Host susceptibility may be critical for the spread of infectious disease, and understanding its basis is a goal of ecological immunology. Here, we employed a series of mechanistic tests to evaluate four factors commonly assumed to influence host susceptibility: parasite exposure, barriers to infection, immune responses, and body size. We tested these factors in an aquatic host–parasite system (Daphnia dentifera and the fungal parasite, Metschnikowia bicuspidata) using both laboratory-reared and field-collected hosts. We found support for each factor as a driver of infection. Elevated parasite exposure, which occurs through consumption of infectious fungal spores, increased a host’s probability of infection. The host’s gut epithelium functioned as a barrier to infection, but in the opposite manner from which we predicted: thinner anterior gut epithelia were more resistant to infectious spores than thick epithelia. This relationship may be mediated by structural attributes associated with epithelial cell height. Fungal spores that breached the host’s gut barrier elicited an intensity-dependent hemocyte response that decreased the probability of infection for some Daphnia. Although larger body sizes were associated with increased levels of spore ingestion, larger hosts also had lower frequencies of parasite attack, less penetrable gut barriers, and stronger hemocyte responses. After investigating which mechanisms underlie host susceptibility, we asked: do these four factors contribute equally or asymmetrically to the outcome of infection? An information-theoretic approach revealed that host immune defenses (barriers and immune responses) played the strongest roles in mediating infection outcomes. These two immunological traits may be valuable metrics for linking host susceptibility to the spread of infectious disease.
Immune responses can be energetically expensive and subject to trade-offs. Prior work on the freshwater zooplankton, Ceriodaphnia cornuta, demonstrated an association between eye size and infection, leading to questions about whether investment in eyes trades off against investment in immunity. We used the crustacean host, Daphnia dentifera, and its fungal parasite, Metschnikowia bicuspidata, to investigate the relationships between eye size, parasite resistance and infection. In the field, we found a negative correlation between size-corrected eye area (SCEA) and Metschnikowia infection, suggesting that either SCEA decreases infection (thereby indicating resistance) or that infection decreases SCEA. Controlled laboratory experiments reinforced the latter result: exposure to the fungal parasite decreased a host’s SCEA, regardless of the parasite dose or host genotype. We also uncovered significant plasticity in this trait—both host age and resource level increased SCEA. Identifying causality in physiological correlations is challenging. Our results suggest that negative associations between parasitism and energetically-expensive traits can arise through plasticity.
more » « less- PAR ID:
- 10550242
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Plankton Research
- ISSN:
- 0142-7873
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Transmission from one host to another is a crucial component of parasite fitness. For some aquatic parasites, transmission occurs via a free‐living stage that spends time in the water, awaiting an encounter with a new host. These parasite transmission stages can be impacted by biotic and abiotic factors that influence the parasite's ability to successfully infect or grow in a new host.
Here we tested whether time spent in the water column and/or exposure to common cyanobacterial toxins impacted parasite transmission stages. More specifically, we tested whether the infectivity, within host growth, and virulence of the fungal parasite
Metschnikowia bicuspidata changed as a result of time spent in the water or from exposure to cyanotoxins in the water column. We exposed parasite transmission spores to different levels of one of two ecologically important cyanotoxins, microcystin‐LR and anatoxin‐a, and factorially manipulated the amount of time spores were incubated in water. We removed the toxins and used those same spores to infect one genotype of the common lake zooplanktonDaphnia dentifera .We found that cyanotoxins did not impact parasite fitness (infection prevalence and spore yield per infected host) or virulence (host lifetime reproduction and survivorship) at the tested concentrations (10 and 30 μg/L). However, we found that spending longer as a transmission spore decreased a spore's chances for successful infection: spores that were only incubated for 24 hr infected approximately 75% of exposed hosts, whereas spores incubated for 10 days infected less than 50% of exposed hosts.
We also found a negative relationship between the final spore yield from infected hosts and the proportion of hosts that became infected. In treatments where spores spent longer in the water column prior to encountering a host, infection prevalence was lower (indicating lower per spore infectivity), but each infected host yielded more spores at the end of infection. We hypothesise that this pattern may result from intraspecific parasite competition within the host.
Overall, these results suggest that transmission spores of this parasite are not strongly influenced by cyanotoxins in the water column, but that other aspects of spending time in the water strongly influence parasite fitness.
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