NSFDEB-NERC: The eco-evolutionary dynamics of age-specific resistance to infectious disease

When a disease epidemic sweeps through a population of plants, animals, or humans, the youngest individuals in the population are often hardest hit. This is because juveniles are typically more susceptible to infectious disease than adults. Indeed, the spread of many human diseases such as measles and chicken pox is largely driven by children. Likewise in many wildlife species, the spring 'pulse' of new highly susceptible young can drive epidemics, including diseases that risk spilling over into human or livestock populations. However, while the importance of juvenile susceptible to disease control has long been recognised, we lack a basic understanding of why juveniles are inherently so susceptible, even after accounting for prior exposure to disease. This research will use mathematical models and experiments with a model plant system to investigate the fundamental ecological and evolutionary processes driving the evolution of age-specific susceptibility. The results will substantially increase our understanding of the feedbacks between resistance evolution and disease spread, which will improve management strategies for wildlife disease, and inform crop breeding for disease resistance. The research will also increase public understanding of science and enrich local biodiversity records and museum collections through new citizen science outreach activities that are integrated with the basic research.

The question of why juveniles are so susceptible is puzzling from an evolutionary perspective because infection prior to reproduction would seem to have a much greater negative impact on a host than infection later in life (after the host has had a chance to reproduce). Natural selection should therefore favour individuals that are less susceptible to disease when they are young. This project will test the novel hypothesis that juvenile susceptibility is maintained by feedbacks between evolutionary change in host resistance and ecological change in disease abundance. These "eco-evolutionary" feedbacks occur because the evolution of disease resistance at any age in the host population can in turn reduce the intensity of disease epidemics. Critically, lower disease-levels make it less likely that a host will encounter disease as a juvenile, thereby allowing the maintenance of juvenile susceptibility. The researchers will build on this novel eco-evolutionary framework to develop a predictive mathematical theory for understanding key host and pathogen traits, and the feedbacks driving the evolution of age-specific disease susceptibility. Then to establish how these age-specific selection pressures are instantiated in a real-world system and to test key predictions from the model, the research team will utilise the model plant-disease system, anther-smut disease (Microbotryum) on white campion (Silene latifolia) to quantify the fitness costs, benefits, and evolutionary potential of age-specific resistance under a range of disease frequencies. To increase the broader impacts and societal benefits of the proposed work they will engage local natural history societies in original scientific research on the distribution and diversity of 'micro-fungi', and provide meaningful research opportunities for undergraduates.

The project will achieve impact for three primary beneficiaries: (i) the academic community, (ii) agricultural industry, and (iii) the general public.

(i) Academic community
This interdisciplinary project will be of interest to academics from a broad range of disciplines, including evolutionary biology, disease ecology, mathematical biology, and plant biology. By integrating theory and experiment to study the eco-evolutionary dynamics of age-specific resistance, our project has the potential to provide important new insights into disease biology and evolutionary biology, in particular. We will disseminate our research to the scientific community through publication in high impact peer-reviewed journals and through presentations at international conferences. The project will also contribute to the next generation of scientists through the mentoring of post-doctoral researchers, and undergraduate students who will be active participants in the research process, and will benefit from the international collaboration through two joint project meetings. These meetings will each include a seminar and workshop targeted to upper-level undergraduates and 1st year graduate students given by the visiting PI.

(ii) Agricultural industry
A greater understanding of the genetic and numeric feedbacks driving the evolution of age-specific disease resistance will help advance practices in agriculture by informing age-specific harvesting and plant breeding strategies in ways that maximise selection for naturally occurring genetic variants. The theoretical component of our research will provide general insights into the evolution of age-specific resistance and the experiments will provide explicit tests of the theory in a tractable model plant-fungi system. Given that the experiments will take place in the context of plants and plant-pathogens, they will be of particular relevance to agricultural crops.

(iii) General Public
The project will increase public understanding of science and enrich local biodiversity records and museum collections through new citizen science outreach activities. We will engage with the Master Naturalist program at UMD Extension, the Mycological Association of Washington DC, the Maryland Native Plant Society, and the Bath Natural History Society to provide education and to record locations and abundance of anther-smut fungi and catalog biodiversity of other smuts and plant-associated 'micro- fungi'. Materials developed for the workshops will reach a broad cross-institutional audience through dissemination on web-based platforms including the teaching disease ecology website (run by Project Partner Dr Emily Bruns) and the disease section of the ESA website.