Distinct spermiogenic phenotypes underlie sperm elimination in the Segregation Distorter meiotic drive system

Segregation Distorter (SD) is a male meiotic drive system in Drosophila melanogaster. Males heterozygous for a selfish SD chromosome rarely transmit the homologous SD+ chromosome. It is well established that distortion results from an interaction between Sd, the primary distorting locus on the SD chromosome and its target, a satellite DNA called Rsp, on the SD+ chromosome. However, the molecular and cellular mechanisms leading to post-meiotic SD+ sperm elimination remain unclear. Here we show that SD/SD+ males of different genotypes but with similarly strong degrees of distortion have distinct spermiogenic phenotypes. In some genotypes, SD+ spermatids fail to fully incorporate protamines after the removal of histones, and degenerate during the individualization stage of spermiogenesis. In contrast, in other SD/SD+ genotypes, protamine incorporation appears less disturbed, yet spermatid nuclei are abnormally compacted, and mature sperm nuclei are eventually released in the seminal vesicle. Our analyses of different SD+ chromosomes suggest that the severity of the spermiogenic defects associates with the copy number of the Rsp satellite. We propose that when Rsp copy number is very high (> 2000), spermatid nuclear compaction defects reach a threshold that triggers a checkpoint controlling sperm chromatin quality to eliminate abnormal spermatids during individualization.

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Examination of a mutable system affecting the components of the segregation distorter meiotic drive system of Drosophila melanogaster.

Genetics ◽

10.1093/genetics/125.1.51 ◽

1990 ◽

Vol 125 (1) ◽

pp. 51-76

Author(s):

K G Golic

Keyword(s):

Drosophila Melanogaster ◽

Transposable Element ◽

X Chromosome ◽

Segregation Distortion ◽

Chromosomal Rearrangements ◽

Meiotic Drive ◽

Drive System ◽

Partial Loss ◽

Segregation Distorter ◽

Relationship Of

Abstract Segregation distortion in Drosophila melanogaster is the result of an interaction between the genetic elements Sd, a Rsp sensitive to Sd, and an array of modifiers, that results in the death of sperm carrying Rsp. A stock (designated M-5; cn bw) has been constructed which has the property of inducing the partial loss of sensitivity from previously sensitive cn bw chromosomes, the partial loss of distorting ability from SD chromosomes, and a concomitant acquisition of modifiers on the X chromosome and possibly also on the autosomes. By several criteria the changes exhibited under the influence of M-5; cn bw are characteristic of the transposable-element systems which produce hybrid dysgenesis. In the first place, the magnitude of these effects depends on the nature of the crosses performed. The analogy is further strengthened by the observation that the changes induced by M-5; cn bw share other stigmata of Drosophila transposable-element systems, including high sterility among the progeny of outcrosses, and the production of chromosomal rearrangements. The possible relationship of this system to the P, I and hobo transposable element systems is discussed, as well as its bearing on aspects of the Segregation Distorter phenomenon which have yet to be explained.

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Transposition of the Responder element (Rsp) of the Segregation distorter system (SD) to the X chromosome in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/122.1.81 ◽

1989 ◽

Vol 122 (1) ◽

pp. 81-86 ◽

Cited By ~ 1

Author(s):

E S Walker ◽

T W Lyttle ◽

J C Lucchesi

Keyword(s):

Drosophila Melanogaster ◽

Y Chromosome ◽

X Chromosome ◽

Meiotic Drive ◽

Genetic System ◽

Drive System ◽

Potential Utility ◽

X Chromosomes ◽

Large Numbers ◽

Segregation Distorter

Abstract In order to test whether the meiotic drive system Segregation distorter (SD) can operate on the X chromosome to exclude it from functional sperm, we have transposed the Responder locus (Rsp) to this element. This was accomplished by inducing detachments of a compound-X chromosome in females carrying a Y chromosome bearing a Rsps allele. Six Responder-sensitive-bearing X chromosomes, with kappa values ranging from 0.90 to 1.00, were established as permanent lines. Two of these have been characterized more extensively with respect to various parameters affecting meiotic drive. SD males with a Responder-sensitive X chromosome produce almost exclusively male embryos, while those with a Rsp-Y chromosome produce almost exclusively female embryos. This provides a genetic system of great potential utility for the study of early sex-specific differentiation events as it allows the collection of large numbers of embryos of a given sex.

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MULTIPLE MEIOTIC DRIVE SYSTEMS IN THE DROSOPHILA MELANOGASTER MALE

Genetics ◽

10.1093/genetics/72.1.105 ◽

1972 ◽

Vol 72 (1) ◽

pp. 105-115

Author(s):

George L Gabor Miklos ◽

Armon F Yanders ◽

W J Peacock

Keyword(s):

Drosophila Melanogaster ◽

Survival Probability ◽

Sex Chromosome ◽

Meiotic Drive ◽

The Other ◽

Segregation Distorter ◽

Two Systems ◽

Combined Action ◽

Drive Systems

ABSTRACT The behaviour of two "meiotic drive" systems, Segregation-Distorter (SD) and the sex chromosome sc4sc8 has been examined in the same meiocyte. It has been found that the two systems interact in a specific way. When the distorting effects of SD and sc4sc8 are against each other, there is no detectable interaction. Each system is apparently oblivious to the presence of the other, gametes being produced according to independence expectations. However when the affected chromosomes are at the same meiotic pole an interaction occurs; the survival probability of the gamete containing both distorted chromosomal products is increased, rather than being decreased by the combined action of two systems.

