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

Palacios, María G.; Winkler, David W.; Klasing, Kirk C.; Hasselquist, Dennis; Vleck, Carol M.

doi:10.1890/10-0662.1

Cited by 58 publications

(54 citation statements)

References 55 publications

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“…In mice, an age-associated decrease in antibody responses to Tindependent antigens, including LPS, has been reported (Chelvarajan et al, 2005). A similar result was found in a natural population of tree swallows (Tachycineta bicolor), where young and mid-age females injected with LPS mounted a specific antibody response, while the oldest individuals did not (Palacios et al, 2011).…”

Section: Introductionsupporting

confidence: 63%

Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle

Zimmerman

Clairardin

Paitz

et al. 2012

Journal of Experimental Biology

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SUMMARYAging is typically associated with a decrease in immune function. However, aging does not affect each branch of the immune system equally. Because of these varying effects of age on immune responses, aging could affect taxa differently based on how the particular taxon employs its resources towards different components of immune defense. An example of this is found in the humoral immune system. Specific responses tend to decrease with age while non-specific, natural antibody responses increase with age. Compared with mammals, reptiles of all ages have a slower and less robust humoral immune system. Therefore, they may invest more in non-specific responses and thus avoid the negative consequences of age on the immune system. We examined how the humoral immune system of reptiles is affected by aging and investigated the roles of non-specific, natural antibody responses and specific responses by examining several characteristics of antibodies against lipopolysaccharide (LPS) in the red-eared slider turtle. We found very little evidence of immunosenescence in the humoral immune system of the red-eared slider turtle, Trachemys scripta, which supports the idea that non-specific, natural antibody responses are an important line of defense in reptiles. Overall, this demonstrates that a taxonʼs immune strategy can influence how the immune system is affected by age.

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Section: Introductionsupporting

confidence: 63%

Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle

Zimmerman

Clairardin

Paitz

et al. 2012

Journal of Experimental Biology

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“…Variation in markers associated with immune function with age has been widely reported in wild vertebrates (Cichoń, Sendecka, & Gustafsson, 2003; Jego et al., 2014; Nussey, Watt, Pilkington, Zamoyska, & McNeilly, 2012; Palacios, Winkler, Klasing, Hasselquist, & Vleck, 2011). Notably, the structure and function of the thymus in mammals and in birds deteriorates remarkably early in life in many vertebrates and the output of naïve T cells may be greatly reduced by the time an individual reaches sexual maturity (Cockburn, 1992; Møller & Erritzøe, 2001).…”

Section: Introductionmentioning

confidence: 99%

Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival

Watson

McNeilly

Watt

et al. 2016

Ecology and Evolution

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Immune defenses are expected to be crucial for survival under the considerable parasite pressures experienced by wild animals. However, our understanding of the association between immunity and fitness in nature remains limited due to both the complexity of the vertebrate immune system and the often‐limited availability of immune reagents in nonmodel organisms. Here, we use methods and reagents developed by veterinary researchers for domestic ungulates on blood samples collected from a wild Soay sheep population, to evaluate an unusually broad panel of immune parameters. Our evaluation included different innate and acquired immune cell types as well as nematode parasite‐specific antibodies of different isotypes. We test how these markers correlate with one another, how they vary with age‐group and sex, and, crucially, whether they predict overwinter survival either within or among demographic groups. We found anticipated patterns of variation in markers with age, associated with immune development, and once these age trends were accounted for, correlations among our 11 immune markers were generally weak. We found that females had higher proportions of naïve T cells and gamma–delta T cells than males, independent of age, while our other markers did not differ between sexes. Only one of our 11 markers predicted overwinter survival: sheep with higher plasma levels of anti‐nematode IgG antibodies were significantly more likely to survive the subsequent high mortality winter, independent of age, sex, or weight. This supports a previous finding from this study system using a different set of samples and shows that circulating antibody levels against ecologically relevant parasites in natural systems represent an important parameter of immune function and may be under strong natural selection. Our data provide rare insights into patterns of variation among age‐ and sex groups in different T‐cell subsets and antibody levels in the wild, and suggest that certain types of immune response—notably those likely to be repeatable within individuals and linked to resistance to ecologically relevant parasites—may be most informative for research into the links between immunity and fitness under natural conditions.

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“…We found that LPS injection during the nestling period activated the immune system, increasing the bacterial-killing capacity of plasma of LPS-challenged birds compared to controls, although this innate immune response was independent of age. Older females (C4 years of age) who displayed reduced PHA skin-swelling, consistent with T cell-mediated immunosenescence, also showed exaggerated sickness behavior compared to younger birds (Palacios et al 2011). These older birds lost body mass and reduced their nest visitation rate compared to controls, whereas younger LPS-challenged birds did not differ from controls (Fig.…”

Section: Immunosenescencementioning

confidence: 84%

“…Immunosenescence has also been demonstrated in several other free-living avian species (reviewed in Palacios et al 2011) and is probably widespread among vertebrates. The fitness consequences of such immunosenescence in free-living birds and other animals, however, remain poorly understood.…”

Section: Immunosenescencementioning

confidence: 98%

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Evolutionary ecology of senescence: a case study using Tree Swallows, Tachycineta bicolor

Vleck

Palacios

2011

J Ornithol

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Tree Swallows, Tachycineta bicolor, have been studied at nest box colonies at sites throughout North America. They can be easily aged, captured, repeatedly sampled, and their physiology and reproductive success measured across their lifetime. These traits have made Tree Swallows an important model species for many ecological and evolutionary studies. We have studied aging in freeliving Tree Swallows colonies located in Iowa and New York, USA, for several years, and here we review what these studies are revealing about physiological attributes of senescence and their ecological and evolutionary consequences. Telomeres, the DNA ''caps'' on each chromosome, shorten with age, which may contribute to the senescing phenotype, and birds with longer telomeres at 1 year of age have a significantly longer predicted life span than birds with shorter telomeres. Tree Swallows display decreased cell-mediated immune function with age, but other components of the immune system do not decline with age. Older, nesting females who display immunosenescence also show exaggerated sickness behavior compared to younger birds in response to a simulated bacterial infection. Sickness behavior in old birds leads to loss of body condition and decreased parental behavior, suggesting that immunosenescence carries fitness costs in the wild.We are also carrying out an experimental test of the leading theory for aging-oxidative stress. Preliminary data from metabolically-handicapped Tree Swallows carrying an extra 5% of their body mass suggest birds may suffer increased oxidative damage and telomere shortening, reduced immune function, and lower reproductive success. Continued cross-sectional and longitudinal studying of Tree Swallows will enable us to distinguish between intrinsic change with age common to all birds and the results of selection on traits that affect survivorship and differ between individuals. Our results suggest continued work with Tree Swallows holds great promise to understand the evolutionary ecology of senescence in birds and other animals.

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

Cited by 58 publications

References 55 publications

Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle

Humoral immune responses are maintained with age in a long-lived ectotherm, the red-eared slider turtle

Cellular and humoral immunity in a wild mammal: Variation with age & sex and association with overwinter survival

Evolutionary ecology of senescence: a case study using Tree Swallows, Tachycineta bicolor

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