Evidence for complex genic interactions between conspecific chromosomes underlying hybrid female sterility in the Drosophila simulans clade.

Genetics ◽  
1994 ◽  
Vol 137 (1) ◽  
pp. 191-199 ◽  
Author(s):  
A W Davis ◽  
E G Noonburg ◽  
C I Wu
Keyword(s):  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
X Chromosomes ◽  
F1 Hybrid ◽  
Drosophila Mauritiana

Abstract F1 hybrid females between the sibling species Drosophila simulans, Drosophila mauritiana and Drosophila sechellia are completely fertile. However, we have found that female sterility can be observed in F2 backcross females who are homozygous for D. simulans X chromosomes and homozygous for autosomal regions from either D. mauritiana or D. sechellia. Our results indicate that neither D. mauritiana autosome (2 or 3) can cause complete female sterility in a D. simulans background. The simultaneous presence of homozygous regions from both the second and third chromosomes of D. mauritiana, however, causes nearly complete female sterility which cannot be accounted for by their individual effects. The two autosomes of D. sechellia may show a similar pattern. From the same crosses, we also obtained evidence against a role for cytoplasmic or maternal effects in causing hybrid male sterility between these species. Taken with the results presented elsewhere, these observations suggest that epistatic interactions between conspecific genes in a hybrid background may be the prevalent mode of hybrid sterility between recently diverged species.

scholarly journals The Genetics of Reproductive Isolation in the Drosophila simulans Clade: X vs. Autosomal Effects and Male vs. Female Effects

Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1243-1255 ◽  
Author(s):  
Hope Hollocher ◽  
Chug-I Wu
Keyword(s):  
Reproductive Isolation ◽  
Male Sterility ◽  
X Chromosome ◽  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Hybrid Inviability

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.

scholarly journals Hidden Effects of X Chromosome Introgressions on Spermatogenesis in Drosophila simulans × D. mauritiana Hybrids Unveiled by Interactions Among Minor Genetic Factors

Genetics ◽  
1998 ◽  
Vol 150 (2) ◽  
pp. 745-754 ◽  
Author(s):  
Xulio R Maside ◽  
José P Barral ◽  
Horacio F Naveira
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Seminal Vesicles ◽  
Genetic Dissection ◽  
Research Strategies ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Epistatic Interactions ◽  
Drosophila Mauritiana ◽  
Chromosome Segments

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.

Genetic Complexity Underlying Hybrid Male Sterility in Drosophila

Genetics ◽  
2004 ◽  
Vol 166 (2) ◽  
pp. 789-796 ◽  
Author(s):  
Kyoichi Sawamura ◽  
John Roote ◽  
Chung-I Wu ◽  
Masa-Toshi Yamamoto
Keyword(s):  
Male Sterility ◽  
Related Species ◽  
Synergistic Effects ◽  
Female Sterility ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Closely Related Species ◽  
Genetic Complexity ◽  
Recessive Genes

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.

A Novel System of Fertility Rescue in Drosophila Hybrids Reveals a Link Between Hybrid Lethality and Female Sterility

Genetics ◽  
2003 ◽  
Vol 163 (1) ◽  
pp. 217-226 ◽  
Author(s):  
Daniel A Barbash ◽  
Michael Ashburner
Keyword(s):  
Drosophila Melanogaster ◽  
Low Temperature ◽  
Genetic Basis ◽  
Female Sterility ◽  
Hybrid Lethality ◽  
Hybrid Male ◽  
Hybrid Female ◽  
F1 Hybrid ◽  
Drosophila Gene

Abstract Hybrid daughters of crosses between Drosophila melanogaster females and males from the D. simulans species clade are fully viable at low temperature but have agametic ovaries and are thus sterile. We report here that mutations in the D. melanogaster gene Hybrid male rescue (Hmr), along with unidentified polymorphic factors, rescue this agametic phenotype in both D. melanogaster/D. simulans and D. melanogaster/D. mauritiana F1 female hybrids. These hybrids produced small numbers of progeny in backcrosses, their low fecundity being caused by incomplete rescue of oogenesis as well as by zygotic lethality. F1 hybrid males from these crosses remained fully sterile. Hmr+ is the first Drosophila gene shown to cause hybrid female sterility. These results also suggest that, while there is some common genetic basis to hybrid lethality and female sterility in D. melanogaster, hybrid females are more sensitive to fertility defects than to lethality.

scholarly journals Hybrid Sterility, Genetic Conflict and Complex Speciation: Lessons From the Drosophila simulans Clade Species

