Periodic Reporting for period 1 - EpiEcoEvo (The role of temperature and transmission route on parasite epidemiological, ecological and evolutionary dynamics)
Okres sprawozdawczy: 2021-09-01 do 2023-08-31
Infectious diseases are of important concern to human health and species conservation, as exemplified by the rise of emerging zoonotic diseases globally over the past decades, and most starkly by the COVID-19 pandemic. The current climate and prediction of more emerging pandemics in the future, demonstrate that now, more than ever it is important to further our understanding of infectious disease epidemiology and transmission dynamics. The overall objective of this project was to disentangle the multifarious drivers of seasonal epidemics including temperature, host demography, transmission route and the broader ecological community through a combination of observational, experimental, and theoretical work using the Daphnia magna-Pasteuria ramosa model host-parasite system.
Daphnia magna, are small aquatic crustaceans that live throughout the northern hemisphere. They mainly reproduce clonaly, but produce sexual resting eggs when conditions are poor, which can hatch when conditions improve. Pasteuria is a common bacterial parasite of Daphnia, which causes 100 % mortality in in infected hosts, and removes their ability to reproduce. It also causes the host to turn bright red in colour, making it easy to differentiate infected from uninfected individuals. It is transmitted from environmental reservoirs in the sediment, when Daphnia pick up spores while filter feeding.
In the wild, seasonal epidemics of the parasite are observed in freshwater ponds. As temperature increases in the spring, Daphnia start to hatch from their resting eggs and their population increases in size. Other aquatic insects begin to hatch, including those that may prey on Daphnia. It has been hypothesized that these small predators may release parasite spores into the water when feeding on infected Daphnia (sloppy feeding) and contribute to transmission. A few weeks later, infections begin to be observed, and prevalence peaks around midsummer, usually reaching nearly 100 %. At the same time, the proportion of hosts in the population that are susceptible to many strains of the parasite declines, reaching nearly 0. The epidemic then declines and ends in the late summer.
Because all of these things are happening simultaneously, it is difficult to attribute these dynamics to any particular driver. The objective of this project was to investigate how these various factors (temperature, transmission from the spore bank, sloppy feeding in the free water and selection for host resistance) interact to influence the repeatable seasonal epidemic dynamics observed in nature in order to further understand the drivers of epidemics, by pairing observational and experimental work.
Daphnia magna, are small aquatic crustaceans that live throughout the northern hemisphere. They mainly reproduce clonaly, but produce sexual resting eggs when conditions are poor, which can hatch when conditions improve. Pasteuria is a common bacterial parasite of Daphnia, which causes 100 % mortality in in infected hosts, and removes their ability to reproduce. It also causes the host to turn bright red in colour, making it easy to differentiate infected from uninfected individuals. It is transmitted from environmental reservoirs in the sediment, when Daphnia pick up spores while filter feeding.
In the wild, seasonal epidemics of the parasite are observed in freshwater ponds. As temperature increases in the spring, Daphnia start to hatch from their resting eggs and their population increases in size. Other aquatic insects begin to hatch, including those that may prey on Daphnia. It has been hypothesized that these small predators may release parasite spores into the water when feeding on infected Daphnia (sloppy feeding) and contribute to transmission. A few weeks later, infections begin to be observed, and prevalence peaks around midsummer, usually reaching nearly 100 %. At the same time, the proportion of hosts in the population that are susceptible to many strains of the parasite declines, reaching nearly 0. The epidemic then declines and ends in the late summer.
Because all of these things are happening simultaneously, it is difficult to attribute these dynamics to any particular driver. The objective of this project was to investigate how these various factors (temperature, transmission from the spore bank, sloppy feeding in the free water and selection for host resistance) interact to influence the repeatable seasonal epidemic dynamics observed in nature in order to further understand the drivers of epidemics, by pairing observational and experimental work.
I have completed two season’s worth of field observations at the Aeglesee, which consisted of weekly sampling trips from March-September of 2022 and 2023. For each trip, I collected water and plankton samples which were used to measure the density of algae, parasite spores and all zooplankton species in the pond, as well as measured water depth and surface temperature. I have also gained even longer-term data from MeteoSwiss from a nearby weather station which I have calibrated to the pond’s temperature. I am using these data to further analyse how temperature and season length may influence outbreak dynamics (preliminary results indicate that climate changed has increased the period over which the parasite is transmissible), and make predictions in the context of climate change, with a manuscript currently in prep.
