Complex Epistasis and the Genetic Basis of Hybrid Sterility in the Drosophila pseudoobscura Bogota-USA Hybridization

Genetics ◽  
2001 ◽  
Vol 158 (3) ◽  
pp. 1089-1100 ◽  
Author(s):  
H Allen Orr ◽  
Shannon Irving
Keyword(s):  
Genetic Basis ◽  
Hybrid Sterility ◽  
F1 Hybrids ◽  
Large Chromosome ◽  
Drosophila Pseudoobscura ◽  
Postzygotic Isolation ◽  
Hybrid Male ◽  
Hybrid Fertility ◽  
The Right ◽  
Chromosome Regions

Abstract We analyzed the genetic basis of postzygotic isolation between the Bogota and USA subspecies of Drosophila pseudoobscura. These subspecies diverged very recently (perhaps as recently as 155,000 to 230,000 years ago) and are partially reproductively isolated: Bogota and USA show very little prezygotic isolation but form sterile F1 males in one direction of the hybridization. We dissected the basis of this hybrid sterility and reached four main conclusions. First, postzygotic isolation appears to involve a modest number of genes: we found large chromosome regions that have no effect on hybrid fertility. Second, although apparently few in number, the factors causing hybrid sterility show a remarkably complex pattern of epistatic interaction. Hybrids suffer no hybrid sterility until they carry the “right” allele (Bogota vs. USA) at at least four loci. We describe the complete pattern of interactions between all chromosome regions known to affect hybrid fertility. Third, hybrid sterility is caused mainly by X-autosomal incompatibilities. Fourth, hybrid sterility does not involve a maternal effect, despite earlier claims to the contrary. In general, our results suggest that fewer genes are required for the appearance of hybrid sterility than implied by previous studies of older pairs of Drosophila species. Indeed, a maximum likelihood analysis suggests that roughly 15 hybrid male steriles separate the Bogota and USA subspecies. Only a subset of these would act in F1 hybrids.

scholarly journals The Genetic Basis of Drosophila sechellia's Resistance to a Host Plant Toxin

Genetics ◽  
1998 ◽  
Vol 149 (4) ◽  
pp. 1899-1908 ◽  
Author(s):  
Corbin D Jones
Keyword(s):  
Host Plant ◽  
Genetic Basis ◽  
Morinda Citrifolia ◽  
F1 Hybrids ◽  
Large Chromosome ◽  
Plant Toxin ◽  
Ecological Isolation ◽  
Two Factors ◽  
Close Relatives ◽  
Chromosome Regions

Abstract Unlike its close relatives, Drosophila sechellia is resistant to the toxic effects of the fruit of its host plant, Morinda citrifolia. Using 15 genetic markers, I analyze the genetic basis of D. sechellia's resistance to this fruit's primary toxin, octanoic acid. D. sechellia's resistance is dominant in F1 hybrids between it and its sister species D. simulans. All chromosomes, except the Y and the dot fourth, carry genes affecting resistance. The third chromosome has the greatest effect and carries at least two factors. The X chromosome has an intermediate effect and harbors at least two genes, whereas the second chromosome carries at least one gene of weak effect. Thus, at least five loci are involved in this adaptation. However, I also identified large chromosome regions having no effect on resistance, suggesting that D. sechellia's resistance is neither very simple nor highly polygenic. Instead, resistance appears to have an oligogenic basis. D. sechellia's resistance to its host may contribute to ecological isolation between it and D. simulans.

scholarly journals Prdm9 Intersubspecific Interactions in Hybrid Male Sterility of House Mouse

2020 ◽  
Vol 37 (12) ◽  
pp. 3423-3438
Author(s):  
Amisa Mukaj ◽  
Jaroslav Piálek ◽  
Vladana Fotopulosova ◽  
Andrew Parker Morgan ◽  
Linda Odenthal-Hesse ◽  
...  
Keyword(s):  
Sperm Count ◽  
Hybrid Sterility ◽  
Laboratory Mouse ◽  
F1 Hybrids ◽  
Laboratory Model ◽  
Mouse Strains ◽  
Hybrid Male ◽  
Meiotic Arrest ◽  
Homologous Chromosomes ◽  
Sterility Gene

