Effects of Coccidial and Mycoplasmal Infections on Carotenoid-based Plumage Pigmentation in Male House Finches

—Carotenoid pigments produce the ornamental red, orange, and yellow integumentary coloration of many species of animals. Among individuals of a population, the hue and saturation of carotenoid-based ornaments can be extremely variable, and studies of fish and birds have shown that females generally prefer males that display the most saturated and reddest coloration. Consequently, there has been a great deal of interest in determining the proximate factors that affect individual expression of carotenoid-based pigmentation. Parasites might affect production of ornamental coloration, and the Hamilton-Zuk hypothesis proposes that parasitized males will show decreased expression of the secondary sexual traits preferred by females. We found that captive male House Finches (Carpodacus mexicanus) experimentally infected with Isospora spp. (coccidians) and/or Mycoplasma gallisepticum produced carotenoid-based plumage coloration that was significantly less red and less saturated than that of noninfected males. These observations validate a necessary condition of the Hamilton-Zuk hypothesis, but heritable resistance to the pathogens we examined remains to be demonstrated. Received 6 July 1999, accepted 27 April 2000. HAMILTON AND ZUK (1982) proposed that secondary sexual characteristics evolved because they serve as reliable indicators of heritable resistance to parasites and disease. According to their hypothesis, only resistant males with low parasite loads can produce the most exaggerated and costly sexual ornamentation. Males with high parasite loads show reduced expression of their sexual ornaments. Consequently, by choosing to mate with a highly ornamented male, a female receives benefits for her offspring in the form of genes for parasite resistance. The Hamilton-Zuk hypothesis makes two predictions concerning the relationship between parasitic infections and secondary sexual characteristics: (1) species that are most subject to infection should have more developed and/or conspicuous secondary sexual traits (brighter coloration, more elaborate plumage, etc.); (2) within species, preferred mates should be the least parasitized. Here, we present a test of the second, or intraspecific, prediction of the hypothesis. For the Hamilton-Zuk hypothesis to work within a species, three critical predictions must be met: (1) the degree of development of sec1 Address correspondence to this author. E-mail: [email protected] ondary sexual characteristics should be related to the intensity of parasitic infection; (2) females should base their choice of mates on expression of the ornamental trait that is correlated with parasitism; and (3) resistance to the parasite must be heritable (McLennan and Brooks 1991). Møller (1988, 1990) has provided the best support for the hypothesis by finding that each of these requirements was satisfied in a host-parasite relationship involving Barn Swallows (Hirundo rustica) and hematophagous mites (Ornithonyssus bursa). Other studies have shown that at least two of the three requirements are met in a variety of host-parasite relationships (see Hamilton and Poulin 1997). One of the most widespread ornamental traits in animals is carotenoid-based coloration of the integument. Animals cannot produce carotenoids and must acquire these pigments in their diet (Goodwin 1984). Because carotenoids must be obtained from the environment, carotenoid pigmentation is likely to be affected by environmental factors such as parasites; indeed, the intensity of infection by various parasites is negatively related to display of carotenoid-based ornamental coloration in some birds and fishes (e.g. Milinski and Bakker 1990, Houde and Torio 1992, Thompson et al. 1997, Merilä et al. 1999). No specific mechanism has been proposed October 2000] 953 Parasites and Plumage Redness for how a parasitic infection depresses the expression of carotenoid pigmentation. According to Brush (1978), carotenoid pigmentation involves four main steps: absorption, transport, metabolism, and deposition. The process of absorption may be particularly susceptible to the effects of parasitic infection. Several intestinal parasites have been shown (either by direct measurement of carotenoid levels in serum and tissue, or by observation of carotenoid-based ornaments) to reduce absorption of dietary carotenoids (Ruff et al. 1974; Allen 1986, 1992; Tyczkowski et al. 1991). The conversion of yellow pigments to red pigments, as well as other processes involved in the metabolism of carotenoids, appears to be energetically costly (Hill 1996, 2000). Individuals that expend energy fighting parasite infestations may not be able to allocate as much energy to the metabolism or transport of pigments used in sexual displays (see Hill 2000). Infection also may lead to decreased energy expenditure on foraging so that fewer carotenoids are ingested. The initial objective of our study was to assess the effects of coccidial infections on the carotenoid-based plumage pigmentation of male House Finches (Carpodacus mexicanus). Because of an epidemic of Mycoplasma gallisepticum among House Finches (Nolan et al. 1998), M. gallisepticum was inadvertently introduced into the experimental groups in both years of the study. This also allowed us to assess the effects of mycoplasmosis (which causes severe conjunctivitis in House Finches) on expression of carotenoid-based plumage coloration. We predicted that male finches with coccidial and/or mycoplasmal infections would show decreased plumage redness compared with uninfected males.