Environmental Persistence Influences Infection Dynamics for a Butterfly Pathogen

Abstract

Many pathogens, including those infecting insects, are transmitted via dormant stages shed into the environment, where they must persist until encountering a susceptible host. Understanding how abiotic conditions influence environmental persistence and how these factors influence pathogen spread are crucial for predicting patterns of infection risk. Here, we explored the consequences of environmental transmission for infection dynamics of a debilitating protozoan parasite (Ophryocystis elektroscirrha) that infects monarch butterflies (Danaus plexippus). We first conducted an experiment to observe the persistence of protozoan spores exposed to natural conditions. Experimental results showed that, contrary to our expectations, pathogen doses maintained high infectivity even after 16 days in the environment, although pathogens did yield infections with lower parasite loads after environmental exposure. Because pathogen longevity exceeded the time span of our experiment, we developed a mechanistic model to better explore environmental persistence for this host-pathogen system. Model analysis showed that, in general, longer spore persistence led to higher infection prevalence and slightly smaller monarch population sizes. The model indicated that typical parasite doses shed onto milkweed plants must remain viable for a minimum of 3 weeks for prevalence to increase during the summer-breeding season, and for 11 weeks or longer to match levels of infection commonly reported from the wild, assuming moderate values for parasite shedding rate. Our findings showed that transmission stages of this butterfly pathogen are long-lived and indicated that this is a necessary condition for the protozoan to persist in local monarch populations. This study provides a modeling framework for future work examining the dynamics of an ecologically important pathogen in an iconic insect.

Transitions in symbiosis: evidence for environmental acquisition & social transmission within a clade of heritable symbionts

“…Shedding and accumulation of the bacterium in the foraging environment (e.g. on flowers) may generate increased infection risk as the foraging season proceeds, as observed for some parasite species [85]. However this would be contingent on the survival of Arsenophonus in the environment, a trait conventionally considered absent from this class of insect symbionts, despite relatively large symbiont genomes and cell free cultivability found within the clade [86,87].…”

Infections on the move: how transient phases of host movement influence disease spread

“…In addition, field and experimental data on the abundance and persistence of parasite infective stages and/or infection vectors in the habitat matrix can inform parameterization of rates of environmental transmission in transient hosts. Theoretical work has begun to use these types of data to explore infection dynamics in single locations [ 68 ], and our framework can guide spatially explicit extensions of these models that distinguish environmental transmission rates at each phase of host movement. Finally, human alteration of habitats comprising host networks, while posing various potentially detrimental consequences for population viability, may afford natural experiments for testing the abiotic factors involved in transience phase infection dynamics.…”

Fine-scale spatial patterns of wildlife disease are common and understudied

“…Because the range of spatial variation in infection depends on environmental gradients across the host population, traits of hosts and parasites are also likely to determine the contexts under which spatial dependence will occur. For example, parasites that persist for longer in the environment are likely to experience stronger influences of environmental gradients than directly transmitted counterparts (Satterfield et al 2017). Similarly, large, mobile species, such as large carnivores or nomadic bats, may more efficiently disseminate pathogens through the environment, reducing their spatial autocorrelation (Peel et al 2013;Gilbertson et al 2016).…”