I ran a large-scale experiment to disentangle the effects of temperature on host development from the effects of temperature on parasite spread using five temperature treatments and three host treatments (ephippia hatchlings, vs clonal broadly susceptible or broadly resistant juveniles) and mud containing parasite spores collected from the field site. I found that the parasite time to infection decreases with increasing temperature at a much faster rate than host development time to development decreases with increasing temperature, that hosts born from resting eggs are less likely to be infected than those born clonally, and that hosts that are susceptible to many strains of the parasite are faster to become infected than those that are susceptible to only a few. These results have been presented at several conferences and seminars, as well as published in Oikos. The raw data is also publicly available on Dryad for further exploitation.
During the 2022 field season I ran several pilots to test the sloppy feeding hypothesis by placing our candidate small predators (midge larvae and water boatmen) in jars with infected and uninfected Daphnia. Unfortunately, in each case, the “predator” died without feeding on the Daphnia, suggesting that they are in fact too small to prey on Daphnia.
However, I did find evidence of spores in the water column through my second large-scale experiment. I exposed Daphnia juveniles to the pond water each week, measuring the rate at which they became infected as a proxy for spore density. I found that individuals did become infected, indicating that spores in the water column do contribute to infection, and that the rate of infection changed throughout the course of the season, tracking with parasite prevalence and zooplankton community density. I then hypothesized that, rather than sloppy feeding, perturbation of the mud by increasing activity could contribute to the fluctuations in spores in the water column, and ran a follow-up experiment in which I measured the sinking rate of spores to demonstrate that repeated perturbation could lead to an accumulation of spores in the water column. I have presented these results at conferences and seminars and am preparing a manuscript.
I ran another experiment over the 2023 field season in which I exposed Daphnia to water from the pond collected each week and measured their infection rate. I this time used highly-specific clones that were each only susceptible to only one of the three major parasite strains, alongside controls that were susceptible to all. In this way, I was able to pin-point which lineages of the parasite were most prominent/infective at which stages of the epidemic, and compare to the resistotype data in order to determine how selection for resistance shapes epidemic and resistance dynamics observed in the pond. A manuscript for this experiment is in-prep, and I presented preliminary results at a workshop.
I ran a large-scale experiment to disentangle the effects of temperature on host development from the effects of temperature on parasite spread using five temperature treatments and three host treatments (ephippia hatchlings, vs clonal broadly susceptible or broadly resistant juveniles) and mud containing parasite spores collected from the field site. I found that the parasite time to infection decreases with increasing temperature at a much faster rate than host development time to development decreases with increasing temperature, that hosts born from resting eggs are less likely to be infected than those born clonally, and that hosts that are susceptible to many strains of the parasite are faster to become infected than those that are susceptible to only a few. These results have been presented at several conferences and seminars, as well as published in Oikos. The raw data is also publicly available on Dryad for further exploitation.
During the 2022 field season I ran several pilots to test the sloppy feeding hypothesis by placing our candidate small predators (midge larvae and water boatmen) in jars with infected and uninfected Daphnia. Unfortunately, in each case, the “predator” died without feeding on the Daphnia, suggesting that they are in fact too small to prey on Daphnia.
However, I did find evidence of spores in the water column through my second large-scale experiment. I exposed Daphnia juveniles to the pond water each week, measuring the rate at which they became infected as a proxy for spore density. I found that individuals did become infected, indicating that spores in the water column do contribute to infection, and that the rate of infection changed throughout the course of the season, tracking with parasite prevalence and zooplankton community density. I then hypothesized that, rather than sloppy feeding, perturbation of the mud by increasing activity could contribute to the fluctuations in spores in the water column, and ran a follow-up experiment in which I measured the sinking rate of spores to demonstrate that repeated perturbation could lead to an accumulation of spores in the water column. I have presented these results at conferences and seminars and am preparing a manuscript.
I ran another experiment over the 2023 field season in which I exposed Daphnia to water from the pond collected each week and measured their infection rate. I this time used highly-specific clones that were each only susceptible to only one of the three major parasite strains, alongside controls that were susceptible to all. In this way, I was able to pin-point which lineages of the parasite were most prominent/infective at which stages of the epidemic, and compare to the resistotype data in order to determine how selection for resistance shapes epidemic and resistance dynamics observed in the pond. A manuscript for this experiment is in-prep, and I presented preliminary results at a workshop.
This project combining laboratory experiments with complementary field observations offers the unique opportunity to explain the population dynamics observed in nature through comparing experimental epidemics to natural ones, and to provide further information about applicability of experimental epidemiology to natural systems. The combination of approaches proposed in this project allow us to disentangle the complex relationships between hosts, parasites, the broader ecological community, and the abiotic environment and gain further insight to the rules that govern epidemic cycles and ecological feedback loops. It further allows to estimate the effect of climate change on the future dynamics of this host-parasite system. Understanding the drivers of infectious disease dynamics and the complex mechanisms of transmission and their relationship to the biotic and abiotic environment are more important than ever as we face the dual and linked challenges of global change and emerging infectious disease.