Abstract
Animal immune systems change dramatically during the ageing process, often accompanied by major increases in pathogen susceptibility. However, the extent to which senescent elevations in infection mortality are causally driven by deteriorations in canonical systemic immune processes is unclear. We studied Drosophila melanogaster and compared the relative contributions of impaired systemic immune defences and deteriorating barrier defences to increased pathogen susceptibility in aged flies. To assess senescent changes in systemic immune response efficacy we injected one and four-week old flies with the entomopathogenic fungus Beauveria bassiana and studied subsequent mortality; whereas to include the role of barrier defences we infected flies by dusting the cuticle with fungal spores. We show that the processes underlying pathogen defence senescence differ between males and females. Both sexes became more susceptible to infection as they aged. However, we conclude that for males, this was principally due to deterioration in barrier defences, whereas for females systemic immune defence senescence was mainly responsible. We discuss the potential roles of sex-specific selection on the immune system and behavioural variation between males and females in driving these different senescent trends.
Highlights
Advanced age is often accompanied by increased infection burden[1]
Explicit comparisons of immunosenescent processes in males and females are rare outside humans. We addressed this by investigating whether the relative rates of barrier defence senescence and systemic immune senescence differ between the two sexes in D. melanogaster
Rather than solely studying the outcome of infection as the proportion of flies that survived until a single time point, we used survival analysis to investigate mortality risk variation across the whole dataset for the full experiment time course (Fig. 2), testing whether the entire pattern of post-infection mortality supported these trends. This alternative analysis approach verified that averaging across all infected treatments older flies died at psae f=naes 0tsec.1re5nra)c,teewophfoipsltas-ttihnfoofegrcetmnioadnleetfshe,naancgeyebodeutenwpgeeeenrndfltiehenset(tχdw1e2ot =einr 5ifo0er8cat.5itoi6on,npr o
Summary
Advanced age is often accompanied by increased infection burden[1]. Whilst many immunological processes show patterns of senescence[2], the extent to which changes in any individual immune parameter drive age-dependent elevations in infection susceptibility is often unclear. Explicit comparisons of immunosenescent processes in males and females are rare outside humans (but see refs 12–14) We addressed this by investigating whether the relative rates of barrier defence senescence and systemic immune senescence differ between the two sexes in D. melanogaster. We investigate how the ability of D. melanogaster flies to defend against infection by the entomopathogenic fungus Beauveria bassiana declines with age This fungus will naturally infect D. melanogaster: when spores contact the fly cuticle they germinate, penetrating this barrier defence before growing systemically in the haemocoel[27]. We assessed age-dependent changes in fly mortality following these two infection routes, testing the relative contribution of declines in barrier defences and systemic immune responses to overall senescence of pathogen protection. Our work demonstrates that the relative importance of senescence in these two pathogen defence systems differs strongly between males and females
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