Genetic linkage between a sexually selected trait and X chromosome meiotic drive

Abstract

Previous studies on the stalk-eyed fly, Cyrtodiopsis dalmanni, have shown that males with long eye-stalks win contests and are preferred by females, and artificial selection on male relative eye span alters brood sex-ratios. Subsequent theory proposes that X-linked meiotic drive can catalyse the evolution of mate preferences when drive is linked to ornament genes. Here we test this prediction by mapping meiotic drive and quantitative trait loci (QTL) for eye span. To map QTL we genotyped 24 microsatellite loci using 1228 F2 flies from two crosses between lines selected for long or short eye span. The crosses differed by presence or absence of a drive X chromosome, X(D), in the parental male. Linkage analysis reveals that X(D) dramatically reduces recombination between X and X(D) chromosomes. In the X(D) cross, half of the F2 males carried the drive haplotype, produced partially elongated spermatids and female-biased broods, and had shorter eye span. The largest QTL mapped 1.3cM from drive on the X chromosome and explained 36% of the variation in male eye span while another QTL mapped to an autosomal region that suppresses drive. These results indicate that selfish genetic elements that distort the sex-ratio can influence the evolution of exaggerated traits.

Figure 1

Inverted images of (a) SR and (b) non-SR male spermatocyst bundles in the process of differentiating into 128 spermatids. DNA stained with Hoechst appears dark. Arrow points to non-elongated spermatid heads found in the majority of cysts from SR males. Bar indicates 50 μm. (c) Distribution of brood sex ratios for 59 F2 males. Open bars indicate males with SR cysts and filled bars indicate males with normal cysts.

Figure 2

Quantitative trait loci (QTL) estimated by composite interval mapping for eye span, adjusted for body length by least squares, in (a–d) female and (e–h) male stalk-eyed flies. Chromosome source is listed above each panel. (d,h) X-linked QTL, estimated from an intercross without an SR parental male. (a–c,e–g) QTL estimated from F2 flies segregating for X^D. Closed diamonds and labels indicate the position and identity (Wright et al. 2004) of microsatellite markers. Note that in (g) (X^D male QTL), all four X-linked markers cosegregate 2.1 cM from SR. Dotted lines indicate likelihood ratio (LR) significance thresholds for p<0.001.

Figure 3

Mean (±s.e.) eye span, adjusted for body length by least squares, for (a–d) female and (e–h) male F2 flies that were homozygous or heterozygous at microsatellite loci (Wright et al. 2004) closest to the QTL of largest effect on each chromosome. Source for alleles is given below each panel, where l and h refer to selected low and high lines, respectively. (c,g) The X-linked low line allele is inherited from an SR parental male. (d,h) Means for F2 flies from the control intercross with a standard parental male (see text).