Limits...
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

Host growth and reproduction across feeding interval treatment and infection class. Both axes are shown in cumulative carbon units to facilitate a direct comparison. Solid lines show the GAMM predictions for each treatment and class, and shadings show the standard error. (a) Feeding treatment has little effect on host growth in control (black) and uninfected animals (grey), but gigantism is substantially reduced in infected animals (red). (b) Feeding treatment substantially reduces host reproduction in control and uninfected animals, but has little impact on castration (the age when reproduction ceases) in the infected class.
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RSPB20141087F2: Host growth and reproduction across feeding interval treatment and infection class. Both axes are shown in cumulative carbon units to facilitate a direct comparison. Solid lines show the GAMM predictions for each treatment and class, and shadings show the standard error. (a) Feeding treatment has little effect on host growth in control (black) and uninfected animals (grey), but gigantism is substantially reduced in infected animals (red). (b) Feeding treatment substantially reduces host reproduction in control and uninfected animals, but has little impact on castration (the age when reproduction ceases) in the infected class.

Mentions: Changing the feeding interval from 1 to 6 days had a minimal impact on the growth trajectories in the control animals (figure 2a; electronic supplementary material, table S2), but caused a strong decrease in the amount of reproduction (figure 2b; electronic supplementary material, table S2). For example, in the 4-day feeding interval treatment, the animals were 7% smaller on average, but reproduced 48% less on average (electronic supplementary material, figure S5). As anticipated, infection induced both gigantism and castration in the everyday feeding treatment (figure 2; electronic supplementary material, table S4). Infected animals also had larger clutches than uninfected animals, though this difference was only statistically significant in T1 and T2 (electronic supplementary material, figure S6). However, the magnitude of gigantism was reduced and its onset delayed as the feeding interval increased. The growth trajectories of control and infected animals were statistically indistinguishable in feeding treatments T4–T6 (figure 2a; electronic supplementary material, table S4). The exposed but uninfected animals had similar growth and reproduction trajectories to the control animals (electronic supplementary material, table S3).Figure 2.


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

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

Host growth and reproduction across feeding interval treatment and infection class. Both axes are shown in cumulative carbon units to facilitate a direct comparison. Solid lines show the GAMM predictions for each treatment and class, and shadings show the standard error. (a) Feeding treatment has little effect on host growth in control (black) and uninfected animals (grey), but gigantism is substantially reduced in infected animals (red). (b) Feeding treatment substantially reduces host reproduction in control and uninfected animals, but has little impact on castration (the age when reproduction ceases) in the infected class.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

RSPB20141087F2: Host growth and reproduction across feeding interval treatment and infection class. Both axes are shown in cumulative carbon units to facilitate a direct comparison. Solid lines show the GAMM predictions for each treatment and class, and shadings show the standard error. (a) Feeding treatment has little effect on host growth in control (black) and uninfected animals (grey), but gigantism is substantially reduced in infected animals (red). (b) Feeding treatment substantially reduces host reproduction in control and uninfected animals, but has little impact on castration (the age when reproduction ceases) in the infected class.
Mentions: Changing the feeding interval from 1 to 6 days had a minimal impact on the growth trajectories in the control animals (figure 2a; electronic supplementary material, table S2), but caused a strong decrease in the amount of reproduction (figure 2b; electronic supplementary material, table S2). For example, in the 4-day feeding interval treatment, the animals were 7% smaller on average, but reproduced 48% less on average (electronic supplementary material, figure S5). As anticipated, infection induced both gigantism and castration in the everyday feeding treatment (figure 2; electronic supplementary material, table S4). Infected animals also had larger clutches than uninfected animals, though this difference was only statistically significant in T1 and T2 (electronic supplementary material, figure S6). However, the magnitude of gigantism was reduced and its onset delayed as the feeding interval increased. The growth trajectories of control and infected animals were statistically indistinguishable in feeding treatments T4–T6 (figure 2a; electronic supplementary material, table S4). The exposed but uninfected animals had similar growth and reproduction trajectories to the control animals (electronic supplementary material, table S3).Figure 2.

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