensity of infection) and (ii) the exploitation of host resources (i.e. size of reproductive structures and propagules), revealed differential host genotype and temperature × host genotype modulation, respectively. This illustrates how parasite fitness results from the interplay of individual parasite traits that are differentially controlled by host and external environment, and stresses the importance of combining multiple traits to gain insights into underlying infection mechanisms.

Experimental evolution can be used to test for and characterize parasite and pathogen adaptation. We undertook a serial-passage experiment in which a single parasite population of the obligate fungal (chytrid) parasite Rhizophydium megarrhizum was maintained over a period of 200 days under different mono- and multiclonal compositions of its phytoplankton host, the bloom-forming cyanobacterium Planktothrix. Despite initially inferior performance, parasite populations under sustained exposure to novel monoclonal hosts experienced rapid fitness increases evidenced by increased transmission rates. This demonstrates rapid adaptation of chytrids to novel hosts and highlights their high evolutionary potential. In contrast, increased fitness was not detected in parasites exposed to multiclonal host mixtures, indicating that cyanobacterial intraspecific diversity hampers parasites adaptation. Significant increases in intensity of infection were observed in monoclonal and multiclonal treatments, suggesting high evolvability of traits involved in parasite attachment onto hosts (i.e., encystment). A comparison of the performance of evolved and unevolved (control) parasite populations against their common ancestral host did not reveal parasite attenuation. Our results exemplify the ability of chytrid parasites to adapt rapidly to new hosts, while providing experimental evidence that genetic diversity in host populations grants increased resistance to disease by hindering parasite adaptation.