2021 ◽  
Vol 12 ◽  
Author(s):  
Daven C. Presgraves ◽  
Colin D. Meiklejohn
Keyword(s):  
Gene Flow ◽  
Male Sterility ◽  
Hybrid Sterility ◽  
Model Organism ◽  
Drosophila Simulans ◽  
Special Role ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Genetic Conflict ◽  
Modern Evolutionary Synthesis

The three fruitfly species of the Drosophila simulans clade— D. simulans, D. mauritiana, and D. sechellia— have served as important models in speciation genetics for over 40 years. These species are reproductively isolated by geography, ecology, sexual signals, postmating-prezygotic interactions, and postzygotic genetic incompatibilities. All pairwise crosses between these species conform to Haldane’s rule, producing fertile F1 hybrid females and sterile F1 hybrid males. The close phylogenetic proximity of the D. simulans clade species to the model organism, D. melanogaster, has empowered genetic analyses of their species differences, including reproductive incompatibilities. But perhaps no phenotype has been subject to more continuous and intensive genetic scrutiny than hybrid male sterility. Here we review the history, progress, and current state of our understanding of hybrid male sterility among the D. simulans clade species. Our aim is to integrate the available information from experimental and population genetics analyses bearing on the causes and consequences of hybrid male sterility. We highlight numerous conclusions that have emerged as well as issues that remain unresolved. We focus on the special role of sex chromosomes, the fine-scale genetic architecture of hybrid male sterility, and the history of gene flow between species. The biggest surprises to emerge from this work are that (i) genetic conflicts may be an important general force in the evolution of hybrid incompatibility, (ii) hybrid male sterility is polygenic with contributions of complex epistasis, and (iii) speciation, even among these geographically allopatric taxa, has involved the interplay of gene flow, negative selection, and positive selection. These three conclusions are marked departures from the classical views of speciation that emerged from the modern evolutionary synthesis.

The genetics of hybrid sterility between subspecies of the complex of Glossina morsitans Westwood (Diptera: Glossinidae)

1985 ◽  
Vol 75 (4) ◽  
pp. 689-699 ◽  
Author(s):  
P. Rawlings
Keyword(s):  
Hybrid Sterility ◽  
Autosomal Gene ◽  
Glossina Morsitans ◽  
Hybrid Male ◽  
Hybrid Female ◽  
Hybrid Male Sterility ◽  
Tsetse Control ◽  
Y Chromosomes ◽  
Control Programmes ◽  
Sterility Genes

AbstractCrosses were made between the three subspecies of the complex of Glossina morsitans Westwood and the hybrid females backcrossed. Hybrid female fecundity was highly ‘reactive’ to foreign male genes when the mother was G. morsitans centralis Machado compared with the reciprocal crosses and backcrosses. Hybrid F1 males were unable to inseminate females successfully, and although in nearly a quarter of the dissections sperm was transferred to the uterus, it did not migrate to the spermathecae. Heterozygosity between the X- and Y-chromosomes and most of the autosomes led to high frequencies of sterile males, but homozygosity between the X- and Y-chromosomes could still yield 30–50% sterility. Successive backcrosses of hybrid females between G. m. morsitans and G. m. centralis to the latter subspecies continued to increase the frequency of fertile males. Interactions between X-chromosome and autosomal gene seemed to be responsible for hybrid male sterility, and the number of sterility genes involved appeared to be very few. Crosses involving G. morsitans submorsitans Newstead generally agreed with those between the other two subspecies, but the distortion in the sex ratio of emergent adults limited the application of the data to this subspecies. Competition experiments using sterile hybrid males and fertile males in population cages (30 cm cube) showed that suppression was possible, especially when the ratio of sterile:fertile males was 2:1. The value of stetile hybrid males in tsetse control programmes and the evolution of reproductive isolation in the complex is discussed.

scholarly journals Further characterization of the Odysseus locus of hybrid sterility in Drosophila: one gene is not enough.

