Abstract
Immunosenescence, the deterioration of immune system capability with age, may play a key role in mediating age-related declines in whole-organism performance, but the mechanisms that underpin immunosenescence are poorly understood. Biomedical research on humans and laboratory models has documented age and disease related declines in the telomere lengths of leukocytes (‘immune cells’), stimulating interest their having a potentially general role in the emergence of immunosenescent phenotypes. However, it is unknown whether such observations generalise to the immune cell populations of wild vertebrates living under ecologically realistic conditions. Here we examine longitudinal changes in the mean telomere lengths of immune cells in wild European badgers (Meles meles). Our findings provide the first evidence of within-individual age-related declines in immune cell telomere lengths in a wild vertebrate. That the rate of age-related decline in telomere length appears to be steeper within individuals than at the overall population level raises the possibility that individuals with short immune cell telomeres and/or higher rates of immune cell telomere attrition may be selectively lost from this population. We also report evidence suggestive of associations between immune cell telomere length and bovine tuberculosis infection status, with individuals detected at the most advanced stage of infection tending to have shorter immune cell telomeres than disease positive individuals. While male European badgers are larger and show higher rates of annual mortality than females, we found no evidence of a sex difference in either mean telomere length or the average rate of within-individual telomere attrition with age. Our findings lend support to the view that age-related declines in the telomere lengths of immune cells may provide one potentially general mechanism underpinning age-related declines in immunocompetence in natural populations.
Highlights
Immunosenescence is the gradual deterioration of immune system capability with age, and may be a major factor influencing age-related declines in whole-organism performance [1]
We found no statistical support for quadratic age effects or an interaction between mean age and D age, suggesting that the rate of change in mean immune cell telomere length does not change with age
Our findings strongly suggest that the age-related declines in immune cell telomere length observed in humans and laboratory models are mirrored by comparable relationships in this population of wild mammals
Summary
Immunosenescence is the gradual deterioration of immune system capability with age, and may be a major factor influencing age-related declines in whole-organism performance [1]. This research has led to the suggestion that age-related declines in immune cell telomere lengths may contribute to the immunosenescence-related health declines previously documented in humans and wild vertebrates [6]. Studies of wild birds have frequently documented agerelated declines in the telomere lengths of nucleated erythrocytes (red blood cells) [7,8 but see 4], which share the same haematopoietic stem cell precursors as immune cells. Despite growing evidence of immunosenescence in wild vertebrate populations [9], it has yet to be investigated whether such agerelated declines in telomere length occur in the immune cell populations of wild vertebrates
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