Abstract
Illnesses caused by a variety of micro- and macro- organisms can negatively affect individuals’ fitness, leading to the expectation that immunity is under positive selection. However, immune responses are costly and individuals must trade-off their immune response with other fitness components (e.g. survival or reproductive success) meaning that individuals with intermediate response may have the greatest overall fitness. Such a process might be particularly acute in species with strong sexual selection because the condition-dependence of male secondary sexual-traits might lead to striking phenotypic differences amongst males of different immune response levels. We tested whether there is selection on immune response by survival and reproduction in yearling and adult male black grouse (Lyrurus tetrix) following an immune challenge with a novel antigen and tested the hypothesis that sexual signals and body mass are honest signals of the immune response. We show that yearling males with highest immune response to these challenges had higher survival, but the reverse was true for adults. Adults with higher responses had highest mass loss and adult males with intermediate immune response had highest mating success. Tail length was related to baseline response in adults and more weakly in yearlings. Our findings reveal the complex fitness consequences of mounting an immune response across age classes. Such major differences in the direction and magnitude of selection in multiple fitness components is an alternative route underpinning the stabilising selection of immune responses with an intermediate immune response being optimal.
Highlights
Within natural populations, individuals are constantly exposed to parasitic organisms that can have significant detrimental effects on their fitness (Poulin 2007)
For yearling and adult males, no phenotypic trait was significantly related to peak antibody response (Table 1), but in both cases the relationship with tail length tended to be positive in yearlings and adult males (Table 1)
We showed that adult males had a decline in body mass while mounting their immune response and this was associated with reduced survival; this suggesting that the energetic costs may partly cause the fitness costs we observed in adult males
Summary
Individuals are constantly exposed to parasitic organisms that can have significant detrimental effects on their fitness (Poulin 2007). Infection and damage by parasites may be resisted by mounting an immune response, and so immune responses should be under positive directional selection (Råberg et al 2000). Mounting an immune response is complex as there are Communicated by Nicolas Lecomte. Oecologia (2018) 186:405–414 response is expected to be under stabilising selection with an intermediate response that manages or balances resistance versus tolerance, but does not necessarily eliminate, infection being optimal (Viney et al 2005; Stjernman et al 2008; Råberg et al 2009; Graham et al 2010). A key fitness component is the ability of males to attract mates. In addition to survival (i.e. natural selection), mating success (i.e. sexual selection) may have a significant role in driving optimal immune response
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