Abstract

Repeated extinction and recolonization events generate a landscape of host populations that vary in their time since colonization. Within this dynamic landscape, pathogens that excel at invading recently colonized host populations are not necessarily those that perform best in host populations at or near their carrying capacity, potentially giving rise to divergent selection for pathogen traits that mediate the invasion process. Rarely, however, has this contention been empirically tested. Using Daphnia magna, we explored how differences in the colonization history of a host population influence the invasion success of different genotypes of the pathogen Pasteuria ramosa. By partitioning the pathogen invasion process into a series of individual steps, we show that each pathogen optimizes invasion differently when encountering host populations that vary in their time since colonization. All pathogen genotypes were more likely to establish successfully in recently colonized host populations, but the production of transmission spores was typically maximized in either the subsequent growth or stationary phase of host colonization. Integrating across the first three pathogen invasion steps (initial establishment, proliferation, and secondary infection) revealed that overall pathogen invasion success (and its variance) was, nonetheless, highest in recently colonized host populations. However, only pathogens that were slow to kill their host were able to maximize host‐facilitated dispersal. This suggests that only a subset of pathogen genotypes—the less virulent and more dispersive—are more likely to encounter newly colonized host populations at the front of a range expansion or in metapopulations with high extinction rates. Our results suggest a fundamental trade‐off for a pathogen between dispersal and virulence, and evidence for higher invasion success in younger host populations, a finding with clear implications for pathogen evolution in spatiotemporally dynamic settings.

Highlights

  • Infectious disease is a major threat to human and wildlife well-being, and it is well recognized that pathogens have the ability to evolve over time to persist in a host population

  • Using the waterflea Daphnia magna and its associated bacterial pathogen Pasteuria ramosa, we experimentally tested the idea that different pathogen strategies may be favored whenever pathogens encounter host populations that vary in their time since colonization

  • Our work demonstrates that pathogen invasion success and spatial spread is strongly linked to the host population dynamics encountered

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Summary

Introduction

Infectious disease is a major threat to human and wildlife well-being, and it is well recognized that pathogens have the ability to evolve over time to persist in a host population. Strategies may be favored at different times of the host colonization process, is essential for understanding the evolution of pathogens in nature. Our results suggest that prudent and highly dispersive pathogens are more likely to encounter (or keep pace with) newly colonized host populations at the range front of an expanding host population or in metapopulations. Our work demonstrates that pathogen invasion success and spatial spread is strongly linked to the host population dynamics encountered. This empirical work reiterates the importance of developing a better understanding of how host population dynamics influences the evolution of infectious disease in spatially explicit settings

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