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Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal

The transfer of antibodies from mother to offspring provides crucial protection against infection to offspring during early life in humans and domestic and laboratory animals. However, few studies have tested the consequences of variation in maternal antibody transfer for offspring fitness in the wi...

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Autores principales: Sparks, Alexandra M., Hayward, Adam D., Watt, Kathryn, Pilkington, Jill G., Pemberton, Josephine M., Johnston, Susan E., McNeilly, Tom N., Nussey, Daniel H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7739501/
https://www.ncbi.nlm.nih.gov/pubmed/33234082
http://dx.doi.org/10.1098/rspb.2020.1931
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author Sparks, Alexandra M.
Hayward, Adam D.
Watt, Kathryn
Pilkington, Jill G.
Pemberton, Josephine M.
Johnston, Susan E.
McNeilly, Tom N.
Nussey, Daniel H.
author_facet Sparks, Alexandra M.
Hayward, Adam D.
Watt, Kathryn
Pilkington, Jill G.
Pemberton, Josephine M.
Johnston, Susan E.
McNeilly, Tom N.
Nussey, Daniel H.
author_sort Sparks, Alexandra M.
collection PubMed
description The transfer of antibodies from mother to offspring provides crucial protection against infection to offspring during early life in humans and domestic and laboratory animals. However, few studies have tested the consequences of variation in maternal antibody transfer for offspring fitness in the wild. Further, separating the immunoprotective effects of antibodies from their association with nutritional resources provided by mothers is difficult. Here, we measured plasma levels of total and parasite-specific antibodies in neonatal (less than 10 days old) wild Soay sheep over 25 years to quantify variation in maternal antibody transfer and test its association with offspring survival. Maternal antibody transfer was predicted by maternal age and previous antibody responses, and was consistent within mothers across years. Neonatal total IgG antibody levels were positively related to early growth, suggesting they reflected nutritional transfer. Neonatal parasite-specific IgG levels positively predicted first-year survival, independent of lamb weight, total IgG levels and subsequent lamb parasite-specific antibody levels. This relationship was partly mediated via an indirect negative association with parasite burden. We show that among-female variation in maternal antibody transfer can have long-term effects on offspring growth, parasite burden and fitness in the wild, and is likely to impact naturally occurring host–parasite dynamics.
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spelling pubmed-77395012020-12-17 Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal Sparks, Alexandra M. Hayward, Adam D. Watt, Kathryn Pilkington, Jill G. Pemberton, Josephine M. Johnston, Susan E. McNeilly, Tom N. Nussey, Daniel H. Proc Biol Sci Evolution The transfer of antibodies from mother to offspring provides crucial protection against infection to offspring during early life in humans and domestic and laboratory animals. However, few studies have tested the consequences of variation in maternal antibody transfer for offspring fitness in the wild. Further, separating the immunoprotective effects of antibodies from their association with nutritional resources provided by mothers is difficult. Here, we measured plasma levels of total and parasite-specific antibodies in neonatal (less than 10 days old) wild Soay sheep over 25 years to quantify variation in maternal antibody transfer and test its association with offspring survival. Maternal antibody transfer was predicted by maternal age and previous antibody responses, and was consistent within mothers across years. Neonatal total IgG antibody levels were positively related to early growth, suggesting they reflected nutritional transfer. Neonatal parasite-specific IgG levels positively predicted first-year survival, independent of lamb weight, total IgG levels and subsequent lamb parasite-specific antibody levels. This relationship was partly mediated via an indirect negative association with parasite burden. We show that among-female variation in maternal antibody transfer can have long-term effects on offspring growth, parasite burden and fitness in the wild, and is likely to impact naturally occurring host–parasite dynamics. The Royal Society 2020-11-25 2020-11-25 /pmc/articles/PMC7739501/ /pubmed/33234082 http://dx.doi.org/10.1098/rspb.2020.1931 Text en © 2020 The Authors. http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/http://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Evolution
Sparks, Alexandra M.
Hayward, Adam D.
Watt, Kathryn
Pilkington, Jill G.
Pemberton, Josephine M.
Johnston, Susan E.
McNeilly, Tom N.
Nussey, Daniel H.
Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title_full Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title_fullStr Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title_full_unstemmed Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title_short Maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
title_sort maternally derived anti-helminth antibodies predict offspring survival in a wild mammal
topic Evolution
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7739501/
https://www.ncbi.nlm.nih.gov/pubmed/33234082
http://dx.doi.org/10.1098/rspb.2020.1931
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