Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

Abstract

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.

Keywords

• competitor versus colonizer
• diversifying selection
• dose–density response, Daphnia magna
• evolution of disease
• epidemiology
• Pasteuria ramosa