Assessing the putative roles of X–autosome and X–Y interactions in hybrid male sterility of the Drosophila bipectinata species complex

Genome ◽  
2007 ◽  
Vol 50 (7) ◽  
pp. 653-659 ◽  
Author(s):  
Paras Kumar Mishra ◽  
Bashisth Narayan Singh

Interspecific F1 hybrid males of the Drosophila bipectinata species complex are sterile, while females are fertile, following Haldane’s rule. A backcross scheme involving a single recessive visible marker on the X chromosome has been used to assess the putative roles of X–autosome and X–Y interactions in hybrid male sterility in the D. bipectinata species complex. The results suggest that X–Y interactions are playing the major role in hybrid male sterility in the crosses D. bipectinata × D. parabipectinata and D. bipectinata × D. pseudoananassae , while X–autosome interactions are largely involved in hybrid male sterility in the crosses D. malerkotliana × D. bipectinata and D. malerkotliana × D. parabipectinata. However, by using this single marker it is not possible to rule out the involvement of autosome–autosome interactions in hybrid male sterility. These findings also lend further support to the phylogenetic relationships among 4 species of the D. bipectinata complex.

Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 745-754 ◽  
Author(s):  
Xulio R Maside ◽  
José P Barral ◽  
Horacio F Naveira

Abstract 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.


Genetics ◽  
1993 ◽  
Vol 135 (1) ◽  
pp. 135-147
Author(s):  
L W Zeng ◽  
R S Singh

Abstract We have attempted to estimate the number of genes involved in postzygotic reproductive isolation between two closely related species, Drosophila simulans and Drosophila sechellia, by a novel approach that involves the use of high resolution two-dimensional gel electrophoresis (2DE) to examine testis proteins in parents, hybrids and fertile and sterile backcross progenies. The important results that have emerged from this study are as follows: (1) about 8% of about 1000 proteins examined showed divergence (presence/absence) between the two species; (2) by tracing individual proteins in parental, hybrid and backcross males, we were able to associate the divergent proteins with different chromosomes and found that most divergent proteins are associated with autosomes and very few with X chromosome, Y chromosome and cytoplasm; (3) when proteins showing both quantitative and qualitative differences between the two species were examined in F1 hybrid males, most (97.4%) proteins were expressed at levels between the two parents and no sign of large scale changes in spot density was observed. All the proteins observed in the two parental species were present in F1 hybrid males except two species-specific proteins that may be encoded (or regulated) by sex chromosomes; (4) when different fertile and sterile backcross male testes were compared, a few D. sechellia-specific proteins were identified to be consistently associated with male sterility. These results along with the observation that a large proportion (23.6%) of first generation backcross males were fertile show that hybrid male sterility between D. simulans and D. sechellia involves a relatively small number of genes. Role of large scale genetic changes due to general genome incompatibility is not supported. The results also suggest that the large effect of X chromosome on hybrid male sterility is not due to higher divergence of X chromosome than autosomes.


Genetics ◽  
2003 ◽  
Vol 164 (4) ◽  
pp. 1383-1398 ◽  
Author(s):  
Yun Tao ◽  
Sining Chen ◽  
Daniel L Hartl ◽  
Cathy C Laurie

AbstractThe genetic basis of hybrid incompatibility in crosses between Drosophila mauritiana and D. simulans was investigated to gain insight into the evolutionary mechanisms of speciation. In this study, segments of the D. mauritiana third chromosome were introgressed into a D. simulans genetic background and tested as homozygotes for viability, male fertility, and female fertility. The entire third chromosome was covered with partially overlapping segments. Many segments were male sterile, while none were female sterile or lethal, confirming previous reports of the rapid evolution of hybrid male sterility (HMS). A statistical model was developed to quantify the HMS accumulation. In comparison with previous work on the X chromosome, we estimate that the X has ∼2.5 times the density of HMS factors as the autosomes. We also estimate that the whole genome contains ∼15 HMS “equivalents”—i.e., 15 times the minimum number of incompatibility factors necessary to cause complete sterility. Although some caveats for the quantitative estimate of a 2.5-fold density difference are described, this study supports the notion that the X chromosome plays a special role in the evolution of reproductive isolation. Possible mechanisms of a “large X” effect include selective fixation of new mutations that are recessive or partially recessive and the evolution of sex-ratio distortion systems.


