Host adaptation to novel pathogen introduction: Predicting conditions that promote evolutionary rescue.

Novel pathogen introduction can have drastic consequences for naive host populations, and outcomes can be difficult to predict. Evolutionary rescue (ER) provides a foundation for understanding whether hosts are driven to extinction or survive via adaptation. Currently, patterns of host population dynamics alongside evidence of adaptation are used to infer ER. However, the gap between established ER theory and complexity inherent in natural systems makes interpreting empirical patterns difficult because they can be confounded with ecological drivers of survival under current theory. To bridge this gap, we expand ER theory to include biological selective agents, such as pathogens. We find birth processes to be more important than previously theorised in determining ER potential. We employ a novel framework evaluating ER potential within natural systems and gain ability to identify system characteristics that make ER possible. Identifying these characteristics allows a shift from retrospective observation to a predictive mindset, and our findings suggest that ER occurrence may be more limited than previously thought. We use the plague system of Yersinia pestis infecting Cynomys ludovicianus (black-tailed prairie dogs) and Spermophilus beecheyi (California ground squirrels) as a case study.

Transmission shifts underlie variability in population responses to Yersinia pestis infection.

Host populations for the plague bacterium, Yersinia pestis, are highly variable in their response to plague ranging from near deterministic extinction (i.e., epizootic dynamics) to a low probability of extinction despite persistent infection (i.e., enzootic dynamics). Much of the work to understand this variability has focused on specific host characteristics, such as population size and resistance, and their role in determining plague dynamics. Here, however, we advance the idea that the relative importance of alternative transmission routes may vary causing shifts from epizootic to enzootic dynamics. We present a model that incorporates host and flea ecology with multiple transmission hypotheses to study how transmission shifts determine population responses to plague. Our results suggest enzootic persistence relies on infection of an off-host flea reservoir and epizootics rely on transiently maintained flea infection loads through repeated infectious feeds by fleas. In either case, early-phase transmission by fleas (i.e., transmission immediately following an infected blood meal) has been observed in laboratory studies, and we show that it is capable of driving plague dynamics at the population level. Sensitivity analysis of model parameters revealed that host characteristics (e.g., population size and resistance) vary in importance depending on transmission dynamics, suggesting that host ecology may scale differently through different transmission routes enabling prediction of population responses in a more robust way than using either host characteristics or transmission shifts alone.