Hidden effects of X chromosome introgressions on spermatogenesis in Drosophila simulans x D. mauritiana hybrids unveiled by interactions among minor genetic factors.

One of the most frequent outcomes of interspecific hybridizations in Drosophila is hybrid male sterility. Genetic dissection of this reproductive barrier has revealed that the number of responsible factors is very high and that these factors are frequently engaged in complex epistatic interactions. Traditionally, research strategies have been based on contrasting introgressions of chromosome segments that produce male sterility with those that allow fertility. Few studies have investigated the phenotypes associated with the boundary between fertility and sterility. In this study, we cointrogressed three different X chromosome segments from Drosophila mauritiana into D. simulans. Hybrid males with these three segments are usually fertile, by conventional fertility assays. However, their spermatogenesis shows a significant slowdown, most manifest at lower temperatures. Each of the three introgressed segments retards the arrival of sperm to the seminal vesicles. Other small disturbances in spermatogenesis are evident, which altogether lead to an overall reduction in the amount of motile sperm in their seminal vesicles. These results suggest that a delay in the timing of spermatogenesis, which might be brought about by the cumulative action of many different factors of minor segment, may be the primary cause of hybrid male sterility.

A polygenic basis of hybrid sterility may give rise to spurious localizations of major sterility factors.

A simple model is presented to illustrate how an underlying generalized polygenic basis of hybrid sterility is expected to lead to spurious localizations of factors with major effects, when a conventional experiment of recombination mapping is carried out. The model shows that a major gene will be detected at roughly the same distance from each of the chromosome markers used in the experiment. These expectations are contrasted with the results from several experiments on hybrid male sterility in Drosophila, which claimed to have mapped single sterility factors. It is concluded that, except for one report, all the evidence presented so far on the genetic basis of hybrid male sterility in Drosophila is in fact compatible with the generalized polygenic model.

On the difficulties of discriminating between major and minor hybrid male sterility factors in Drosophila by examining the segregation ratio of sterile and fertile sons in backcrossing experiments.

The observation of segregation ratios of sterile and fertile males in offspring samples from backcrossed hybrid females is, in principle, a valid method to unveil the genetic basis of hybrid male sterility in Drosophila. When the female parent is heterozygous (hybrid) for a sterility factor with major effects, equal proportions of fertile and sterile sons are expected in her offspring. However, intact (not recombined) chromosome segments of considerable length are expected to give segregation ratios that can not be easily differentiated from the 1:1 ratio expected from a single factor. When the phenotypic character under analysis can be determined by combinations of minor factors from the donor species spanning a certain chromosome length, very large offspring samples may be needed to test this alternative hypothesis against the null hypothesis of a single major factor. This is particularly the case of hybrid male sterility determinants in Drosophila.

A three-locus system of interspecific incompatibility underlies male inviability in hybrids between Drosophila buzzatii and D. koepferae.

In hybrids between the sibling species D. buzzatii and D. koepferae, both sexes are more or less equally viable in the F1. However, backcross males to D. buzzatii are frequently inviable, apparently because of interspecific genetic incompatibilities that are cryptic in the F1. We have performed a genetic dissection of the effects of the X chromosome from D. koepferae. We found only two cytological regions, termed hmi-1 and hmi-2, altogether representing 9% of the whole chromosome, which when introgressed into D. buzzatii cause inviability of hybrid males. Observation of the pattern of asynapsis of polytene chromosomes (incomplete pairing, marking introgressed material) in females and segregation analyses were the technique used to infer the X chromosome regions responsible for this hybrid male inviability. The comparison of these results with those previously obtained with the same technique for hybrid male sterility in this same species pair indicate that in the X chromosome of D. koepferae there are at least seven times more regions that produce hybrid male sterility than hybrid male inviability. We have also found that the inviability brought about by the introgression of hmi-1 is suppressed by the cointrogression of two autosomal sections from D. koepferae. Apparently, these three regions conform to a system of species-specific complementary factors involved in an X-autosome interaction that, when disrupted in backcross hybrids by recombination with the genome of its sibling D. buzzatii, brings about hybrid male inviability.

Location of X-linked polygenic effects causing sterility in male hybrids of Drosophila simulans and D. mauritiana.

There is general agreement that hybrid male sterility in Drosophila is caused by changes at several (perhaps many) factors, most of them located on the X chromosome. These factors have been generally considered as major genes, each one of them able to bring about sterility by itself. However, the evidence on this last point is not conclusive. In principle, the possibility that they correspond to located polygenic effects instead of genes with a large effect cannot be excluded. This paper shows that some of the factors that cause male sterility in D. simulans/D. mauritiana hybrids, located by recombination on the X chromosome, are indeed 'effective factors', or located polygenic effects. Some of the consequences of this finding are explored.