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Locomotor effects of a fibrosis-based immune response in stickleback fish

The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, b...

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Autores principales: Matthews, David G., Maciejewski, Meghan F., Wong, Greta A., Lauder, George V., Bolnick, Daniel I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10326981/
https://www.ncbi.nlm.nih.gov/pubmed/37425734
http://dx.doi.org/10.1101/2023.06.24.546342
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author Matthews, David G.
Maciejewski, Meghan F.
Wong, Greta A.
Lauder, George V.
Bolnick, Daniel I.
author_facet Matthews, David G.
Maciejewski, Meghan F.
Wong, Greta A.
Lauder, George V.
Bolnick, Daniel I.
author_sort Matthews, David G.
collection PubMed
description The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences.
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spelling pubmed-103269812023-07-08 Locomotor effects of a fibrosis-based immune response in stickleback fish Matthews, David G. Maciejewski, Meghan F. Wong, Greta A. Lauder, George V. Bolnick, Daniel I. bioRxiv Article The vertebrate immune system provides an impressively effective defense against parasites and pathogens. However, these benefits must be balanced against a range of costly side-effects including energy loss and risks of auto-immunity. These costs might include biomechanical impairment of movement, but little is known about the intersection between immunity and biomechanics. Here, we show that a fibrosis immune response in threespine stickleback (Gasterosteus aculeatus) has collateral effects on their locomotion. When freshwater stickleback are infected with the tapeworm parasite Schistocephalus solidus, they face an array of fitness consequences ranging from impaired body condition and fertility to an increased risk of mortality. To fight the infection, some stickleback will initiate a fibrosis immune response in which they produce excess collagenous tissue in their coelom. Although fibrosis is effective at reducing infection, some populations of stickleback actively suppress this immune response, possibly because the costs of fibrosis outweigh the benefits. Here we quantify the locomotor effects of the fibrosis immune response in the absence of parasites to investigate whether there are collateral costs of fibrosis that could help explain why some fish forego this effective defense. To do this, we induce fibrosis in stickleback and then test their C-start escape performance. Additionally, we measure the severity of fibrosis, body stiffness, and body curvature during the escape response. We were able to estimate performance costs of fibrosis by including these variables as intermediates in a structural equation model. This model reveals that among control fish without fibrosis, there is a performance cost associated with increased body stiffness. However, fish with fibrosis did not experience this cost but rather displayed increased performance with higher fibrosis severity. This result demonstrates that the adaptive landscape of immune responses can be complex with the potential for wide reaching and unexpected fitness consequences. Cold Spring Harbor Laboratory 2023-06-26 /pmc/articles/PMC10326981/ /pubmed/37425734 http://dx.doi.org/10.1101/2023.06.24.546342 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Matthews, David G.
Maciejewski, Meghan F.
Wong, Greta A.
Lauder, George V.
Bolnick, Daniel I.
Locomotor effects of a fibrosis-based immune response in stickleback fish
title Locomotor effects of a fibrosis-based immune response in stickleback fish
title_full Locomotor effects of a fibrosis-based immune response in stickleback fish
title_fullStr Locomotor effects of a fibrosis-based immune response in stickleback fish
title_full_unstemmed Locomotor effects of a fibrosis-based immune response in stickleback fish
title_short Locomotor effects of a fibrosis-based immune response in stickleback fish
title_sort locomotor effects of a fibrosis-based immune response in stickleback fish
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10326981/
https://www.ncbi.nlm.nih.gov/pubmed/37425734
http://dx.doi.org/10.1101/2023.06.24.546342
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