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

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.

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Genetic Dissection of Hybrid Incompatibilities BetweenDrosophila simulansandD. mauritiana. I. Differential Accumulation of Hybrid Male Sterility Effects on theXand Autosomes

Genetics ◽

10.1093/genetics/164.4.1383 ◽

2003 ◽

Vol 164 (4) ◽

pp. 1383-1398 ◽

Cited By ~ 18

Author(s):

Yun Tao ◽

Sining Chen ◽

Daniel L Hartl ◽

Cathy C Laurie

Keyword(s):

Male Sterility ◽

X Chromosome ◽

Rapid Evolution ◽

Special Role ◽

Genetic Dissection ◽

Male Sterile ◽

Hybrid Male ◽

Evolutionary Mechanisms ◽

Hybrid Male Sterility ◽

Minimum Number

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.

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

Genetics ◽

10.1093/genetics/138.2.329 ◽

1994 ◽

Vol 138 (2) ◽

pp. 329-341 ◽

Cited By ~ 3

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.

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Genetic Dissection of Hybrid Male Sterility Across Stages of Spermatogenesis

Genetics ◽

10.1534/genetics.118.301658 ◽

2018 ◽

Vol 210 (4) ◽

pp. 1453-1465 ◽

Cited By ~ 10

Author(s):

Denise J. Schwahn ◽

Richard J. Wang ◽

Michael A. White ◽

Bret A. Payseur

Keyword(s):

Male Sterility ◽

Genetic Dissection ◽

Hybrid Male ◽

Hybrid Male Sterility

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A combined classical genetic and high resolution two-dimensional electrophoretic approach to the assessment of the number of genes affecting hybrid male sterility in Drosophila simulans and Drosophila sechellia.

Genetics ◽

10.1093/genetics/135.1.135 ◽

1993 ◽

Vol 135 (1) ◽

pp. 135-147

Author(s):

L W Zeng ◽

R S Singh

Keyword(s):

Male Sterility ◽

X Chromosome ◽

Large Scale ◽

Two Dimensional ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

F1 Hybrid ◽

Drosophila Sechellia ◽

Number Of Genes ◽

Specific Proteins

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.

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

Genome ◽

10.1139/g07-049 ◽

2007 ◽

Vol 50 (7) ◽

pp. 653-659 ◽

Cited By ~ 10

Author(s):

Paras Kumar Mishra ◽

Bashisth Narayan Singh

Keyword(s):

Male Sterility ◽

X Chromosome ◽

Phylogenetic Relationships ◽

Species Complex ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Drosophila Bipectinata ◽

Single Marker ◽

Drosophila Bipectinata Species Complex ◽

Rule Out

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.

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Genetic Dissection of Hybrid Incompatibilities BetweenDrosophila simulansandD. mauritiana. II. Mapping Hybrid Male Sterility Loci on the Third Chromosome

Genetics ◽

10.1093/genetics/164.4.1399 ◽

2003 ◽

Vol 164 (4) ◽

pp. 1399-1418 ◽

Cited By ~ 13

Author(s):

Yun Tao ◽

Zhao-Bang Zeng ◽

Jian Li ◽

Daniel L Hartl ◽

Cathy C Laurie

Keyword(s):

Male Sterility ◽

Small Region ◽

Interval Mapping ◽

Genetic Dissection ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

The Third ◽

Gradual Evolution ◽

Trait Locus ◽

High Level

AbstractHybrid male sterility (HMS) is a rapidly evolving mechanism of reproductive isolation in Drosophila. Here we report a genetic analysis of HMS in third-chromosome segments of Drosophila mauritiana that were introgressed into a D. simulans background. Qualitative genetic mapping was used to localize 10 loci on 3R and a quantitative trait locus (QTL) procedure (multiple-interval mapping) was used to identify 19 loci on the entire chromosome. These genetic incompatibilities often show dominance and complex patterns of epistasis. Most of the HMS loci have relatively small effects and generally at least two or three of them are required to produce complete sterility. Only one small region of the third chromosome of D. mauritiana by itself causes a high level of infertility when introgressed into D. simulans. By comparison with previous studies of the X chromsome, we infer that HMS loci are only ∼40% as dense on this autosome as they are on the X chromosome. These results are consistent with the gradual evolution of hybrid incompatibilities as a by-product of genetic divergence in allopatric populations.

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Genetic analysis of hybrid sterility in crosses of the tsetse flies Glossina palpalis palpalis and Glossina palpalis gambiensis (Diptera: Glossinidae)

Canadian Journal of Zoology ◽

10.1139/z97-133 ◽

1997 ◽

Vol 75 (7) ◽

pp. 1109-1117 ◽

Cited By ~ 12

Author(s):

R. H. Gooding

Keyword(s):

Linkage Group ◽

Male Sterility ◽

X Chromosome ◽

Sex Chromosomes ◽

Hybrid Sterility ◽

Glossina Palpalis Palpalis ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Reciprocal Crosses ◽

Glossina Palpalis

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.

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

Genetics ◽

10.1093/genetics/134.1.251 ◽

1993 ◽

Vol 134 (1) ◽

pp. 251-260 ◽

Cited By ~ 2

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.

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

Genetics ◽

10.1093/genetics/137.1.191 ◽

1994 ◽

Vol 137 (1) ◽

pp. 191-199 ◽

Cited By ~ 2

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.

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Hybrid Male Sterility in Rice Is Due to Epistatic Interactions with a Pollen Killer Locus

Genetics ◽

10.1534/genetics.111.132035 ◽

2011 ◽

Vol 189 (3) ◽

pp. 1083-1092 ◽

Cited By ~ 28

Author(s):

Takahiko Kubo ◽

Atsushi Yoshimura ◽

Nori Kurata

Keyword(s):

Male Sterility ◽

Hybrid Male ◽

Hybrid Male Sterility ◽

Epistatic Interactions

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