An immunological marker of tolerance to infection in wild rodents.
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...
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Public Library of Science (PLoS)
2014
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oai:doaj.org-article:32f0f91d0a234beab6d95f3349f12eec2021-11-25T05:33:02ZAn immunological marker of tolerance to infection in wild rodents.1544-91731545-788510.1371/journal.pbio.1001901https://doaj.org/article/32f0f91d0a234beab6d95f3349f12eec2014-07-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25004450/?tool=EBIhttps://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Hosts 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.Joseph A JacksonAmy J HallIda M FribergCatriona RalliAnn LoweMalgorzata ZawadzkaAndrew K TurnerAlexander StewartRichard J BirtlesSteve PatersonJanette E BradleyMike BegonPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 12, Iss 7, p e1001901 (2014) |
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EN |
| topic |
Biology (General) QH301-705.5 |
| spellingShingle |
Biology (General) QH301-705.5 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 Janette E Bradley Mike Begon An immunological marker of tolerance to infection in wild rodents. |
| description |
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. |
| format |
article |
| author |
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 Janette E Bradley Mike Begon |
| author_facet |
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 Janette E Bradley Mike Begon |
| author_sort |
Joseph A Jackson |
| title |
An immunological marker of tolerance to infection in wild rodents. |
| title_short |
An immunological marker of tolerance to infection in wild rodents. |
| title_full |
An immunological marker of tolerance to infection in wild rodents. |
| title_fullStr |
An immunological marker of tolerance to infection in wild rodents. |
| title_full_unstemmed |
An immunological marker of tolerance to infection in wild rodents. |
| title_sort |
immunological marker of tolerance to infection in wild rodents. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2014 |
| url |
https://doaj.org/article/32f0f91d0a234beab6d95f3349f12eec |
| work_keys_str_mv |
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