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An Immunological Marker of Tolerance to Infection in Wild Rodents

Jackson, Joseph A.; Hall, Amy J.; Friberg, Ida M.; Ralli, Catriona; Lowe, Ann; Zawadzka, Malgorzata; Turner, Andrew K.; Stewart, Alexander; Birtles, Richard J.; Paterson, Steve; Bradley, Janette E.; Begon, Mike

Authors

Joseph A. Jackson

Amy J. Hall

Ida M. Friberg

Catriona Ralli

Ann Lowe

Malgorzata Zawadzka

Andrew K. Turner

Alexander Stewart

Richard J. Birtles

Steve Paterson

JAN BRADLEY jan.bradley@nottingham.ac.uk
Professor of Parasitology

Mike Begon



Contributors

David S. Schneider
Editor

Abstract

Hosts are likely to respond to parasitic infections by a combination of resistance (expulsion of pathogens) and tolerance (active mitigation of pathology). Of these strategies, the basis of tolerance in animal hosts is relatively poorly understood, with especially little known about how tolerance is manifested in natural populations. We monitored a natural population of field voles using longitudinal and cross-sectional sampling modes and taking measurements on body condition, infection, immune gene expression, and survival. Using analyses stratified by life history stage, we demonstrate a pattern of tolerance to macroparasites in mature compared to immature males. In comparison to immature males, mature males resisted infection less and instead increased investment in body condition in response to accumulating burdens, but at the expense of reduced reproductive effort. We identified expression of the transcription factor Gata3 (a mediator of Th2 immunity) as an immunological biomarker of this tolerance response. Time series data for individual animals suggested that macroparasite infections gave rise to increased expression of Gata3, which gave rise to improved body condition and enhanced survival as hosts aged. These findings provide a clear and unexpected insight into tolerance responses (and their life history sequelae) in a natural vertebrate population. The demonstration that such responses (potentially promoting parasite transmission) can move from resistance to tolerance through the course of an individual’s lifetime emphasises the need to incorporate them into our understanding of the dynamics and risk of infection in the natural environment. Moreover, the identification of Gata3 as a marker of tolerance to macroparasites raises important new questions regarding the role of Th2 immunity and the mechanistic nature of the tolerance response itself. A more manipulative, experimental approach is likely to be valuable in elaborating this further.

Citation

Jackson, J. A., Hall, A. J., Friberg, I. M., Ralli, C., Lowe, A., Zawadzka, M., …Begon, M. (2014). An Immunological Marker of Tolerance to Infection in Wild Rodents. PLoS Biology, 12(7), https://doi.org/10.1371/journal.pbio.1001901

Journal Article Type Article
Acceptance Date May 29, 2014
Online Publication Date Jul 8, 2014
Publication Date Jul 8, 2014
Deposit Date Jul 12, 2016
Publicly Available Date Jul 12, 2016
Journal PLoS Biology
Print ISSN 1544-9173
Electronic ISSN 1545-7885
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 12
Issue 7
Article Number e1001901
DOI https://doi.org/10.1371/journal.pbio.1001901
Public URL http://eprints.nottingham.ac.uk/id/eprint/34897
Publisher URL http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1001901
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0





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