Abstract The classical definition posits hybrid sterility as a phenomenon when two parental taxa each of which is fertile produce a hybrid that is sterile. The first hybrid sterility gene in vertebrates, Prdm9, coding for a histone methyltransferase, was identified in crosses between two laboratory mouse strains derived from Mus mus musculus and M. m. domesticus subspecies. The unique function of PRDM9 protein in the initiation of meiotic recombination led to the discovery of the basic molecular mechanism of hybrid sterility in laboratory crosses. However, the role of this protein as a component of reproductive barrier outside the laboratory model remained unclear. Here, we show that the Prdm9 allelic incompatibilities represent the primary cause of reduced fertility in intersubspecific hybrids between M. m. musculus and M. m. domesticus including 16 musculus and domesticus wild-derived strains. Disruption of fertility phenotypes correlated with the rate of failure of synapsis between homologous chromosomes in meiosis I and with early meiotic arrest. All phenotypes were restored to normal when the domesticus Prdm9dom2 allele was substituted with the Prdm9dom2H humanized variant. To conclude, our data show for the first time the male infertility of wild-derived musculus and domesticus subspecies F1 hybrids controlled by Prdm9 as the major hybrid sterility gene. The impairment of fertility surrogates, testes weight and sperm count, correlated with increasing difficulties of meiotic synapsis of homologous chromosomes and with meiotic arrest, which we suppose reflect the increasing asymmetry of PRDM9-dependent DNA double-strand breaks.

Genetics of reproductive isolation in the Drosophila simulans clade: complex epistasis underlying hybrid male sterility.

Genetics ◽  
1994 ◽  
Vol 137 (1) ◽  
pp. 175-189 ◽  
Author(s):  
E L Cabot ◽  
A W Davis ◽  
N A Johnson ◽  
C I Wu
Keyword(s):  
Male Sterility ◽  
Genetic Basis ◽  
Species Differences ◽  
Single Gene ◽  
Hybrid Sterility ◽  
Drosophila Simulans ◽  
Theoretical Argument ◽  
Hybrid Male ◽  
Individual Factor ◽  
Resolution Mapping

Abstract We have analyzed the sterility associated with introgressions of the distal one-fourth of the X chromosome from either Drosophila mauritiana or Drosophila sechellia into the genome of Drosophila simulans using a series of visible and DNA markers. Because in Drosophila hybrids, male sterility is usually complete and is often tightly linked with each of several markers used in crosses, a simple genetic basis has generally been assumed. In our low resolution mapping experiment, we were not able to reject the null hypothesis that a single gene, introgressed from either D. mauritiana or D. sechellia, is the cause of male sterility. High resolution mapping, however, reveals a much more complex picture. At least three distinct factors from D. mauritiana, or two from D. sechellia, were identified that need to be jointly present to confer full sterility. Each individual factor by itself is relatively ineffective in causing sterility, or even a partial spermatogenic defect. Moreover, there appear to be more sterility factors on comparable introgressions from D. mauritiana than from D. sechellia. On the basis of these observations, we propose a model which suggests that multilocus weak allele interactions are a very common cause of reproductive incompatibility between closely related species. We also present theoretical argument and empirical evidence against extrapolating the results of within-species analysis to interpret the genetic basis of species differences. The implications of this model on the theories of evolution of species differences and the attempt to understand the mechanisms of hybrid sterility/inviability at the molecular level are discussed.

scholarly journals Stage-specific disruption of X chromosome expression during spermatogenesis in sterile house mouse hybrids

2021 ◽  
Author(s):  
Erica Larson ◽  
Emily Emiko Konishi Kopania ◽  
Kelsie E Hunnicutt ◽  
Dan Vanderpool ◽  
Sara Keeble ◽  
...  
Keyword(s):  
Gene Expression ◽  
X Chromosome ◽  
Gene Networks ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Critical Role ◽  
F1 Hybrids ◽  
House Mice ◽  
Mus Musculus Domesticus ◽  
Hybrid Male

