MHC Genotype and Ornamentation

Differences among males in immunocompetence can affect resistance to parasites and diseases, and sexual ornaments have been suggested to function as indicators of additive genetic variation in disease resistance, health and condition in the good gene models of sexual selection. In this paper the role of genetic variation in the immune system is discussed as an alternative route to explore whether or not immunological variation influences condition and sexual ornamentation. In vertebrates, the effect of the genes located in the major histocompatibility complex (MHC) in shaping immunodominance, lasting immunity, and the risk of developing pathological immune responses are suggested as the link between genetic variation at the MHC and male ornaments. It is also suggested that general immune responsiveness may be optimized at an individual basis depending on the MHC associated risk of autoimmune disorders. 323 IN: ES P M A R K,Y. , AM U N D S E N,T. & RO S E N Q V I S T,G. (ED S.) 1999. AN I M A L SI G N A L S. SI G N A L L I N G A N D SI G N A L DE S I G N I N AN I M A L CO M M U N I C A T I O N. TH E RO Y A L NO R W E G I A N SO C I E T Y O F SC I E N C E S A N D LE T T E R S, TH E FO U N D A T I O N TA P I R PU B L I S H E R S, TR O N D H E I M, NO R W A Y The expression of ornaments is highly variable among males within a species and can also differ both between and within seasons for individual males. The variation in ornaments is often correlated with condition and survival (canine teeth in primates: Manning & Chamberlain 1993; carotenoid pigmentation in fish and birds: Milinski & Bakker 1990; Hill 1990, 1991; Niccoletto 1993; combs in red jungle fowl Gallus gallus: Zuk et al. 1990; see also a general review by Andersson 1994). Theoretical models have suggested that the intensity of male ornaments and displays are used by the females in many animal species through behaviours and other adaptations aimed at picking out high quality males to sire their young (Zahavi 1975, 1977; Andersson 1982, 1986, 1994; Hamilton & Zuk 1982; Kodric-Brown & Brown 1984). By basing mate choice on the information displayed by the males, a female can increase the quality, viability, and future reproductive success of her offspring even in the absence of non-genetic direct benefits (Pomiankowski & Møller 1995; see also Kirkpatrick & Ryan 1991). Studies of animals, from vertebrates to insects, in the lab and the wild support the concept of honest indicators of good genes by showing that females indeed can increase offspring fitness by mating with more ornamented males (Norris 1993; Møller 1994; von Schantz et al. 1994; Hasselquist et al. 1996; Welch et al. 1998; Hoikkala et al. 1998). In search of the link between ornamentation and condition of males, controlled infection experiments have shown that ornaments are sensitive to diseases (Houde & Torio 1992) even more so than other morphological traits (Hillgarth 1990; Zuk et al. 1990). Several different methods have been used to evaluate an individual’s capacity to control infections. Antibody response to novel or familiar antigens, levels of serum globulin, size of immune organs and lymphocyte counts have all been used to estimate variation in immunocompetence. From an immunological perspective it is not always evident that these assays accurately reflect individual variation in immunocompetence and how these estimates relates to variation in fitness (Sheldon & Verhulst 1996; Penn & Potts 1998). The emerging picture is less than clear: more ornamented males have been interpreted to show weaker responses to pathogens, as measured by counts of white blood cells (Zuk et al. 1995; Skarstein & Folstad 1996) but stronger immune reaction to novel antigens when assayed with delayed hypersensitivity tests (Zuk & Johnsen 1998) or total immunoglobulin response (Sanio & Møller 1996). A major problem when exploring the connection between variation in disease resistance and ornamentation comes from the observation that immune function and disease resistance is itself dependent on condition. Individuals with a poor immune system will be in poor condition but it is equally true that individuals in poor condition will have a weakened immune system (Lord et al. 1998). Hence, the causality works in both directions and firm evidence that link disease resistance and ornamentation, independently of an underlying correlation to general condition, can be difficult to establish by exploring the relationship between quantitative variables of the immune system and ornamentation (Fig. 1).