Abstract
When species interbreed, the hybrid offspring that are produced are often sterile. If only one hybrid sex is sterile, it is almost always the heterogametic (XY or ZW) sex. Taking this trend into account, the predominant model used to explain the genetic basis of F1 sterility involves a deleterious interaction between recessive sex-linked loci from one species and dominant autosomal loci from the other species. This model is difficult to evaluate, however, as only a handful of loci influencing interspecies hybrid sterility have been identified, and their autosomal genetic interactors have remained elusive. One hindrance to their identification has been the overwhelming effect of the sex chromosome in mapping studies, which could ‘mask’ the ability to accurately map autosomal factors. Here, we use a novel approach employing attached-X chromosomes to create reciprocal backcross interspecies hybrid males that have a non-recombinant sex chromosome and recombinant autosomes. The heritable variation in phenotype is thus solely caused by differences in the autosomes, thereby allowing us to accurately identify the number and location of autosomal sterility loci. In one direction of backcross, all males were sterile, indicating that sterility could be entirely induced by the sex chromosome complement in these males. In the other direction, we identified nine quantitative trait loci that account for a surprisingly large amount (56%) of the autosome-induced phenotypic variance in sterility, with a large contribution of autosome-autosome epistatic interactions. These loci are capable of acting dominantly, and thus could contribute to F1 hybrid sterility.
Highlights
Reproductive isolation occurs when there is a barrier that prevents two species from producing fit hybrid offspring
None of the males resulting from a backcross to D. simulans had motile sperm (N = 266), while approximately 15% of D. mauritiana backcross males (111 out of 760) had motile sperm (Figure 2)
The second comparison was similar to the first but included the presence of non-motile sperm as an intermediate trait between sperm absence and motile sperm. This map is similar to that produced from the first comparison, with the addition of quantitative trait locus (QTL) #4 in the middle of the second chromosome. Two of these QTL have an epistatic interaction with each other, and one has an epistatic interaction with a locus at 197 cM2 Range (cM) on the third chromosome (Table 2), identifying an additional QTL that is within this region
Summary
Reproductive isolation occurs when there is a barrier that prevents two species from producing fit hybrid offspring. One of the predominant models for explaining this trend is a combination of the Dobzhansky-Muller (D-M) model and the dominance model, whereby dysfunction in the interspecies F1 is caused by a deleterious interaction between a recessive sexlinked factor from one species and a dominant autosomal factor from the other species [4,5,6,7]. The dominance of the autosomal factor explains how it affects an interspecies F1; the recessive sexlinked factor is masked in homogametic individuals and unmasked in heterogametic individuals, explaining the appearance of sterility in heterogametic individuals, and Haldane’s Rule. Several studies have mapped genomic regions containing autosomal sterility loci using introgressions (e.g., [12,13,14,15]). Of the identified loci, only Overdrive acts in a manner consistent with the predominant theoretical model, and the individual interactor loci have not yet been identified [16]
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