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Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival

Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circula...

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Autores principales: Nussey, Daniel H., Watt, Kathryn A., Clark, Abigail, Pilkington, Jill G., Pemberton, Josephine M., Graham, Andrea L., McNeilly, Tom N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3924079/
https://www.ncbi.nlm.nih.gov/pubmed/24500168
http://dx.doi.org/10.1098/rspb.2013.2931
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author Nussey, Daniel H.
Watt, Kathryn A.
Clark, Abigail
Pilkington, Jill G.
Pemberton, Josephine M.
Graham, Andrea L.
McNeilly, Tom N.
author_facet Nussey, Daniel H.
Watt, Kathryn A.
Clark, Abigail
Pilkington, Jill G.
Pemberton, Josephine M.
Graham, Andrea L.
McNeilly, Tom N.
author_sort Nussey, Daniel H.
collection PubMed
description Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circulating in vivo reflect a composite of constitutive and induced functional variants of diverse specificities (e.g. binding antigens from prevalent parasites, self tissues or novel non-self sources). Here, we measured plasma concentrations of 11 different antibody types in adult females from an unmanaged population of Soay sheep on St Kilda. Correlations among antibody measures were generally positive but weak, and eight of the measures independently predicted body mass, strongyle parasite egg count or survival over the subsequent winter. These independent and, in some cases, antagonistic relationships point to important multivariate immunological heterogeneities affecting organismal health and fitness in natural systems. Notably, we identified a strong positive association between anti-nematode immunoglobulin (Ig) G antibodies in summer and subsequent over-winter survival, providing rare evidence for a fitness benefit of helminth-specific immunity under natural conditions. Our results highlight both the evolutionary and ecological importance and the complex nature of the immune phenotype in the wild.
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spelling pubmed-39240792014-03-22 Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival Nussey, Daniel H. Watt, Kathryn A. Clark, Abigail Pilkington, Jill G. Pemberton, Josephine M. Graham, Andrea L. McNeilly, Tom N. Proc Biol Sci Research Articles Despite our rapidly advancing mechanistic understanding of vertebrate immunity under controlled laboratory conditions, the links between immunity, infection and fitness under natural conditions remain poorly understood. Antibodies are central to acquired immune responses, and antibody levels circulating in vivo reflect a composite of constitutive and induced functional variants of diverse specificities (e.g. binding antigens from prevalent parasites, self tissues or novel non-self sources). Here, we measured plasma concentrations of 11 different antibody types in adult females from an unmanaged population of Soay sheep on St Kilda. Correlations among antibody measures were generally positive but weak, and eight of the measures independently predicted body mass, strongyle parasite egg count or survival over the subsequent winter. These independent and, in some cases, antagonistic relationships point to important multivariate immunological heterogeneities affecting organismal health and fitness in natural systems. Notably, we identified a strong positive association between anti-nematode immunoglobulin (Ig) G antibodies in summer and subsequent over-winter survival, providing rare evidence for a fitness benefit of helminth-specific immunity under natural conditions. Our results highlight both the evolutionary and ecological importance and the complex nature of the immune phenotype in the wild. The Royal Society 2014-03-22 /pmc/articles/PMC3924079/ /pubmed/24500168 http://dx.doi.org/10.1098/rspb.2013.2931 Text en http://creativecommons.org/licenses/by/3.0/ © 2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Research Articles
Nussey, Daniel H.
Watt, Kathryn A.
Clark, Abigail
Pilkington, Jill G.
Pemberton, Josephine M.
Graham, Andrea L.
McNeilly, Tom N.
Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title_full Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title_fullStr Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title_full_unstemmed Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title_short Multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
title_sort multivariate immune defences and fitness in the wild: complex but ecologically important associations among plasma antibodies, health and survival
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3924079/
https://www.ncbi.nlm.nih.gov/pubmed/24500168
http://dx.doi.org/10.1098/rspb.2013.2931
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