Interactions among symbionts operate across scales to influence parasite epidemics

Abstract

Parasite epidemics may be influenced by interactions among symbionts, which can depend on past events at multiple spatial scales. Within host individuals, interactions can depend on the sequence in which symbionts infect a host, generating priority effects. Across host individuals, interactions can depend on parasite phenology. To test the roles of parasite interactions and phenology in epidemics, we embedded multiple cohorts of sentinel plants, grown from seeds with and without a vertically transmitted symbiont, into a wild host population, and tracked foliar infections caused by three common fungal parasites. Within hosts, parasite growth was influenced by coinfections, but coinfections were often prevented by priority effects among symbionts. Across hosts, parasite phenology altered host susceptibility to secondary infections, symbiont interactions and ultimately the magnitude of parasite epidemics. Together, these results indicate that parasite phenology can influence parasite epidemics by altering the sequence of infection and interactions among symbionts within host individuals.

Priority effects within coinfected hosts can drive unexpected population‐scale patterns of parasite prevalence

“…For within‐host priority effects to arise, some component of parasite fitness (host mortality, parasite clearance, or transmission rate) must depend on infection order. Most empirical studies on within‐host priority effects measure parasite transmission (Levin , Lohr et al 2010, Hall and Little , Marchetto and Power , Rynkiewicz et al ), though some measure effects on host mortality (Lohr et al 2010, Marchetto and Power ) or parasite clearance (Sandoval‐Aguilar et al ). Because it was the most common focus of the empirical studies, we chose to implement within‐host priority effects by making parasite transmission, specifically the production of infectious propagules, depend on parasite arrival order.…”

“…Priority effects may occur through niche preemption, where early arriving species deplete resources available to later‐arriving species, thus limiting their population growth (Urban and De Meester , Hernandez and Chalcraft , Rasmussen et al 2014, Fukami ). For niche preemption to occur within hosts, coinfecting parasites must compete for limiting resources such as nutrients (Wale et al ) or space (Dobson and Barnes ). Priority effects may also occur via niche modification, where the first species to arrive in a patch alters available niches, thus increasing or decreasing the fitness of later arriving species (Scheffer et al , Petraitis et al , Fukami and Nakajima ).…”

Cross‐scale dynamics in community and disease ecology: relative timescales shape the community ecology of pathogens

“…, Halliday et al. ). By analogy, dispersal of free‐living species can also depend on their frequency across a landscape (Smith et al.…”

“…, Halliday et al. ). Together, this information could suggest, at least phenomenologically, the relative pace of dynamics within vs. among hosts.…”

“…Plant pathogens inhibit one another's growth but co‐infections remain common (Hood , Halliday et al. ). Clearly, competitive exclusion is frequently interrupted by dispersal, disturbance, transmission, or host death.…”