Immunosenescence in some but not all immune components in a free-living vertebrate, the tree swallow

Abstract

A wide diversity of free-living organisms show increases in mortality rates and/or decreases in reproductive success with advancing age. However, the physiological mechanisms underlying these demographic patterns of senescence are poorly understood. Immunosenescence, the age-related deterioration of immune function, is well documented in humans and laboratory models, and often leads to increased morbidity and mortality due to disease. However, we know very little about immunosenescence in free-living organisms. Here, we studied immunosenescence in a free-living population of tree swallows, Tachycineta bicolor, assessing three components of the immune system and using both in vivo and in vitro immunological tests. Immune function in tree swallow females showed a complex pattern with age; acquired T-cell mediated immunity declined with age, but neither acquired nor innate humoral immunity did. In vitro lymphocyte proliferation stimulated by T-cell mitogens decreased with age, suggesting that reduced T-cell function might be one mechanism underlying the immunosenescence pattern of in vivo cell-mediated response recently described for this same population. Our results provide the most thorough description of immunosenescence patterns and mechanisms in a free-living vertebrate population to date. Future research should focus on the ecological implications of immunosenescence and the potential causes of variation in patterns among species.

Complex Interplay of Body Condition, Life History, and Prevailing Environment Shapes Immune Defenses of Garter Snakes in the Wild

“…Here we used a wholeblood mitogenic stimulation assay that does not require terminal sampling (Palacios et al 2007) and that we adapted for use in free-living garter snakes. Parameters reported here provided optimal proliferation responses for garter snake blood in preliminary trial analyses (refer to the appendix in the online edition of Physiological and Biochemical Zoology for information on assay optimization).…”

“…Activation and proliferation of lymphocytes are critical initial steps of acquired immune responses-both cellular, mediated by cytotoxic T-lymphocytes, and humoral, mediated by B-lymphocytes and helper T-lymphocytes-leading to the formation of clones of cells that can more effectively fight the invader (Roitt et al 1998). In vitro lymphocyte proliferation assays are widely employed by immunologists and immunotoxicologists (Froebel et al 1999;Grasman 2002;Fairbrother et al 2004) and can provide val-Immune Defense Strategies of Garter Snakes in the Wild 549 uable insights into the immune function of free-living animals (Palacios et al 2007.…”

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

“…(2) Most studies to date have focused on a single immune defense component, either acquired cell-mediated, acquired humoral, or innate humoral immunity. More integrative studies that incorporate various aspects of immune defense (e.g., Palacios et al 2007) would help us understand the patterns of immune system aging, including whether decline in one component might be somewhat compensated by increase in a different one. (3) Declines in each of the major immune defense components have been documented in at least one wild population to date, while an increase with age has never been reported.…”

“…(4) Immune function involving T-lymphocytes seems to be the most pervasively affected by age in free-living vertebrates, which is consistent with patterns of immunosenescence in humans and laboratory models (Pawelec et al 2002), while acquired and innate humoral components show signs of senescence in some but not all free-living species studied to date. (5) Based on the study in Tree Swallows (Palacios et al 2007), it appears that not all immune defense components are equally affected by age in a given species. While some components seem to decline, others seem to be well preserved into old age.…”

Capture and blood sampling do not affect foraging behaviour, breeding success and return rate of a large seabird: the black-browed albatross

“…In this respect, many eco-physiological studies of vertebrates are based on the collection of blood because it can provide useful information without requiring prolonged restraint, surgery or killing of a wild animal. Thus, immune, metabolic, endocrine, isotopic and toxicological processes in birds are usually studied by performing blood analyses (e.g., Landys et al 2005;Angelier et al 2007a;Palacios et al 2007;Wada et al 2009). Moreover, red cells are nucleated in birds and can therefore be used for genetic purposes such as sex determination, paternity or ageing processes (e.g., Fridolfsson and Ellegren 1999;Schmoll et al 2009;Bize et al 2009).…”