How does parasite environmental transmission stage concentration change before, during, and after disease outbreaks?

Abstract

Outbreaks of environmentally transmitted parasites require that susceptible hosts encounter transmission stages in the environment and become infected, but we also know that transmission stages can be in the environment without triggering disease outbreaks. One challenge in understanding the relationship between environmental transmission stages and disease outbreaks is that the distribution and abundance of transmission stages outside of their hosts have been difficult to quantify. Thus, we have limited data about how changes in transmission stage abundance influence disease dynamics; moreover, we do not know whether the relationship between transmission stages and outbreaks differs among parasite species. We used digital PCR to quantify the environmental transmission stages of five parasites in six lakes in southeastern Michigan every 2 weeks from June to November 2021. At the same time, we quantified infection prevalence in hosts and host density. Our study focused on eight zooplankton host species (Daphnia spp. and Ceriodaphnia dubia) and five of their parasites from diverse taxonomic groups (bacteria, yeast, microsporidia, and oomycete) with different infection mechanisms. We found that parasite transmission stage concentration increased prior to disease outbreaks for all parasites. However, parasites differed significantly in the relative timing of peaks in transmission stage concentration and infection outbreaks. The “continuous shedder” parasites had transmission stage peaks at the same time as or slightly after the outbreak peaks. In contrast, parasites relying on host death for transmission (“obligate killers”) had transmission stage peaks before outbreak peaks. For most parasites, lakes with outbreaks had higher spore concentrations than those without outbreaks, especially once an outbreak began; the exception was for a parasite, Pasteuria ramosa, with very strong genotypic specificity of infection. Overall, our results show that disease outbreaks are tightly linked to transmission stage concentration; outbreaks were preceded by increases in transmission stage concentration in the environment and then were fueled by the production of more transmission stages during the outbreak itself, with concentrations decreasing to pre-outbreak levels as outbreaks waned. Thus, tracking transmission stages in the environment improves our understanding of the drivers of disease outbreaks and reveals how parasite traits may affect these dynamics.