Alternative hypotheses linking the immune system and mate choice for good genes

Why do males often have extravagant morphological and behavioural traits, and why do females prefer to mate with such males? The answers have been the focus of considerable debate since Darwin's 'The descent of man, and selection in relation to sex' appeared in 1871. Recently, the broadening of investigation to include fields outside evolutionary biology has shed new light on mate choice and sexual selection. Here, we focus on a specific set of hypotheses relating the biology of resisting disease-causing organisms with the production of condition-dependent sexual signals (advertisements). We present a framework that distinguishes three different hypotheses about trade-offs within the immune system that affect general condition. The original Hamilton & Zuk hypothesis suggests that hosts fight off disease via resistance to particular pathogens, which lowers resistance to other pathogens. Changes in pathogens over evolutionary time in turn favours changes in which genes confer the best resistance. Alternatively, the immunocompetence hypotheses suggest that the energetic costs of mounting a response to any pathogen compete for resources with other things, such as producing or maintaining advertisements. Finally, improving resistance to pathogens could increase the negative impacts of the immune system on the host, via immunopathologies such as allergies or autoimmune diseases. If both disease and immunopathology affect condition, then sexual advertisements could signal a balance between the two. Studies of hypothesized links between genes, condition, the immune system and advertisements will require careful consideration of which hypothesis is being considered, and may necessitate different measures of immune system responses and different experimental protocols.