Hybrid sterility is a complex phenotype that can result from the breakdown of spermatogenesis at multiple developmental stages. Here, we disentangle two proposed hybrid male sterility mechanisms in the house mice, Mus musculus domesticus and M. m. musculus, by comparing patterns of gene expression in sterile F1 hybrids from a reciprocal cross. We found that hybrid males from both cross directions showed disrupted X chromosome expression during prophase of meiosis I consistent with a loss of Meiotic Sex Chromosome Inactivation (MSCI) and Prdm9-associated sterility, but that the degree of disruption was greater in mice with an M. m. musculus X chromosome consistent with previous studies. During postmeiotic development, gene expression on the X chromosome was only disrupted in one cross direction, suggesting that misexpression at this later stage was genotype-specific and not a simple downstream consequence of MSCI disruption which was observed in both reciprocal crosses. Instead, disrupted postmeiotic expression may depend on the magnitude of earlier disrupted MSCI, or the disruption of particular X-linked genes or gene networks. Alternatively, only hybrids with a potential deficit of Sly copies, a Y-linked ampliconic gene family, showed overexpression in postmeiotic cells, consistent with a previously proposed model of antagonistic coevolution between the X and Y-linked ampliconic genes contributing to disrupted expression late in spermatogenesis. The relative contributions of these two regulatory mechanisms and their impact on sterility phenotypes awaits further study. Our results further support the hypothesis that X-linked hybrid sterility in house mice has a variable genetic basis, and that genotype-specific disruption of gene regulation contributes to overexpression of the X chromosome at different stages of development. Overall, these findings underscore the critical role of epigenetic regulation of the X chromosome during spermatogenesis and suggest that these processes are prone to disruption in hybrids.

scholarly journals Stage-specific disruption of X chromosome expression during spermatogenesis in sterile house mouse hybrids

2021 ◽  
Author(s):  
Erica L Larson ◽  
Emily E K Kopania ◽  
Kelsie E Hunnicutt ◽  
Dan Vanderpool ◽  
Sara Keeble ◽  
...  
Keyword(s):  
Gene Expression ◽  
X Chromosome ◽  
Gene Networks ◽  
Sex Chromosome ◽  
Hybrid Sterility ◽  
Critical Role ◽  
F1 Hybrids ◽  
House Mice ◽  
Mus Musculus Domesticus ◽  
Hybrid Male

Abstract Hybrid sterility is a complex phenotype that can result from the breakdown of spermatogenesis at multiple developmental stages. Here, we disentangle two proposed hybrid male sterility mechanisms in the house mice, Mus musculus domesticus and M. m. musculus, by comparing patterns of gene expression in sterile F1 hybrids from a reciprocal cross. We found that hybrid males from both cross directions showed disrupted X chromosome expression during prophase of meiosis I consistent with a loss of Meiotic Sex Chromosome Inactivation (MSCI) and Prdm9-associated sterility, but that the degree of disruption was greater in mice with an M. m. musculus X chromosome consistent with previous studies. During postmeiotic development, gene expression on the X chromosome was only disrupted in one cross direction, suggesting that misexpression at this later stage was genotype-specific and not a simple downstream consequence of MSCI disruption which was observed in both reciprocal crosses. Instead, disrupted postmeiotic expression may depend on the magnitude of earlier disrupted MSCI, or the disruption of particular X-linked genes or gene networks. Alternatively, only hybrids with a potential deficit of Sly copies, a Y-linked ampliconic gene family, showed overexpression in postmeiotic cells, consistent with a previously proposed model of antagonistic coevolution between the X and Y-linked ampliconic genes contributing to disrupted expression late in spermatogenesis. The relative contributions of these two regulatory mechanisms and their impact on sterility phenotypes awaits further study. Our results further support the hypothesis that X-linked hybrid sterility in house mice has a variable genetic basis, and that genotype-specific disruption of gene regulation contributes to overexpression of the X chromosome at different stages of development. Overall, these findings underscore the critical role of epigenetic regulation of the X chromosome during spermatogenesis and suggest that these processes are prone to disruption in hybrids.

scholarly journals Genetics of Male and Female Sterility in Hybrids of Drosophila pseudoobscura and D. persimilis

Genetics ◽  
1987 ◽  
Vol 116 (4) ◽  
pp. 555-563
Author(s):  
H Allen Orr
Keyword(s):  
Male Sterility ◽  
X Chromosome ◽  
Male Fertility ◽  
Genetic Basis ◽  
Female Sterility ◽  
Drosophila Pseudoobscura ◽  
Testis Size ◽  
Hybrid Male ◽  
Male And Female ◽  
Male And Female Sterility

