My research focuses on two major themes:
(1) how ecological context (including physical and chemical features of the environment as well as the community of organisms living there) affects the risk of infection and consequences of disease for hosts, and
(2) how diseases impact not only host populations, but also the surrounding ecological community and ecosystem. I am particularly interested in trait-mediated indirect effects of parasites; i.e., trait changes in infected hosts that affect other species and/or ecosystem processes.
Fascinating complications to these research questions include:
(a) effects of disease on ecosystems may feedback to affect disease risk (Figure 1),
(b) hosts, parasites, and other species in the community may be evolving in response to each other (or other selection pressures) on ecological timescales (reviews on this topic: Penczykowski et al. 2011, Freshwater Biol; Penczykowski et al. 2016, Evol Appl), and
(c) human-driven changes in climate, land use, and biodiversity are altering the ecological context in which host–parasite interactions occur.
Figure 1. Schematic illustrating the potential for feedbacks between ecosystems and disease. Environmental and ecological context can shape host–parasite interactions. Parasite epidemics can in turn alter the structure and function of ecological communities and ecosystems.
Here, I describe some of my past and ongoing work (click the Publications tab to see additional projects in which I have been involved).
(1) Ecological context affects disease risk:
The likelihood of host–parasite contact and subsequent infection can depend strongly on physical, chemical, and ecological characteristics of the environment. My PhD research explored mechanisms by which abiotic and biotic components of lake environments modulate disease risk for Daphnia hosts (Figure 2). I found that decreasing the quality of algal resources available to hosts – a change often triggered by excess nutrients in lakes – can lower transmission potential of a fungal parasite by altering key host traits (Penczykowski et al. 2014, Funct Ecol). Specifically, poor quality cyanobacterial food stunted host growth and decreased their size-corrected feeding rate (i.e., hosts were small and also fed slowly for their size). Because hosts get infected with the focal parasite by non-selectively ingesting fungal spores along with their food, the reduced foraging rate of hosts on the poor quality diet protected them from infection. These hosts also supported less within-host parasite growth. By contrast, hosts reared on high quality green algae grew larger, had higher infection risk, and fuelled more parasite growth. This study highlights that hosts in good overall condition are not more robust against disease if they are more likely to encounter pathogens or provide better resources for pathogen growth. I also performed a field experiment which revealed that nutrient enrichment and decreased habitat structure (i.e., increased water column mixing) can interact to promote disease prevalence (Penczykowski et al. in prep). At a larger spatial scale, I linked physical properties of 18 lakes to the size of their epidemics via direct connections with pathogen viability and indirect pathways involving ecological drivers of disease (Penczykowski et al. 2014, Limnol Oceanogr). Together, these studies indicate that predicting the spread of disease requires understanding the direct and indirect mechanisms by which environments influence host–parasite interactions.
Figure 2. Female Daphnia dentifera from lakes in the midwestern USA. (A) This host is heavily infected with the virulent fungus Metschnikowia bicuspidata. She appears opaque because tens of thousands of needle-shaped parasite spores fill her body cavity. (B) This uninfected host has embryos in her brood pouch (arrow) and green algae in her gut.
As a post-doctoral researcher, I investigated how the physical environment and genetic structure of host and parasite populations determine disease risk among and within plant populations (Figure 3). In a 13-year time series of data from a network of over 4000 Plantago lanceolata populations, I found that prevalence of powdery mildew infection was greater following winters in which pathogen resting structures were less exposed to freezing temperatures. Collaboration with spatial statisticians in the Biostatistics and Spatial Processes group at INRA (Avignon, France) yielded a theoretical model showing that mild climatic conditions during the winter off-season can drive spatial synchrony of pathogen persistence across the metapopulation, consistent with patterns observed in nature (Penczykowski et al. 2015, New Phytol). Within Plantago populations, powdery mildew infections are considerably aggregated (Penczykowski & Laine, unpubl. data). In the summer of 2014, I performed a field experiment to tease apart how variation in host/pathogen genotypes and environmental characteristics contribute to spatial patterns of disease within populations (website: http://ParasitesInSpace.com). I then mentored a Master’s student in a lab experiment which helped disentangle effects of host genotype and host condition on these spatial patterns. These studies identify roles of environmental variation in determining disease risk at spatial scales ranging from a few meters to an entire metapopulation.
Figure 3. Leaves of the herbacious perennial Plantago lanceolata infected with the powdery mildew Podosphaera plantaginis. The pathogen persists as a dynamic metapopulation in a large network of meadows in the Åland archipelago of southwest Finland.
(2) Diseases affect populations, communities, and ecosystems:
By definition, pathogens harm their hosts. However, consequences of disease for wild populations remain poorly understood, and we know even less about the role of pathogens at the broader community and ecosystem level. In my research with Daphnia, I showed that infection reduces host feeding rate as well as survival. A dynamic epidemiological model revealed that depressed consumption during epidemics can allow enough compensatory resource growth to fuel greater host density, and I found support for this mechanism in the field (Penczykowski et al., submitted). This counterintuitive result – that disease increased host density – could not be explained without knowing how infection alters host traits and accounting for indirect effects of disease on the host’s resources.
While there are infamous examples of pathogens devastating tree species or ravishing crops, other plant pathogens have much more subtle effects on population size. I am fascinated by the roles of these less dramatic diseases in populations, communities, and ecosystems. For example, across the Plantago metapopulation, I found a negative relationship between powdery mildew infection and annual growth rate of populations (Penczykowski et al. 2015, New Phytol). However, effects of disease on individual populations varied over space and time. In such a system, what are the consequences of disease for productivity or nutrient turnover? A major theme of my future research will be the role of parasites in food webs and ecosystem processes, including mechanisms involving parasite-driven changes in host growth, resource use, and nutrient stoichiometry.