Musth as a handicap Immune suppression by testosterone

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The innovative biologist Amotz Zahavi proposed in 1975 a novel hypothesis to explain the evolution of exaggerated male secondary sexual characters. At first glance, some of these, such as the peacock's gorgeous train of feathers, do not seem to serve any purpose beyond merely displaying to potential mates. Indeed, these actually seem to draw the attention of predators and directly impair the ability of males possessing these to escape from a predator. Charles Darwin devoted a whole book to this paradox, extensively documenting examples from the animal kingdom. Darwin recognized that "these characters are the result of sexual and not of ordinary [i.e., natural] selection" (1871, Vol. I, p. 258). In other words, such male characters can be attributed solely to female mating preferences.

For several decades, not much thought was given to this problem until, in 1958, mathematician Ronald Fisher reasoned using genetical theory that initially the evolution of a female mating preference should have a reproductive advantage, but later could proceed purely through sexual selection even if any advantage through natural selection has ceased. The process of an increasingly exaggerated male secondary dimorphism is termed runaway sexual selection. Biologists have pondered how such male traits could evolve purely through female choice in the absence of any inherent male genetic quality linked to these traits.

Zahavi's explanation was that female preference for what seems to be a handicap in a male has evolved precisely because of the handicap. A male possessing an exaggerated secondary trait has after all survived in spite of this "handicap" and is therefore demonstrating his inherent vigor and quality. Known as the handicap principle, this explanation has been applied to a variety of puzzling biological phenomena, including sexual dimorphisms, patterns of animal coloration, alarm signals, and "dangerous" behaviors. Related theories linking the evolution of sexual secondary traits with parasitism and disease have also been much debated, and I apply these to sexual selection in elephants.

As discussed, musth is an expensive proposition for male elephants in terms of the physiological costs involved. By the end of the musth period, the bull is in poor body condition. To that extent, a bull is "handicapped" by going through musth. There is, however, a much more serious handicap that a bull suffers when it is in musth, an aspect that has been overlooked by elephant biologists. The high levels of the major androgen, testosterone, associated with musth (or the development of secondary sexual characters, for that matter) also seriously impair the functioning of the immune system, exposing the male to debilitating parasitism and disease.

W. J. Freeland was possibly the first to suggest that female choice of mates (in primates) may be influenced by the parasitic burden of males, and that females could even incite male-male competition to identify fitter males. This idea was independently elaborated by William Hamilton and Marlene Zuk to implicate the role of parasites in the evolution of extreme male ornamentation. They suggested that male secondary sexual characters allow females to appraise the male's ability to resist parasites (the word parasites is used in the broader sense to include diseases). By preferring males with exaggerated traits, the female ensures "good genes" for her offspring, in terms of parasite resistance, assuming that the trait is heritable. Unlike earlier good gene hypotheses, however, the resistance gene will be changing since the parasites are also evolving; thus, the system remains dynamic and maintains the importance of female choice.

While Hamilton and Zuk recognized their hypothesis to be a variation of the handicap principle, Ivan Folstad and Andrew Karter went a step further in more formally linking the parasite-male handicap idea with the immunocom-petence burden. The differences between males and females in hormone profiles need not be elaborated here. These hormonal differences may translate into differences in immune response between the sexes. Typically, the male shows weaker immune response to several antigens than do females. High levels of testosterone, vital to the development of male secondary sexual traits, reduce the immunity of the individual. The physiological interplay of testosterone and the immune system is complex, involving various organs, tissues, and cell types. Testosterone may reduce immunity through shrinkage of the thymus gland and other lymphoid tissue and through humoral and cell-mediated immunity.

Reduced immunity would thus make the individual more susceptible to parasitism. A male elephant in musth, surging with testosterone, is thus advertising a considerable handicap to estrous females. It is also signaling that it can shoulder this immunocompetence burden during the musth period. Thus, musth can again be thought of as an honest signal of male genetic quality.

While there is some empirical evidence from several mammal species for the Folstad-Karter scenarios, hardly any work has been done on this aspect in elephants. However, Milind Watve and I have looked at a related aspect of this issue—that of tusk length and parasite loads in Asian elephants. In the course of this work, we found that the highest recorded level of fecally dispersed parasite loads was from a bull in musth. I discuss this work in greater detail in the next section.

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