Energetic scaling across different host densities and its consequences for pathogen proliferation

Nørgaard, Louise Solveig; Ghedini, Giulia; Phillips, Benjamin L.; Hall, Matthew D.

doi:10.1111/1365-2435.13721

Cited by 11 publications

(14 citation statements)

References 59 publications

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“…Our findings show that individuals differ consistently in how their MR responds to acute temperature changes over an ecologically relevant time period, although overall repeatability of the slope was relatively low and imprecise. It is important to note that repeatability estimates capture variation due to both genetic and environmental effects, such as different developmental environments experienced by animals (Careau et al 2014, Nørgaard et al 2021). However, assuming a proportion of among‐individual differences is the result of heritable variation our findings suggests that metabolic thermal plasticity may be capable of evolutionary change allowing shifts in population‐level metabolic reaction norms (Ghalambor et al 2007).…”

Section: Discussionmentioning

confidence: 99%

Individual variation in thermal plasticity and its impact on mass‐scaling

Kar

Nakagawa

Friesen

et al. 2021

Oikos

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Physiological processes vary widely across individuals and can influence how individuals respond to environmental change. Repeatability in how metabolic rate changes across temperatures (i.e. metabolic thermal plasticity) can influence mass‐scaling exponents in different thermal environments. Moreover, repeatable plastic responses are necessary for reaction norms to respond to selective forces which is important for populations living in fluctuating environments. Nonetheless, only a small number of studies have explicitly quantified repeatability in metabolic plasticity, and fewer have explored how it can impact mass‐scaling. We repeatedly measured standard metabolic rate of n = 42 delicate skinks Lampropholis delicata at six temperatures over the course of four months (N[observations] = 4952). Using hierarchical statistical techniques, we accounted for multi‐level variation and measurement error in our data in order to obtain more precise estimates of reaction norm repeatability and mass‐scaling exponents at different acute temperatures. Our results show that individual differences in metabolic thermal plasticity were somewhat consistent over time (Rslope = 0.25, 95% CI = 2.48 × 10−8 – 0.67), however estimates were associated with a large degree of error. After accounting for measurement error, which decreased steadily with temperature, we show that among individual variance remained consistent across all temperatures. Congruently, temperature specific repeatability of average metabolic rate was stable across temperatures. Cross‐temperature correlations were positive but were not uniform across the reaction norm. After taking into account multiple sources of variation, our estimates for mass‐scaling did not change with temperature and were in line with published values for snakes and lizards. This implies that repeatable plastic responses may promote thermal stability of scaling exponents. Our work contributes to understanding how energy expenditure scales with abiotic and biotic factors and the capacity for reaction norms to respond to selection.

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Section: Discussionmentioning

confidence: 99%

Individual variation in thermal plasticity and its impact on mass‐scaling

Kar

Nakagawa

Friesen

et al. 2021

Oikos

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“…The increased burden of providing energy for both parasite functions and its own can lead to an overall increased host energy use and metabolic rate (e.g. [ 99 ]). For example, a crab infected by a mature rhizocephalan can have double the metabolic rate of the uninfected host [ 109 ].…”

Section: Host Heat Tolerance During Infection: What Mechanisms Could ...mentioning

confidence: 99%

Infection burdens and virulence under heat stress: ecological and evolutionary considerations

Hector

Gehman

King

2023

Phil. Trans. R. Soc. B

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As a result of global change, hosts and parasites (including pathogens) are experiencing shifts in their thermal environment. Despite the importance of heat stress tolerance for host population persistence, infection by parasites can impair a host's ability to cope with heat. Host–parasite eco-evolutionary dynamics will be affected if infection reduces host performance during heating. Theory predicts that within-host parasite burden (replication rate or number of infecting parasites per host), a key component of parasite fitness, should correlate positively with virulence—the harm caused to hosts during infection. Surprisingly, however, the relationship between within-host parasite burden and virulence during heating is often weak. Here, we describe the current evidence for the link between within-host parasite burden and host heat stress tolerance. We consider the biology of host–parasite systems that may explain the weak or absent link between these two important host and parasite traits during hot conditions. The processes that mediate the relationship between parasite burden and host fitness will be fundamental in ecological and evolutionary responses of host and parasites in a warming world. This article is part of the theme issue ‘Infectious disease ecology and evolution in a changing world’.

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“…shown to correlate positively with pathogen load in this study system (Gipson et al, 2022;Nørgaard et al, 2021). Clearing infection, however, is instead expected to occur more rapidly.…”

Section: Discussionmentioning

confidence: 59%

“…Measures of host activity and feeding rates are currently not available for hosts that were exposed to a pathogen and successfully resisted infection in this system. However, infection has been shown to reduce activity (Nørgaard et al, 2019a(Nørgaard et al, , 2019b and slightly reduce feeding rates (albeit in a genotype-specific manner, Gipson et al, 2022;Nørgaard et al, 2021), hinting that resistant hosts are most likely behaving differently. However, regardless of the mechanism, our results suggest that the physiological (i.e.…”

Section: Discussionmentioning

confidence: 99%

The hidden costs of resistance: Contrasting the energetics of successfully and unsuccessfully fighting infection

Hall,

Phillips,

White

et al. 2024

Functional Ecology

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Exposure to a pathogen is predicted to lead to increased energy use as hosts attempt to activate a costly immune system and repair damaged tissue. To meet this demand, metabolic rates, which capture the rate at which a host can use, transform and expend energy, are expected to increase. Yet for many host–pathogen systems, metabolic rates after encountering a pathogen are just as likely to decrease as increase, suggesting that increased energy expenditure may not always be best for fighting infection. Diverging metabolic trajectories have been previously attributed to the different pathways that specific pathogen classes, such as bacteria or viruses, induce in a host. Here, we test how the magnitude and direction of metabolic change following pathogen exposure might also depend on whether a host has cleared infection or is instead fighting to reduce pathogen burden, as well as interactions between host and pathogen genotypes of a single host–pathogen system. Using a model system, Daphnia magna and its bacterial pathogen, we quantified changes in mass‐independent metabolic rates over a 30‐day period for multiple host and pathogen genotypes. We found that the metabolic trajectory of an exposed host diverged quickly during the infection process. For hosts that were exposed to a pathogen and resisted infection, their mass‐independent metabolic rates remained suppressed long after exposure, leading to a sustained reduction in total energy use compared to unexposed animals. The reverse was true for hosts in which the pathogen was able to establish an infection. Underlying these changes were differences in the energetic burden that each pathogen genotype imposed on its host, as well as changes in the way host genotype and the outcome of infection shaped underlying scaling relationships between host body mass and metabolic rates. Our results demonstrate how variation in an organism's metabolic rate and overall energy use can arise from within a single host–pathogen encounter and depend on the likelihood of pathogen clearance, as well as the within‐species genetic variability of both hosts and pathogens. Read the free Plain Language Summary for this article on the Journal blog.

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Energetic scaling across different host densities and its consequences for pathogen proliferation

Cited by 11 publications

References 59 publications

Individual variation in thermal plasticity and its impact on mass‐scaling

Individual variation in thermal plasticity and its impact on mass‐scaling

Infection burdens and virulence under heat stress: ecological and evolutionary considerations

The hidden costs of resistance: Contrasting the energetics of successfully and unsuccessfully fighting infection

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