Genetics ◽  
1995 ◽  
Vol 140 (1) ◽  
pp. 201-206 ◽  
Author(s):  
D E Perez ◽  
C I Wu
Keyword(s):  
Related Species ◽  
Genetic Background ◽  
Hybrid Sterility ◽  
Weak Effect ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Closely Related Species ◽  
Drosophila Mauritiana ◽  
Average Gene

Abstract Previously we mapped by genetical and molecular means a gene that contributes to hybrid-male sterility between Drosophila mauritiana and D. simulans to the cytological interval of 16D. In this report, we refine the mapping of this gene, Odysseus (Ods) and show that it can be delineated to a region the size of an average gene. We further demonstrate that, while Ods appears to be a discrete element, it requires other nearby gene(s) to be cointrogressed to confer full hybrid sterility effect. This observation is in agreement with the view that reproductive isolation between closely related species of Drosophila is usually caused by several genes of weak effect from the same species that interact strongly among themselves as well as with the foreign genetic background.

scholarly journals Genetics of hybrid male sterility between drosophila sibling species: a complex web of epistasis is revealed in interspecific studies.

Genetics ◽  
1994 ◽  
Vol 138 (2) ◽  
pp. 329-341 ◽  
Author(s):  
M F Palopoli ◽  
C I Wu
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Functional Divergence ◽  
Hybrid Sterility ◽  
Sequence Divergence ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Common Component ◽  
Drosophila Mauritiana ◽  
Linkage Relationships

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.

scholarly journals The genetic basis of Haldane's rule and the nature of asymmetric hybrid male sterility among Drosophila simulans, Drosophila mauritiana and Drosophila sechellia.

Genetics ◽  
1993 ◽  
Vol 134 (1) ◽  
pp. 251-260 ◽  
Author(s):  
L W Zeng ◽  
R S Singh
Keyword(s):  
Male Sterility ◽  
Y Chromosome ◽  
Genetic Basis ◽  
Drosophila Simulans ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Haldane’S Rule ◽  
Drosophila Sechellia ◽  
Haldane's Rule ◽  
Drosophila Mauritiana

Abstract Haldane's rule (i.e., the preferential hybrid sterility and inviability of heterogametic sex) has been known for 70 years, but its genetic basis, which is crucial to the understanding of the process of species formation, remains unclear. In the present study, we have investigated the genetic basis of hybrid male sterility using Drosophila simulans, Drosophila mauritiana and Drosophila sechellia. An introgression of D. sechellia Y chromosome into a fairly homogenous background of D. simulans did not show any effect of the introgressed Y on male sterility. The substitution of D. simulans Y chromosome into D. sechellia, and both reciprocal Y chromosome substitutions between D. simulans and D. mauritiana were unsuccessful. Introgressions of cytoplasm between D. simulans and D. mauritiana (or D. sechellia) also did not have any effect on hybrid male sterility. These results rule out the X-Y interaction hypothesis as a general explanation of Haldane's rule in this species group and indicate an involvement of an X-autosome interaction. Models of symmetrical and asymmetrical X-autosome interaction have been developed which explain the Y chromosome substitution results and suggest that evolution of interactions between different genetic elements in the early stages of speciation is more likely to be of an asymmetrical nature. The model of asymmetrical X-autosome interaction also predicts that different sets of interacting genes may be involved in different pairs of related species and can account for the observation that hybrid male sterility in many partially isolated species is often nonreciprocal or unidirectional.

scholarly journals The Broom of the Sorcerer's Apprentice: The Fine Structure of a Chromosomal Region Causing Reproductive Isolation Between Two Sibling Species of Drosophila

Genetics ◽  
1996 ◽  
Vol 143 (3) ◽  
pp. 1287-1298 ◽  
Author(s):  
Andrew W Davis ◽  
Chug-I Wu
Keyword(s):  
Reproductive Isolation ◽  
Sibling Species ◽  
Related Species ◽  
Hybrid Sterility ◽  
Drosophila Genome ◽  
Hybrid Male ◽  
Hybrid Male Sterility ◽  
Closely Related Species ◽  
Drosophila Mauritiana ◽  
Two Factors

Abstract How many genes contribute to reproductive isolation between closely related species? We determined the number of genes located in the 9D-12B region of the Drosophila mauritiana X chromosome that cause hybrid male sterility in a D. simulans background. Previous low resolution studies suggested that a single hybrid sterility factor was associated with this region. In this study, by taking advantage of a cluster of visible and DNA markers, we identified three D. mauritiana factors in this region and then subjected one of them to detailed analysis. This factor again turned out to be comprised of three factors; one of which, mapped to within 200 kb, may in fact be two factors. The title refers to this exercise of splitting sterile introgressions into ever smaller ones, each of which retains partial or full sterility effects. In a region representing a mere 3% of the Drosophila genome, no fewer than six loci of hybrid sterility were identified between two sibling species that have not shown clear divergence at the molecular level. These results suggest that levels of genetic divergence between closely related species may be quite high for functionally important traits even when the opposite is true for randomly chosen loci.

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