Inferring the energy cost of resistance to parasitic infection and its link to a trade-off
Abstract Background In infected hosts, immune responses trigger a systemic energy reallocation away from energy storage and growth, to fuel a costly defense program. The exact energy costs of immune defense are however unknown in general. Life history theory predicts that such costs underpin trade-o...
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BMC
2025-01-01
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| Series: | BMC Ecology and Evolution |
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| Online Access: | https://doi.org/10.1186/s12862-024-02340-0 |
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| author | Frédéric Douhard Carole Moreno-Romieux Andrea B. Doeschl-Wilson |
| author_facet | Frédéric Douhard Carole Moreno-Romieux Andrea B. Doeschl-Wilson |
| author_sort | Frédéric Douhard |
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| description | Abstract Background In infected hosts, immune responses trigger a systemic energy reallocation away from energy storage and growth, to fuel a costly defense program. The exact energy costs of immune defense are however unknown in general. Life history theory predicts that such costs underpin trade-offs between host disease resistance and other fitness related traits, yet this has been seldom assessed. Here we investigate immune energy cost induced by infection, and their potential link to a trade-off between host resistance and fat storage that we previously exposed in sheep divergently selected for resistance to a pathogenic helminth. Results To this purpose, we developed a mathematical model of host-parasite interaction featuring individual changes in energy allocation over the course of infection. The model was fitted to data from an experimental infectious challenge in sheep from genetically resistant and susceptible lines to infer the magnitude of immune energy costs. A relatively small and transient immune energy cost in early infection best explained within-individual changes in growth, energy storage and parasite burden. Among individuals, predicted responses assuming this positive energy cost conformed to the observed trade-off between resistance and storage, whereas a cost-free scenario incorrectly predicted no trade-off. Conclusions Our mechanistic model fitting to experimental data provides novel insights into the link between energy costs and reallocation due to induced resistance within-individual, and trade-offs among individuals of selected lines. These will be useful to better understand the exact role of energy allocation in the evolution of host defenses, and for predicting the emergence of trade-offs in genetic selection. |
| format | Article |
| id | doaj-art-e4354ae823fe44dc823d3a62cf2915fa |
| institution | Kabale University |
| issn | 2730-7182 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj-art-e4354ae823fe44dc823d3a62cf2915fa2025-02-02T12:05:44ZengBMCBMC Ecology and Evolution2730-71822025-01-0125111810.1186/s12862-024-02340-0Inferring the energy cost of resistance to parasitic infection and its link to a trade-offFrédéric Douhard0Carole Moreno-Romieux1Andrea B. Doeschl-Wilson2GenPhySE, Université de Toulouse, INRAE, ENVTGenPhySE, Université de Toulouse, INRAE, ENVTThe Roslin Institute and Royal (Dick) School of Veterinary Studies, University of EdinburghAbstract Background In infected hosts, immune responses trigger a systemic energy reallocation away from energy storage and growth, to fuel a costly defense program. The exact energy costs of immune defense are however unknown in general. Life history theory predicts that such costs underpin trade-offs between host disease resistance and other fitness related traits, yet this has been seldom assessed. Here we investigate immune energy cost induced by infection, and their potential link to a trade-off between host resistance and fat storage that we previously exposed in sheep divergently selected for resistance to a pathogenic helminth. Results To this purpose, we developed a mathematical model of host-parasite interaction featuring individual changes in energy allocation over the course of infection. The model was fitted to data from an experimental infectious challenge in sheep from genetically resistant and susceptible lines to infer the magnitude of immune energy costs. A relatively small and transient immune energy cost in early infection best explained within-individual changes in growth, energy storage and parasite burden. Among individuals, predicted responses assuming this positive energy cost conformed to the observed trade-off between resistance and storage, whereas a cost-free scenario incorrectly predicted no trade-off. Conclusions Our mechanistic model fitting to experimental data provides novel insights into the link between energy costs and reallocation due to induced resistance within-individual, and trade-offs among individuals of selected lines. These will be useful to better understand the exact role of energy allocation in the evolution of host defenses, and for predicting the emergence of trade-offs in genetic selection.https://doi.org/10.1186/s12862-024-02340-0Resource allocation trade-offsHost resistanceMathematical modelling |
| spellingShingle | Frédéric Douhard Carole Moreno-Romieux Andrea B. Doeschl-Wilson Inferring the energy cost of resistance to parasitic infection and its link to a trade-off BMC Ecology and Evolution Resource allocation trade-offs Host resistance Mathematical modelling |
| title | Inferring the energy cost of resistance to parasitic infection and its link to a trade-off |
| title_full | Inferring the energy cost of resistance to parasitic infection and its link to a trade-off |
| title_fullStr | Inferring the energy cost of resistance to parasitic infection and its link to a trade-off |
| title_full_unstemmed | Inferring the energy cost of resistance to parasitic infection and its link to a trade-off |
| title_short | Inferring the energy cost of resistance to parasitic infection and its link to a trade-off |
| title_sort | inferring the energy cost of resistance to parasitic infection and its link to a trade off |
| topic | Resource allocation trade-offs Host resistance Mathematical modelling |
| url | https://doi.org/10.1186/s12862-024-02340-0 |
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