Folstad and Karter (7) recently proposed the immunocompetence handicap hypothesis as a general proximate mechanism to explain the costs of ornamentation; this hypothesis states that males carry ornaments at the expense of their resistance to disease and parasites. This tradeoff was originally hypothesized to arise as a consequence of the dual effect of androgens on ornamentation and immune function (higher androgen levels result in larger ornaments, but suppress immune function), but could also be the consequence of variation in resource allocation in the absence of direct effects of sex hormones (8).
The immunocompetence handicap hypothesis was based on a number of well established physiological relationships between condition, testosterone, sexual ornamentation, and the immune system, but when initially proposed, there were no studies that directly related immune function to sexual ornamentation (7). Since then, several attempts have been made to test this hypothesis by using different approaches. Some studies have manipulated testosterone levels (9–12) and studied the consequences for immune function or parasite burden. Although testosterone administration can be used to investigate the effects of this hormone on ornamentation and immune function, this experiment does not test directly whether there is a tradeoff between sexual ornamentation and immunocompetence. Other studies used natural variation to investigate the relationship between immune function and ornamentation and generally reported reduced immune function in individuals with larger or brighter ornaments (13–16). However, such correlations cannot be taken as evidence for a tradeoff between these traits, because reduced immune function in individuals with large ornaments could reflect reduced exposure to disease (for example, dominant individuals may succeed in foraging in patches with low parasite prevalence) or more efficient immune function in the past.
The demonstration of a tradeoff requires experiments in which a trait involved in the tradeoff is manipulated (17, 18). With respect to the immunocompetence hypothesis, one such study has been published, which reported reduced humoral immune function in male swallows Hirundo rustica with elongated tails (15) [tail length in swallows is a sexually selected trait (19)], suggesting a tradeoff between immunocompetence and sexual ornamentation. Here we report a study in which we use the converse approach, a manipulation of immune function, to test the immunocompetence handicap hypothesis. We compared comb size of domestic fowl Gallus domesticus between males belonging to lines divergently selected on their response to sheep erythrocytes (20). Domestic fowl is a suitable system to test this hypothesis, because the importance of comb size in inter- and intrasexual selection is well established (13, 21–23), and comb size is strongly dependent on testosterone level (13, 24, 25). Based on the immunocompetence handicap hypothesis, we predicted a negative association between immune function and comb size among selection lines. We restricted our analyses to the selection-line level, because we have no predictions for variation within selection lines, since this concerns spontaneous natural variation rather than experimental artificial variation (17, 26). For example, the immunocompetence handicap hypothesis predicts a negative relationship between comb size and immunocompetence, but within a line both comb size and immunocompetence are likely to be positively correlated with fitness and hence with each other. As a result of such a mixture of effects, negative, zero, or positive correlations can be found, but none of these would constitute evidence for or against the existence of a tradeoff. This point has been discussed at length in the life history literature (17, 18, 26–29) in the context of demonstration of the costs of reproduction (30).