US-UKEEIDCollab:Understanding the effects of spatial structure on evolution of virulence in the real world: honeybees and their destructive parasites

Individuals tend to interact more with individuals that are close to them or within their family or social groups. It follows therefore that in diseases that are spread by contact, infected individuals are more likely to contact other individuals that are close by or within certain social groups with whom they interact more. The disease therefore spreads spatially through the populations. There has been a number of computer models that show that this spatial spread can have a major effect on the disease dynamics, but our work has shown that this spatial structure can have important implications to the evolution of parasites. In particular if they tend to spread locally, they are selected for lower transmission and virulence.

But how do we test this kind of theory? One way is experimentally where we artificially manipulate the range of transmission and examine the impact on the evolution of the parasite. We have previously developed an insect virus system in which we can manipulate how locally the hosts move. and our recent work using this system has confirmed the predictions of the theory; virulence was lower in the more viscose population. This is a good experimental test of the theory, but we now propose to see whether this theory is relevant in an important real world disease system. We propose to examine the role of structure created by different rearing practices in the honeybee on the virulence of their parasite, the varroa mite.

Honey bees are under threat from a wide range of parasites of which the varroa mite is one of the most important. We will manipulate transmission of the mite in a replicated experimental design. The transmission will range from local between nearest colonies to global over large differences. With this manipulation we will see whether local transmission does indeed allow less virulent mites to persist. We will develop new theory that is tailored to the honey bee system and examines how different bee rearing practices are predicted to impact on the virulence of the parasites.

In addition we will develop new theory on how variation in susceptibility within host populations impacts on parasite virulence and test the predictions of the theory within the established honey bee system. The overall aim is to gain a better understanding of how to virulence evolves in order to improve the management of disease with a particular focus on a major disease of honey bees.

Understanding the factors that select for parasite virulence has great relevance to managing disease risks of humans and agricultural animals alike. Evolutionary theory has shown that spatial structure is crucially important in driving virulence evolution: when hosts are more likely to transmit disease to close neighbors only (i.e. local transmission), parasites are expected to evolve lower virulence than when hosts are equally likely to infect nearest neighbors and far-away individuals (i.e. global transmission). This theory has been confirmed in a few laboratory systems, but remains untested in a real-life system in the field.

This proposal will use honeybees (Apis mellifera) and their destructive parasitic mites (Varroa destructor) to study the role of increased population mixing and global transmission on virulence evolution. This system is particularly well suited for this question, because human-managed and wild bees vary widely in the importance of local and global mite transmission. Moreover, standard beekeeping practices routinely increase global parasite transmission and thus have the potential to unintentionally select for devastating parasites. In addition to experimentally testing the importance of spatial structure on virulence evolution, this proposal will also develop and test theory on the effects of heterogeneity in host susceptibility. This is again highly relevant in the honeybee-Varroa system, where beekeepers routinely split bee colonies to mitigate the ongoing colony losses due to mite infestations.

The deliverables most anticipated from this proposal are new recommendations on practices that beekeepers may adopt to minimize parasite transmission between colonies or apiaries. Delaplane's directorship of the Managed Pollinator Coordinated Agricultural Project (CAP) will greatly facilitate this through the dissemination of results and recommendations through local, regional, and national client meetings, and through inclusion in the Best Management Practices guide being developed by this coordinated project. The proposal will also integrate research with education in several ways. Postdocs as well as students of multiple levels (undergraduate and graduate) and from diverse backgrounds will participate in the design, execution and presentation of this work. The researchers will also host high school teachers to develop research projects for use in their classes. Finally, the proposal will enhance scientific collaborations between institutions in the US and the UK, and will provide students and postdocs with complementary training in experimentation, modeling, and outreach to the community.