Stabilising selection on immune response in male black grouse Lyrurus tetrix

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.

Keywords: ELISA; Ecological immunology; Immunocompetance; Life history theory; Stabilising selection.

Fig. 1

a Location of study sites (filled circles) in central Finland. 1: Köskenpaa, 2: Lehtosuo, 3: Teerisuo 4: Kummunsuo. 5: Valkeisuo; b an image of a male black grouse on the lek (photo by Gilbert Ludwig) and c timeline of the experiment carried out over 2002 and 2003. DT: Diphtheria-tetanus vaccination; DTL: Diphtheria-tetanus vaccination and levamisole treatment

Fig. 2

The relationship between (maximum lyre length (cm) and log tetanus antibody level at initial capture for adult males (solid points; N = 58) and yearling males (N = 58). The significant regression line for adult males is shown (y = 8.97 + 0.17x)

Fig. 3

Median ± IQR log peak antibody response level in relation to survival to the following year (died, survived) for a adult (N = 34) and yearling birds (N = 34) and b for territorial (N = 23 (9 died, 14 survived) and non-territorial (N = 11, 8 died, 3 survived) adult birds

Fig. 4

The a Change in mass (g) between initial capture and peak immune response in adults (solid points, solid regression line: y = 249.83 − 17.55x; N = 25) and yearlings (open points; N = 28) and b median ± IQR change in mass (g) of yearling (18 died, 10 survived) and older males (14 died, 11 survived) according to their survival rate to the following year

Fig. 5

The number of copulations in relation to log tetanus antibody level during the peak response (20–40 days) for adult birds (N = 25). The significant quadratic regression line is shown (solid line)