Host-parasite coadaptation in a warming world

Global changes are escalating the frequency and severity of heating events and disease outbreaks. The extent to which thermal stress and infection may impact species evolution and persistence is however unclear. By causing stress and disrupting homeostasis, parasite infection may disrupt a host's ability to cope with extreme environments. A key challenge for environmental science is to understand the interaction between these dual threats in enough detail to predict how species will respond in the future. Accounting for the impact of both temperature stress and infection in animals is therefore vital for managing natural systems over policy-relevant timescales.

This project will tackle this problem in a microscopic Caenorhabditis nematode-microbial parasite interaction. These are members of animal and plant microbiota found globally, but originally isolated together on rotting banana stems. Given their short generation times and the fitness consequences of their interaction, these species have the potential to coevolve rapidly over weeks and in response to extreme temperatures, in the lab and in their natural habitat. The typical speed of coevolution in wild host-parasite communities during warming remains largely unknown, however, due to challenges in tracking coevolution in natural systems.

We will take advantage of natural collections, sequencing, selection experiments, and the tractable power of the model C. elegans, to document patterns and potential processes of host-parasite coevolution across warming scenarios. We have previously developed experimental evolution for this system in the laboratory and its diversity in the field has been assayed by others. Here, we will integrate these approaches and quantify coevolutionary dynamics and its impact on host thermal performance.

Firstly, we will co-isolating nematodes and parasites across banana plantations in Cape Verde and Canary Islands. We will quantify host and parasite thermal performances. We will examine whether there is divergence across altitudes in thermal performance during infection - currently unknown in wild infectious disease systems. This work will shed light on the importance of host-parasite interactions on a species' ability to survive thermal stress across its global distribution.

Secondly, we will co-passage nematode and parasite populations in an evolution experiment in which warming regimes will be manipulated. Tests for co-adaptation will determine whether hosts and parasite coevolved locally within patches, followed by an assessment of a host's thermal limits and parasite virulence in co-adapted pairs. Further, sequencing will determine whether hosts have diverged in genetic composition and gene expression across warming regimes.

Lastly, we will characterise the tempo of coevolution by tracking changes over time in host resistance and parasite infectivity. We will use performance assays and genomices to test whether warming can break down or accelerate coevolutionary interactions, with heat waves favouring disproportionately faster parasite adaptation but gradual warming giving hosts time to 'catch up' in the coevolutionary race. This work will yield a new way to establish coevolutionary rate and stability in the face of extreme environments - usable in other microbial and infectious disease systems.