ABSTRACT The genetic basis of male and female sterility in hybrids of Drosophila pseudoobscura-Drosophila persimilis was studied using backcross analysis. Previous studies indirectly assessed male fertility by measuring testis size; these studies concluded that male sterility results from an X chromosome-autosome imbalance. By directly scoring for the production of motile sperm, male sterility is shown to be largely due to an incompatibility between genes on the X and Y chromosomes of these two species. These species have diverged at a minimum of nine loci affecting hybrid male fertility. Semisterility of hybrid females appears to result from an X chromosome-cytoplasm interaction; the X chromosome thus has the largest effect on sterility in both male and female hybrids. This is apparently the first analysis of the genetic basis of female sterility, or of sterility/inviability affecting both sexes, in an animal hybridization.

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 The Genetic Basis of High Resistance to Rice Yellow Mottle Virus (RYMV) in Cultivars of Two Cultivated Rice Species

Plant Disease ◽  
1999 ◽  
Vol 83 (10) ◽  
pp. 931-935 ◽  
Author(s):  
M. N. Ndjiondjop ◽  
L. Albar ◽  
D. Fargette ◽  
C. Fauquet ◽  
A. Ghesquière
Keyword(s):  
Genetic Basis ◽  
Virus Isolate ◽  
Mottle Virus ◽  
F1 Hybrids ◽  
Enzyme Linked Immunosorbent Assay ◽  
Rice Yellow Mottle Virus ◽  
Recessive Resistance ◽  
Cultivated Rice ◽  
Recessive Resistance Gene ◽  
Yellow Mottle

Three cultivars of Oryza sativa (IR64, Azucena, and Gigante) and four cultivars of O. glaberrima (Tog5681, Tog5673, CG14, and SG329) were evaluated for their resistance to two isolates of rice yellow mottle virus (RYMV) by enzyme-linked immunosorbent assay (ELISA) and symptomatology. Cultivars Tog5681 and Gigante were highly resistant, and no symptoms were observed when either virus isolate was inoculated at 10 or 20 days postgermination and assayed by ELISA at 7, 14, 22, 35, 50, or 64 days postinoculation. Azucena showed a partial resistance, whereas the other cultivars were susceptible. Symptom appearance was associated with increase in ELISA absorbance in the systemically infected leaves. The best discrimination among the cultivars occurred when the plants were inoculated at 10 days postgermination. Crosses were made between the highly resistant (Gigante and Tog5681) and the susceptible (IR64) cultivars to determine the genetic basis of resistance to RYMV. Evaluation of F1 hybrids and interspecific progenies, as well as the segregation of resistance in F2 and F3 lines of the IR64 × Gigante cross, provided results consistent with the presence of a single recessive resistance gene common to Tog5681 and Gigante.

STUDIES ON THE SAL LOCUS IN DROSOPHILA PSEUDOOBSCURA. III. THE MOLECULAR PATTERN OF DNA IN ACTIVE AND INACTIVE CHROMOSOME REGIONS

1973 ◽  
Vol 15 (3) ◽  
pp. 497-507 ◽  
Author(s):  
Eileen Sutton Gersh
Keyword(s):  
Double Helix ◽  
Drosophila Pseudoobscura ◽  
Chromosome 3 ◽  
Gene Products ◽  
Position Effects ◽  
Molecular Pattern ◽  
Cytological Changes ◽  
Dna Double Helix ◽  
Osmotic Effects ◽  
Chromosome Regions

The banding pattern at the tip of salivary gland chromosome 3 in Drosophila pseudoobscura is determined by a nearby locus, sal (salivary). A number of cytological changes in the neighborhood of the sal locus have been obtained. Their effects on the appearance of bands are interpreted in terms of the fine structure of the chromosome and the arrangement of the DNA double helix. Bands as viewed in the light microscope may become dispersed, as in puffs, or compacted, as in position effects involving their transposition to heterochromatic regions. Changes of bands are interpreted in terms of dispersion or compaction of DNA.Secondary puffing is induced in a paired sal chromosome which does not puff when unpaired, by a sal+ homologue which puffs when unpaired. This is explained as being due to osmotic effects caused by added protein and gene products (RNAs) diffusing from the sal+ to the sal chromosome, when they are paired, through submicroscopic interconnecting spaces within the chromosomes.

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