Natural selection on individual variation in tolerance of gastrointestinal nematode infection.

Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-paras...

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Autores principales:	Adam D Hayward, Daniel H Nussey, Alastair J Wilson, Camillo Berenos, Jill G Pilkington, Kathryn A Watt, Josephine M Pemberton, Andrea L Graham
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/33ce780e602d4cb59db35f8ca8078a9d
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spelling	oai:doaj.org-article:33ce780e602d4cb59db35f8ca8078a9d2021-11-25T05:33:01ZNatural selection on individual variation in tolerance of gastrointestinal nematode infection.1544-91731545-788510.1371/journal.pbio.1001917https://doaj.org/article/33ce780e602d4cb59db35f8ca8078a9d2014-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25072883/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.Adam D HaywardDaniel H NusseyAlastair J WilsonCamillo BerenosJill G PilkingtonKathryn A WattJosephine M PembertonAndrea L GrahamPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 7, p e1001917 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Adam D Hayward Daniel H Nussey Alastair J Wilson Camillo Berenos Jill G Pilkington Kathryn A Watt Josephine M Pemberton Andrea L Graham Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
description	Hosts may mitigate the impact of parasites by two broad strategies: resistance, which limits parasite burden, and tolerance, which limits the fitness or health cost of increasing parasite burden. The degree and causes of variation in both resistance and tolerance are expected to influence host-parasite evolutionary and epidemiological dynamics and inform disease management, yet very little empirical work has addressed tolerance in wild vertebrates. Here, we applied random regression models to longitudinal data from an unmanaged population of Soay sheep to estimate individual tolerance, defined as the rate of decline in body weight with increasing burden of highly prevalent gastrointestinal nematode parasites. On average, individuals lost weight as parasite burden increased, but whereas some lost weight slowly as burden increased (exhibiting high tolerance), other individuals lost weight significantly more rapidly (exhibiting low tolerance). We then investigated associations between tolerance and fitness using selection gradients that accounted for selection on correlated traits, including body weight. We found evidence for positive phenotypic selection on tolerance: on average, individuals who lost weight more slowly with increasing parasite burden had higher lifetime breeding success. This variation did not have an additive genetic basis. These results reveal that selection on tolerance operates under natural conditions. They also support theoretical predictions for the erosion of additive genetic variance of traits under strong directional selection and fixation of genes conferring tolerance. Our findings provide the first evidence of selection on individual tolerance of infection in animals and suggest practical applications in animal and human disease management in the face of highly prevalent parasites.
format	article
author	Adam D Hayward Daniel H Nussey Alastair J Wilson Camillo Berenos Jill G Pilkington Kathryn A Watt Josephine M Pemberton Andrea L Graham
author_facet	Adam D Hayward Daniel H Nussey Alastair J Wilson Camillo Berenos Jill G Pilkington Kathryn A Watt Josephine M Pemberton Andrea L Graham
author_sort	Adam D Hayward
title	Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
title_short	Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
title_full	Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
title_fullStr	Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
title_full_unstemmed	Natural selection on individual variation in tolerance of gastrointestinal nematode infection.
title_sort	natural selection on individual variation in tolerance of gastrointestinal nematode infection.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/33ce780e602d4cb59db35f8ca8078a9d
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Natural selection on individual variation in tolerance of gastrointestinal nematode infection.

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