Is There an Immunological Cost to Carotenoid-Based Ornamental Coloration?

Originally it was proposed that dietary access alone might explain variation in expression of carotenoid pigmentation (Endler 1980; Kodric-Brown 1985; Hill 1990). By this idea, carotenoids are scarce in the environment, and only those individuals in the best condition gain access to sufficient carotenoids for maximum ornament display. To this idea of limited access was added the idea that parasites might negatively impact expression of carotenoid pigmentation (Milinski and Bakker 1990; Houde and Torio 1992; Zuk 1992). Indeed, from studies with poultry it is well established that coccidia (protozoan gut parasites) directly inhibit carotenoid absorption (Ruff et al. 1974; Augustine and Ruff 1983; Allen 1987, 1992; Tyczkowski et al. 1991). In several studies with species that have carotenoid-based ornamental display, it has been shown that parasites, including particularly coccidia, inhibit expression of carotenoid pigmentation (Milinski and Bakker 1990; Houde and Torio 1992; Brawner 1997; Thompson et al. 1997). It seems likely that parasite load and limited access to dietary carotenoids combine to determine color expression in many species of animals (Hill 1999). Carotenoids are used for more than integumentary colorants in animals. Some carotenoids, particularly betacarotene and related molecules, function as vitamin A precursors (Bauernfeind 1972). In addition, a variety of carotenoids, including both carotenoids that serve as vitamin A precursors and carotenoids that do not serve as vitamin A precursors, have been found to reduce the risk of infection in mammals (Bendich 1989, 1993, 1996; Chew 1993) and help prevent the onset of cancer (Peto et al. 1981; Krinsky 1989; Ziegler 1989). Both of these immu-