Ectoparasitism in Mothers Causes Higher Positional Fluctuating Asymmetry in Their Sons: Implications for Sexual Selection

Abstract

Random deviations from perfect bilateral symmetry, fluctuating asymmetry, arise from developmental instability. I tested experimentally whether parasitism in female Drosophila nigrospiracula increases fluctuating asymmetry in male offspring. I also developed a novel measure for estimating developmental instability in a meristic trait called positional fluctuating asymmetry, which is based on the difference in the position of thoracic bristles between the right and left sternopleuron. I expected this measure to be a more sensitive indicator of developmental instability than the traditional numerical fluctuating asymmetry, because the latter is based on the difference in the actual presence or absence of bristles. Female flies burdened with hematophagous mites, Macrocheles subbadius (Macrochelidae), produced sons with significantly higher positional fluctuating asymmetry than did females carrying no mites. This effect, which may have resulted from impaired provisioning of oocytes by infested females, was dose dependent and magnified in the progeny of younger (18-20 d) versus older (30-32 d) females. This apparent magnification resulted from a slight but not significant increase in asymmetry of offspring of the older and unparasitized females. In contrast, the same mite loads had no effect on offspring numerical fluctuating asymmetry. If low-positional fluctuating asymmetry males enjoy a mating advantage, then with appropriate genetic variability, sexual selection could drive the evolution of host resistance in host populations. However, variability in neither kind of asymmetry influenced male mating success in nature. Thus, although male positional fluctuating asymmetry is causally associated with parasitism via maternal effects, asymmetry-based sexual selection is unlikely to influence the evolution of mite resistance in D. nigrospiracula. The value of the sensitivity afforded by positional fluctuating asymmetry is discussed in the context of sexual selection and conservation biology.