Sex ratio meiotic drive as a plausible evolutionary mechanism for hybrid male sterility

Abstract

Biological diversity on Earth depends on the multiplication of species or speciation, which is the evolution of reproductive isolation such as hybrid sterility between two new species. An unsolved puzzle is the exact mechanism(s) that causes two genomes to diverge from their common ancestor so that some divergent genes no longer function properly in the hybrids. Here we report genetic analyses of divergent genes controlling male fertility and sex ratio in two very young fruitfly species, Drosophila albomicans and D. nasuta. A majority of the genetic divergence for both traits is mapped to the same regions by quantitative trait loci mappings. With introgressions, six major loci are found to contribute to both traits. This genetic colocalization implicates that genes for hybrid male sterility have evolved primarily for controlling sex ratio. We propose that genetic conflicts over sex ratio may operate as a perpetual dynamo for genome divergence. This particular evolutionary mechanism may largely contribute to the rapid evolution of hybrid male sterility and the disproportionate enrichment of its underlying genes on the X chromosome--two patterns widely observed across animals.

Fig 1. Key stocks of D. albomicans and D. nasuta used in this study.

(A) Karyotypes of these two species. Robertsonian fusions between the X (Y) and the 3^rd chromosomes in their ancestor led to a pair of new sex chromosomes X-3/Y-3 in D. albomicans. Muller’s elements are assigned to chromosomal arms, along with the translocations detected by molecular markers and genetic linkage from this study (S1 Dataset and S1 Table). (B) Stockes used in this study. Shown are fixed inversions and the associated breakpoints for true-bred stocks (alb267 and alb215) derived from alb2, and nas314 and nas384 from nas3, as well as the segregating inversions (shl2-hap1 and shl2-hap2) in shl2. The polytene sequence was determined according to the standard map made from alb267 (S2 Dataset). The centromere position on the “dot” chromosome 4 is not determined.

Fig 2. Abnormal spermatid indicating HMS.

Cross sections of condensed sperm heads (upper row) and mature spermatid tails (lower row) in the F1 males from three interspecific (first three columns) and one intraspecific control (rightmost column) crosses (♀ × ♂). All sperm heads were normal, but frequent twin tail fusions (arrow heads) were counted in all but the F1 males from nas3 × alb2 (Mean ± s.e.m. with the numbers of spermatid bundles examined in parentheses under the representative TEM images. P < 0.05 for all pairwise comparisons, ANOVA and TukeyHSD). All scale bars are 1 μm.

Fig 3. Polymorphism of HMS and SRD genes in D. albomicans.

Males and females from inbred lines of D. abomicans (alb2, shl2) and D. nasuta (nas3) were tested for fertility and sex ratio using the exhaustive mating protocol, so were the F1 males and female from the crosses (♀ × ♂) among these three lines. Virgins from alb2 were used as testers throughout (Materials and Methods). Box plots of male fertility (A) and offspring sex ratio (B), female fertility (C) and offspring sex ratio (D). Phenotypes not sharing the same numerals (1–4) in each panel are significantly different (P < 0.05, ANOVA and TukeyHSD). The sample sizes are shown above the abscissa.

Fig 4. QTL detected from the three mapping experiments.

Synopsized from S5 Fig and S1–S4 Tables. QTL of sex ratio and male fertility (T) are shown at the left and right of chromosomes, respectively. Linkage groups are shown to scale, with their total lengths shown at the distal ends. The names of some key markers are also shown (See S1 Table for complete dataset). “Good” QTL (rectangles) are those implicated by both CIM and MIM for sex ratio, or those by both T and at least one transformation of T (log₁₀ ^(T+1) or binary) for fertility; otherwise the QTL are “tentative” (circles). For each QTL, the horizontal bar points to its most likely position on the map. The 95% confidence intervals and the phenotypic effects (measured as additive genetic variance h ²) of the “good” QTL are represented by the heights and widths of the rectangles, respectively. For “tentative” QTL, no 95% confidence intervals can be given, but their effects are proportional to the diameters of the circles. In Exp1, the alb267 alleles have positive effects (filled rectangle or circle) or negative effects (empty), as relative to the shl2-hap1 alleles. Similarly, the effects of the alb267 alleles are shown relative to the nas314 alleles in Exp2, so are the effects of shl2-hap1 alleles relative to the nas314 alleles in Exp3. HMS7 is not drawn to scale because neither its location nor its effect is stable across the three mapping analyses (S5 Fig, S3 Table). Four regions (R1–R4) are highlighted because they contribute most of the h ² in all three experiments (Table 2).