Aging in personal and social immunity: do immune traits senesce at the same rate?

• Published in: Ecology and evolution 2015-10, Vol.5 (19), p.4365-4375
• Main Authors: Reavey, Catherine E., Warnock, Neil D., Garbett, Amy P., Cotter, Sheena C.
• Format: Article
• Language: English
• Subjects: Age; Aging; Animal breeding; Antimicrobial agents; Bees; Beetles; Breeding; Breeding status; Coleoptera; defensin; ecological immunology; Fitness; Genes; Immune response; Immune system; Immunity; insect; Insects; Investment policy; Life span; lifespan; lysozyme; Mortality; Nicrophorus; Offspring; Original Research; parental care; Phenoloxidase; Physiology; Senescence; Studies; Survival; Wounding
• ISSN: 2045-7758; 2045-7758
• DOI: 10.1002/ece3.1668

Summary How much should an individual invest in immunity as it grows older? Immunity is costly and its value is likely to change across an organism's lifespan. A limited number of studies have focused on how personal immune investment changes with age in insects, but we do not know how social immunity, immune responses that protect kin, changes across lifespan, or how resources are divided between these two arms of the immune response. In this study, both personal and social immune functions are considered in the burying beetle, Nicrophorus vespilloides. We show that personal immune function declines (phenoloxidase levels) or is maintained (defensin expression) across lifespan in nonbreeding beetles but is maintained (phenoloxidase levels) or even upregulated (defensin expression) in breeding individuals. In contrast, social immunity increases in breeding burying beetles up to middle age, before decreasing in old age. Social immunity is not affected by a wounding challenge across lifespan, whereas personal immunity, through PO, is upregulated following wounding to a similar extent across lifespan. Personal immune function may be prioritized in younger individuals in order to ensure survival until reproductive maturity. If not breeding, this may then drop off in later life as state declines. As burying beetles are ephemeral breeders, breeding opportunities in later life may be rare. When allowed to breed, beetles may therefore invest heavily in “staying alive” in order to complete what could potentially be their final reproductive opportunity. As parental care is important for the survival and growth of offspring in this genus, staying alive to provide care behaviors will clearly have fitness payoffs. This study shows that all immune traits do not senesce at the same rate. In fact, the patterns observed depend upon the immune traits measured and the breeding status of the individual. Multiple immune responses have evolved to protect the individual (personal) or their kin (social). Several studies have considered how personal immunity changes with age, but this is the first study to consider how social immunity changes with age. We found that in virgins, personal immunity declined or was maintained with age, while in breeders, it was maintained or even increased with age. Social immunity increased to middle age before falling in old age. We discuss the potential reasons for these differing responses to aging.