Evolution and ecology of phenotypic plasticity in parasite life history strategies

The environments experienced by parasites inside hosts and vectors are highly changeable. For example, resources become scarce as hosts get sick, immune responses directed at parasites develop, and parasites often have to compete with other strains and species sharing their host. Given that parasites live in the bodies of others, with which they are engaged in a life-and-death struggle, knowledge about how parasites cope with the challenges of their lifestyle is remarkably shallow.

Understanding the strategies that parasites have evolved to cope with the challenging environments they face inside hosts and vectors is the aim of this proposal. Parasite strategies are important because they are determinants of how sick hosts get (virulence) and how infectious parasites are (transmission). In evolutionary ecology, plasticity in life-history traits is a well-known adaptation to life in variable environments. Adaptive plasticity enables organisms to change their phenotype in response to changes in their circumstances in ways that maintain fitness across environments. That the environment is complex and shapes phenotypes has been known for over a century but because parasites have been viewed as creatures with inflexible strategies, plasticity in their traits - and whether it is beneficial - has been overlooked.

Mounting evidence is revealing considerable plasticity in parasite traits that underpin the ability to survive during infections and to transmit to new hosts. Our recent research shows that parasites adjust their traits in response to the conditions (resource availability, competition with other strains, and anti-parasite drugs) they experience in the host. We know want to investigate why parasites do this by testing theory that predicts they adjust their traits in ways that maximise fitness. We will identify how much variation in parasite traits is explained by parasite strategies and complex interactions between hosts and parasites, whether plasticity benefits parasites, and whether plasticity has evolved to enable to parasites to cope with variable environmental conditions. Therefore, our project will reveal how sophisticated parasite strategies for survival and transmission really are, and reveal weaknesses that could be exploited for disease control.

Malaria (Plasmodium) parasites offer an excellent system to explain the ecological and evolutionary drivers of variation in traits that shape the virulence and transmission phenotypes of parasites. A key fitness-determining trait for malaria parasites is the trade-off between the allocation of resources to asexually replicating stages (required for within-host survival) and sexually reproducing stages (required for transmission), which is called "reproductive effort" in evolutionary biology. Our project will determine how host and parasite factors contribute to plasticity in reproductive effort, quantify the patterns generated across environmental gradients and parasite genetic backgrounds, test whether parasite strategies are adjusted in response to the environment in ways that benefit survival and transmission, and investigate whether plasticity is costly by testing if it is lost under selection in constant environmental conditions.

Explaining variation in the virulence and infectiousness of parasites is a major aim in evolutionary biology and predicting how parasites adapt to their environment is becoming increasingly important. For example, changes in parasite ecology (e.g. composition of host-parasite-vector communities, and habitats) are implicated in the emergence of new infectious diseases of wildlife, crops, livestock, and humans. For applied science, a better understanding of parasites is necessary because evolution continually erodes efforts to control diseases responsible for considerable mortality and morbidity.

In addition to the academic beneficiaries described above, our research will also benefit the following groups.

PUBLIC. We have strong track records in communicating with the media (for recent efforts see http://reece.bio.ed.ac.uk/media.html) and write press releases on our work. We will continue to seek these opportunities and contribute to local science festivals, public engagement events, and participate as experts in online discussions.

HIGH SCHOOL PUPILS. We will organize an event for sixth form Biology students to visit our lab, learn about and observe our research, and talk to lab members in an informal setting. The ambitions for this event also include an opportunity to communicate to students what evolutionary biology and ecology can bring to all biological disciplines.

POLICY MAKERS AND DRUG DEVELOPERS INVOLVED IN DISEASE CONTROL. Our project will use evolutionary theory to understand how parasites adapt to maximize in-host survival and between-host transmission. Whilst we focus on malaria parasites, the fitness components we study are general to all sexually reproducing organisms so our results will be relevant to a broad range of infectious disease researchers. The information we generate will ultimately inform the development of intervention strategies that interfere with transmission, including the potential for new types of drugs. Because members of these communities usually have a biomedical background, communicating the value of an evolutionary framework for disease control is a task for evolutionary ecologists. We will organise a workshop to communicate the short- and long-term implications of our project to relevant users and explore what directions for the development of our project would be most useful to users. We will use established contacts with policy makers, field and clinical parasitologists, and biomedical researchers to form the participants list. In our experience these groups are curious about what an evolutionary framework can offer to disease control, but clear links between experimental data and pathogenicity or epidemiology are required to turn passing curiosity into sufficient interest to engage in knowledge transfer. We will also use this workshop to form collaborations to test our key results in natural populations and to improve procedures to monitor markers for parasite evolution in natural populations.

The benefits of our research to the above groups will also be facilitated by developing a website with an area dedicated to the provision of information targeted to professional users and a parallel area to communicate to the media and public by outlining the rationale and objectives of the project and lay translations of all resulting papers.