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Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows

Palacios, Maria G.; Winkler, David W.; Klasing, Kirk C.; Hasselquist, Dennis LU and Vleck, Carol M. (2011) In Ecology 92(4). p.952-966
Abstract
Immunosenescence, the aging of the immune system, is well documented in humans and laboratory models and is known to increase infection risk, morbidity, and mortality among the old. Immunosenescence patterns have recently been unveiled in various free-living populations, but their consequences in the wild have not been explored. We investigated the consequences of immunosenescence in free-living Tree Swallows Tachycineta bicolor through a field experiment simulating a bacterial infection (challenge with lipopolysaccharide, LPS) in females of different ages during the nestling rearing period. We assessed behavioral and physiological responses of females, as well as growth and quality of their offspring, to determine the costs associated... (More)
Immunosenescence, the aging of the immune system, is well documented in humans and laboratory models and is known to increase infection risk, morbidity, and mortality among the old. Immunosenescence patterns have recently been unveiled in various free-living populations, but their consequences in the wild have not been explored. We investigated the consequences of immunosenescence in free-living Tree Swallows Tachycineta bicolor through a field experiment simulating a bacterial infection (challenge with lipopolysaccharide, LPS) in females of different ages during the nestling rearing period. We assessed behavioral and physiological responses of females, as well as growth and quality of their offspring, to determine the costs associated with the simulated infection. Results of the experiment differed between the two years of study. In the first year, old females challenged with LPS lost more body mass and reduced their nest visitation rates more, and their offspring tended to grow slower compared to similarly challenged younger females. In contrast, in the second year, old females did not appear to suffer larger costs than younger ones. Interestingly, immunosenescence was only detected during the first year of the study, suggesting that it is the dysregulated immune function characteristic of immunosenescent individuals rather than age per se that can lead to higher costs of immune defense in old individuals. These results provide the first evidence of costs of immunosenescence in free-living animals and support the hypothesis that old, immunosenescent individuals pay higher costs than younger ones when faced with a challenge to their immune system. Our results also suggest that these costs are mediated by an exaggerated sickness behavior, as seen in laboratory models, and can be modulated by ecological factors such as weather conditions and food availability. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
acute phase response, bacterial killing, disease, ecological, immunology, immunocompetence, lipopolysaccharide, lysozyme, senescence, sickness behavior
in
Ecology
volume
92
issue
4
pages
952 - 966
publisher
Ecological Society of America
external identifiers
  • wos:000290533700016
  • scopus:79955651817
ISSN
0012-9658
DOI
10.1890/10-0662.1
language
English
LU publication?
yes
id
9f1fa3f3-c997-4644-8e13-5999eba8a51a (old id 1986881)
date added to LUP
2011-06-29 09:53:07
date last changed
2017-09-17 05:54:14
@article{9f1fa3f3-c997-4644-8e13-5999eba8a51a,
  abstract     = {Immunosenescence, the aging of the immune system, is well documented in humans and laboratory models and is known to increase infection risk, morbidity, and mortality among the old. Immunosenescence patterns have recently been unveiled in various free-living populations, but their consequences in the wild have not been explored. We investigated the consequences of immunosenescence in free-living Tree Swallows Tachycineta bicolor through a field experiment simulating a bacterial infection (challenge with lipopolysaccharide, LPS) in females of different ages during the nestling rearing period. We assessed behavioral and physiological responses of females, as well as growth and quality of their offspring, to determine the costs associated with the simulated infection. Results of the experiment differed between the two years of study. In the first year, old females challenged with LPS lost more body mass and reduced their nest visitation rates more, and their offspring tended to grow slower compared to similarly challenged younger females. In contrast, in the second year, old females did not appear to suffer larger costs than younger ones. Interestingly, immunosenescence was only detected during the first year of the study, suggesting that it is the dysregulated immune function characteristic of immunosenescent individuals rather than age per se that can lead to higher costs of immune defense in old individuals. These results provide the first evidence of costs of immunosenescence in free-living animals and support the hypothesis that old, immunosenescent individuals pay higher costs than younger ones when faced with a challenge to their immune system. Our results also suggest that these costs are mediated by an exaggerated sickness behavior, as seen in laboratory models, and can be modulated by ecological factors such as weather conditions and food availability.},
  author       = {Palacios, Maria G. and Winkler, David W. and Klasing, Kirk C. and Hasselquist, Dennis and Vleck, Carol M.},
  issn         = {0012-9658},
  keyword      = {acute phase response,bacterial killing,disease,ecological,immunology,immunocompetence,lipopolysaccharide,lysozyme,senescence,sickness behavior},
  language     = {eng},
  number       = {4},
  pages        = {952--966},
  publisher    = {Ecological Society of America},
  series       = {Ecology},
  title        = {Consequences of immune system aging in nature: a study of immunosenescence costs in free-living Tree Swallows},
  url          = {http://dx.doi.org/10.1890/10-0662.1},
  volume       = {92},
  year         = {2011},
}