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Starvation reveals the cause of infection-induced castration and gigantism.

Cressler CE, Nelson WA, Day T, McCauley E - Proc. Biol. Sci. (2014)

Bottom Line: Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them.Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration.These results are consistent with an energetic structure where the parasite uses growth energy as a resource.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Queen's University, Kingston, Ontario, Canada cressler@queensu.ca.

ABSTRACT
Parasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna-Pasteuria ramosa host-parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.

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Related in: MedlinePlus

Parasite fitness across treatments for animals with transmission spores. (a) Parasite spore density increases with host age at death and decreases with reduced energy to host reproduction. (b) Parasite spore density increases with size of the animal, but this relationship is not affected by the manipulation of energy to host reproduction. Circles show parasite density of each animal at death, lines show the relationships with statistical support and colours denote the feeding interval treatment.
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RSPB20141087F3: Parasite fitness across treatments for animals with transmission spores. (a) Parasite spore density increases with host age at death and decreases with reduced energy to host reproduction. (b) Parasite spore density increases with size of the animal, but this relationship is not affected by the manipulation of energy to host reproduction. Circles show parasite density of each animal at death, lines show the relationships with statistical support and colours denote the feeding interval treatment.

Mentions: Infection success decreased slightly with increasing feeding interval, but this effect is not statistically significant (table 1; logistic regression, likelihood ratio test χ2 = 6.19, d.f. = 5, p = 0.29). Feeding treatment did have a significant effect on spore production. We expected spore load to increase with age at death [17]. To evaluate whether there was a significant effect of treatment on spore production, we fitted an exponential growth model to the spore load by age at death data. We found strong statistical support for feeding treatment affecting the rate of spore production (a significant effect of treatment on the slope of the log-linear regression; F = 10.93, d.f. = 5.32, p = 3.4 × 10−6; figure 3). We also expected spore load to increase with host size at death [8]. Interestingly, however, while spore load did increase with host size, this relationship was unaffected by feeding treatment (log-linear regression, F = 1.11, d.f. = 5.32, p = 0.37).Table 1.


Starvation reveals the cause of infection-induced castration and gigantism.

Cressler CE, Nelson WA, Day T, McCauley E - Proc. Biol. Sci. (2014)

Parasite fitness across treatments for animals with transmission spores. (a) Parasite spore density increases with host age at death and decreases with reduced energy to host reproduction. (b) Parasite spore density increases with size of the animal, but this relationship is not affected by the manipulation of energy to host reproduction. Circles show parasite density of each animal at death, lines show the relationships with statistical support and colours denote the feeding interval treatment.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150321&req=5

RSPB20141087F3: Parasite fitness across treatments for animals with transmission spores. (a) Parasite spore density increases with host age at death and decreases with reduced energy to host reproduction. (b) Parasite spore density increases with size of the animal, but this relationship is not affected by the manipulation of energy to host reproduction. Circles show parasite density of each animal at death, lines show the relationships with statistical support and colours denote the feeding interval treatment.
Mentions: Infection success decreased slightly with increasing feeding interval, but this effect is not statistically significant (table 1; logistic regression, likelihood ratio test χ2 = 6.19, d.f. = 5, p = 0.29). Feeding treatment did have a significant effect on spore production. We expected spore load to increase with age at death [17]. To evaluate whether there was a significant effect of treatment on spore production, we fitted an exponential growth model to the spore load by age at death data. We found strong statistical support for feeding treatment affecting the rate of spore production (a significant effect of treatment on the slope of the log-linear regression; F = 10.93, d.f. = 5.32, p = 3.4 × 10−6; figure 3). We also expected spore load to increase with host size at death [8]. Interestingly, however, while spore load did increase with host size, this relationship was unaffected by feeding treatment (log-linear regression, F = 1.11, d.f. = 5.32, p = 0.37).Table 1.

Bottom Line: Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them.Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration.These results are consistent with an energetic structure where the parasite uses growth energy as a resource.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Queen's University, Kingston, Ontario, Canada cressler@queensu.ca.

ABSTRACT
Parasites often induce life-history changes in their hosts. In many cases, these infection-induced life-history changes are driven by changes in the pattern of energy allocation and utilization within the host. Because these processes will affect both host and parasite fitness, it can be challenging to determine who benefits from them. Determining the causes and consequences of infection-induced life-history changes requires the ability to experimentally manipulate life history and a framework for connecting life history to host and parasite fitness. Here, we combine a novel starvation manipulation with energy budget models to provide new insights into castration and gigantism in the Daphnia magna-Pasteuria ramosa host-parasite system. Our results show that starvation primarily affects investment in reproduction, and increasing starvation stress reduces gigantism and parasite fitness without affecting castration. These results are consistent with an energetic structure where the parasite uses growth energy as a resource. This finding gives us new understanding of the role of castration and gigantism in this system, and how life-history variation will affect infection outcome and epidemiological dynamics. The approach of combining targeted life-history manipulations with energy budget models can be adapted to understand life-history changes in other disease systems.

Show MeSH
Related in: MedlinePlus