Light gradients are an inherent feature in aquatic ecosystems and play a key role in shaping the biology of phytoplankton. Parasitism by chytrid fungi is gaining increasing attention as a major control agent of phytoplankton due to its previously overlooked ubiquity, and profound ecological and evolutionary consequences. Despite this interest, if and how light conditions modulate phytoplankton chytridiomycosis remains poorly studied. We investigated life-history traits of a chytrid parasite, Rhizophydium megarrhizum, under different light intensities and spectral compositions when infecting two closely related planktonic cyanobacteria with different light-harvesting strategies: Planktothrix rubescens and P. agardhii. In general, parasite transmission was highest under light conditions (both intensity and quality) that maximized growth rates for uninfected cyanobacteria. Chytrid encystment on hosts was significantly affected by light intensity and host strain identity. This likely resulted from higher irradiances stimulating the increased discharge of photosynthetic by-products, which drive parasite chemotaxis, and from strain-specific differences at the cell-surface. Comparisons of parasite transmission and host growth rates under different light conditions suggest the potential for epidemic development at higher irradiances, whereas host and parasite could coexist without epidemic outbreaks at lower light levels. These results illustrate the close relationship between parasite transmission and host fitness, which is ultimately modulated by the external environment.

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.

Gene flow maintains the genetic integrity of species over large spatial scales, and dispersal maintains gene flow among separate populations. However, body size is a strong correlate of dispersal ability, with small-bodied organisms being poor dispersers. For parasites, small size may be compensated by using their hosts for indirect dispersal. In trematodes, some species use only aquatic hosts to complete their life cycle, whereas others use birds or mammals as final hosts, allowing dispersal among separate aquatic habitats. We performed the first test of the universality of the type of life cycle as a driver of parasite dispersal, using a meta-analysis of 16 studies of population genetic structure in 16 trematode species. After accounting for the geographic scale of a study, the number of populations sampled, and the genetic marker used, we found the type of life cycle to be the best predictor of genetic structure (Fst): trematode species bound to complete their life cycle within water showed significantly more pronounced genetic structuring than those leaving water through a bird or mammal host. This finding highlights the dependence of parasites on host traits for their dispersal, suggesting that genetic differentiation of parasites reflects the mobility of their hosts.