1997 ◽  
Vol 75 (7) ◽  
pp. 1109-1117 ◽  
Author(s):  
R. H. Gooding

Reciprocal crosses of Glossina palpalis gambiensis Vanderplank and Glossina palpalis palpalis (Robineau-Desvoidy) were carried out using flies that had four marker genes on the X chromosome, two in linkage group II and one in linkage group III: The results of the reciprocal crosses conformed to Haldane's rule: F1 males were sterile and most F1 females were fertile. F1 females mated to G. p. gambiensis were more likely to be fertilized than females that were mated to G. p. palpalis. In three of the four experiments, the fertility of backcross females was not significantly different from that of F1 females, and there was little evidence that specific chromosomal combinations influenced the fertility of backcross females. Intrachromosomal recombination was lower in hybrid females than in G. p. palpalis. The major genetic factor associated with sterility among backcross males was the presence of sex chromosomes from two subspecies; a minor factor was the number of heterozygous autosomes, but interactions between sex chromosomes and autosomes from different taxa did not contribute to hybrid male sterility. Evidence is presented that a major factor causing hybrid male sterility lies between the loci tan (an eye color) and Est-t (testicular esterase) on the X chromosome. The use of differences between the fertility of males produced by backcrossing F1 females to the two parental subspecies as indicators that other X chromosome loci have a role in hybrid sterility is discussed.


Genetics ◽  
1994 ◽  
Vol 138 (2) ◽  
pp. 329-341 ◽  
Author(s):  
M F Palopoli ◽  
C I Wu

Abstract To study the genetic differences responsible for the sterility of their male hybrids, we introgressed small segments of an X chromosome from Drosophila simulans into a pure Drosophila mauritiana genetic background, then assessed the fertility of males carrying heterospecific introgressions of varying size. Although this analysis examined less than 20% of the X chromosome (roughly 5% of the euchromatic portion of the D. simulans genome), and the segments were introgressed in only one direction, a minimum of four factors that contribute to hybrid male sterility were revealed. At least two of the factors exhibited strong epistasis: males carrying either factor alone were consistently fertile, whereas males carrying both factors together were always sterile. Distinct spermatogenic phenotypes were observed for sterile introgressions of different lengths, and it appeared that an interaction between introgressed segments also influenced the stage of spermatogenic defect. Males with one category of introgression often produced large quantities of motile sperm and were observed copulating, but never inseminated females. Evidently these two species have diverged at a large number of loci which have varied effects on hybrid male fertility. By extrapolation, we estimate that there are at least 40 such loci on the X chromosome alone. Because these species exhibit little DNA-sequence divergence at arbitrarily chosen loci, it seems unlikely that the extensive functional divergence observed could be due mainly to random genetic drift. Significant epistasis between conspecific genes appears to be a common component of hybrid sterility between recently diverged species of Drosophila. The linkage relationships of interacting factors could shed light on the role played by epistatic selection in the dynamics of the allele substitutions responsible for reproductive barriers between species.


Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1243-1255 ◽  
Author(s):  
Hope Hollocher ◽  
Chug-I Wu

Abstract A strong effect of homozygous autosomal regions on reproductive isolation was found for crosses between the species in the Drosophila simulans clade. Second chromosome regions were introgressed from D. mauritiana and D. sechellia into D. simulans and tested for their homozygous effects on hybrid male and hybrid female sterility and inviability. Most introgressions are fertile as heterozygotes, yet produce sterile male offspring when made homozygous. The density of homozygous autosomal factors contributing to hybrid male sterility is comparable to the density of X chromosome factors for this level of resolution. Female sterility was also revealed, yet the disparity between male and female levels of sterility was great, with male sterility being up to 23 times greater than female sterility. Complete hybrid inviability was also associated with some regions of the second chromosome, yet there were no strong sex differences. In conclusion, we find no evidence to support a strong X chromosome bias in the evolution of hybrid sterility or inviability but do find a very strong sex bias in the evolution of hybrid sterility. In light of these findings, we reevaluate the current models proposed to explain the genetic pattern of reproductive isolation.


Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 789-796 ◽  
Author(s):  
Kyoichi Sawamura ◽  
John Roote ◽  
Chung-I Wu ◽  
Masa-Toshi Yamamoto

Abstract Recent genetic analyses of closely related species of Drosophila have indicated that hybrid male sterility is the consequence of highly complex synergistic effects among multiple genes, both conspecific and heterospecific. On the contrary, much evidence suggests the presence of major genes causing hybrid female sterility and inviability in the less-related species, D. melanogaster and D. simulans. Does this contrast reflect the genetic distance between species? Or, generally, is the genetic basis of hybrid male sterility more complex than that of hybrid female sterility and inviability? To clarify this point, the D. simulans introgression of the cytological region 34D-36A to the D. melanogaster genome, which causes recessive male sterility, was dissected by recombination, deficiency, and complementation mapping. The 450-kb region between two genes, Suppressor of Hairless and snail, exhibited a strong effect on the sterility. Males are (semi-)sterile if this region of the introgression is made homozygous or hemizygous. But no genes in the region singly cause the sterility; this region has at least two genes, which in combination result in male sterility. Further, the males are less fertile when heterozygous with a larger introgression, which suggests that dominant modifiers enhance the effects of recessive genes of male sterility. Such an epistatic view, even in the less-related species, suggests that the genetic complexity is special to hybrid male sterility.


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