XV.188.8.131.52 The indicator hypothesis of the level of infestation by parasites does not take the parasite’s evolutionary countermoves into consideration
A fundamental drawback of the indicator hypothesis of the level of infestation by parasites is that it completely ignores the fact that the parasite is also an object of biological evolution. It cannot be expected that the evolution of the parasite will “helplessly watch” how the host organism creates a defense against effective spreading of parasites from one individual to another. The selection pressures of the host organism on the parasite are certainly more intense than the selection pressures of the parasite on the host (if only because not every individual of the host species encounters the particular parasite during its lifetime, while every parasite must find a host or otherwise does not leave behind any offspring). Thus, it can be expected that the parasite would rapidly form counter-mechanisms through which it would either reduce the manifestations of its presence on the degree of expression of the secondary sexual trait or would even learn to positively influence the expression of these traits. Because of the extreme advantageousness of such a mechanism for the parasite and the extraordinary speed of evolution in parasitic species, it can be expected that the degree of expression of secondary sexual traits in some species will be positively correlated with the level of infestation of the given individual by parasites.
The published results so far indicate that similar situations could occur, for example, in zebra birds (Taeniopygia guttata guttata), in which the intensity of the red beak color is positively correlated with the number of parasites mites and lice (Burley, Tidemann, & Halupka 1991). Further, similar results were obtained for Sceloporus occidentalis lizards infested by protozoa of the Plasmodium genus (Ressel & Schall 1989)and amongst Papio cynocephalus baboons infected by various species of helminths (Hausfater & Watson 1976). However, one difficulty must be pointed out in this connection. The degree of expression of secondary sexual traits is frequently related to the level of sex hormones and these sex hormones frequently negatively affect the functioning of the immune system. Consequently, any positive correlation between the degree of infestation by parasites and the degree of expression of secondary sexual traits may be caused, not by the action of the parasite, but by the joint action of sex hormones on immunity against parasites and expression of secondary sexual traits. Amongst other things, this possibility formed a basis for the immunocompetence handicap hypothesis, which assumes that correlation of the level of sex hormones with the degree of expression of secondary sexual traits and simultaneously with the damage to the immune system facilitates long-term functioning of the system of identification of good-quality males on the basis of the level of expression of secondary sexual traits (Folstad & Karter 1992). Reduction of the functioning of the immune system constitutes a real handicap, reducing his viability, for a male with fully developed secondary sexual traits. This ensures that this signal cannot be falsified and only really good-quality males can permit (can survive) damage to the immune system following from an elevated level of sex hormones.
In birds, it should theoretically be possible to decide between the two possible causes of greater occurrence of parasites in males with maximum expression of secondary sexual traits, i.e. the action of parasites vs. the damage to the immune system by sex hormones, because here the level of expression of some (secondary) sexual traits, such as coloration and feather length, is determined by the absence of female sex hormones and not the presence of male hormones.s