Abstract
This study provides the first direct evidence from wild populations of stalk-eyed flies to support the hypothesis that male eyespan is a signal of meiotic drive. Several stalk-eyed fly species are known to exhibit X-linked meiotic drive. A recent quantitative trait locus analysis in Teleopsis dalmanni found a potential link between variation in male eyespan, a sexually selected ornamental trait, and the presence of meiotic drive. This was based on laboratory populations subject to artificial selection for male eyespan. In this study, we examined the association between microsatellite markers and levels of sex ratio bias (meiotic drive) in 12 wild T. dalmanni populations. We collected two data sets: (a) brood sex ratios of wild-caught males mated to standard laboratory females and (b) variation in a range of phenotypic traits associated with reproductive success of wild-caught males and females. In each case, we typed individuals for eight X-linked microsatellite markers, including several that previously were shown to be associated with male eyespan and meiotic drive. We found that one microsatellite marker was very strongly associated with meiotic drive, whereas a second showed a weaker association. We also found that, using both independent data sets, meiotic drive was strongly associated with male eyespan, with smaller eyespan males being associated with more female-biased broods. These results suggest that mate preference for exaggerated male eyespan allows females to avoid mating with males carrying the meiotic drive gene and is thus a potential mechanism for the maintenance and evolution of female mate preference.
Highlights
The majority of species have B1:1 offspring sex ratios
When ms395 allele sizes were split into two groups (above and below the mean (205 bp)) and compared with sex ratio bias, we found a significant association (w21 1⁄4 23.3450, N 1⁄4 29, Po0.0001)
We examined the relationship between meiotic drive, measured as sex ratio distortion of progeny, and a number of X-linked microsatellite loci (Wright et al, 2004; Johns et al, 2005)
Summary
The majority of species have B1:1 offspring sex ratios. A number of forces, including local mate competition and differential payoffs for the sexes against environmental gradients, can lead to well-characterised deviations from a balanced sex ratio (Hamilton, 1967). Selfish genetic elements further their interests in ways that result in the distortion of the normal offspring sex ratio. One common form of selfish genetic element is sex chromosome meiotic drive, usually linked to the X chromosome and active in the heterogametic sex in species with the XY sex-determination system (Hurst and Pomiankowski, 1991; Lyttle, 1993). Individuals that possess the driving X chromosome (XD) produce female-biased offspring sex ratios (Hamilton, 1967). This is typically due to differential sperm maturation or survival during spermatogenesis (Lyttle, 1993). The sperm of a number of species fail to undergo complete spermatid development and individualisation, leading to low survival among Y-bearing sperm and few male offspring, for example, in Drosophila melanogaster (Tokuyasu et al, 1972), Drosophila simulans (Montchamp-Moreau and Joly, 1997; Cazemajor et al, 2000) and Teleopsis whitei (formerly Cyrtodiopsis whitei) (Wilkinson and Sanchez, 2001)
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