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MEIOTIC DRIVE IN NATURAL POPULATIONS OF DROSOPHILA MELANOGASTER. III. POPULATIONAL IMPLICATIONS OF THE SEGREGATION-DISTORTER LOCUS,

Evolution ◽

10.1111/j.1558-5646.1960.tb03111.x ◽

1960 ◽

Vol 14 (4) ◽

pp. 433-444

Author(s):

Yuichiro Hiraizumi ◽

L. Sandler ◽

James F. Crow

Keyword(s):

Drosophila Melanogaster ◽

Natural Populations ◽

Meiotic Drive ◽

Segregation Distorter ◽

Distorter Locus

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On the components of segregation distortion in Drosophila melanogaster. V. Molecular analysis of the Sd locus.

Genetics ◽

10.1093/genetics/129.1.133 ◽

1991 ◽

Vol 129 (1) ◽

pp. 133-144 ◽

Cited By ~ 7

Author(s):

P A Powers ◽

B Ganetzky

Keyword(s):

Drosophila Melanogaster ◽

Sequence Analysis ◽

Molecular Analysis ◽

Tandem Duplication ◽

Meiotic Drive ◽

Northern Blots ◽

Sequence Identity ◽

Naturally Occurring ◽

Segregation Distorter ◽

Genomic Probes

Abstract Segregation Distorter (SD) is a naturally occurring meiotic drive system comprising at least three distinct loci: Sd, Rsp and E(SD). Heterozygous SD/SD+ males transmit the SD chromosome in vast excess over the normal homolog. The distorted transmission involves the induced dysfunction of the spermatids that receive the SD+ chromosome. In the 220-kb region of DNA that contains the Sd gene, we identified a 5-kb tandem duplication that is uniquely associated with all SD chromosomes, absent in SD+ chromosomes, and detectably altered in Sd revertants. On northern blots, genomic probes from the tandem duplication detect an SD-specific 4-kb transcript in addition to several smaller transcripts present in both SD and SD+. Seven classes of cDNAs derived from these transcripts have been isolated. All of these cDNAs share extensive sequence identity at their 3' ends but differ at their 5' ends. Sequence analysis indicates that these cDNAs potentially encode four distinct, but related, polypeptides. Introduction of the tandem duplication into SD+ flies by germline transformation did not confer the dominant gain-of-function Sd phenotype. This result, taken together with our analysis of the Sd cDNAs, suggests that the duplication is part of a much larger gene that encodes several different polypeptides.

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ON THE COMPONENTS OF SEGREGATION DISTORTION IN DROSOPHILA MELANOGASTER. III. NATURE OF ENHANCER OF SD

Genetics ◽

10.1093/genetics/107.3.423 ◽

1984 ◽

Vol 107 (3) ◽

pp. 423-434

Author(s):

John G Brittnacher ◽

Barry Ganetzky

Keyword(s):

Drosophila Melanogaster ◽

Segregation Distortion ◽

Allelic Variation ◽

Meiotic Drive ◽

Dependent Manner ◽

X Ray ◽

Segregation Distorter ◽

In Cis ◽

General Component

ABSTRACT Analysis of X-ray-induced deletions in the Segregation Distorter (SD) chromosome, SD-5, revealed that this chromosome had a gene proximal to lt in the centric heterochromatin of 2L that strongly enhanced the meiotic drive caused by the SD chromosome. This Enhancer of Segregation Distortion [E(SD)] locus had not been characterized in earlier studies of SD chromosomes because it cannot be readily separated by recombination from the Responder (Rsp) locus in the proximal heterochromatin of 2R.—To determine whether E(SD) is a general component of all SD chromosomes and to examine further its effects on distortion, we produced deletions of E(SD) in three additional SD chromosomes. Analysis of these deletions leads to the following conclusions: (1) along with Sd and Rsp, E(SD) is common to all SD chromosomes; (2) the E(SD) allele on each SD chromosome enhances distortion by the same amount, which indicates that allelic variation at the E(SD) locus is not responsible for the different drive strengths seen among SD chromosomes; (3) E(SD) causes very little or no distortion by itself in the absence of Sd; (4) E(SD), like Sd, acts in a dosage-dependent manner; (5) E(SD) exerts its effect in cis or trans to Sd; and (6) if E(SD) + exists, its function is not related to SD.

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Rapid Evolution of a Coadapted Gene Complex: Evidence From the Segregation Distorter (SD) System of Meiotic Drive in Drosophila melanogaster

Genetics ◽

10.1093/genetics/143.4.1675 ◽

1996 ◽

Vol 143 (4) ◽

pp. 1675-1688 ◽

Cited By ~ 1

Author(s):

Michael F Palopoli ◽

Chung-I Wu

Keyword(s):

Drosophila Melanogaster ◽

Rapid Evolution ◽

Natural Populations ◽

Meiotic Drive ◽

Pericentromeric Region ◽

Genomic Region ◽

Gene Complex ◽

Segregation Distorter ◽

Normal Homologue ◽

Coadapted Gene Complex

Abstract Segregation Distorter (SD) is a system of meiotic drive found in natural populations of Drosophila melanogaster. Males heterozygous for an SD second chromosome and a normal homologue (SD +) produce predominantly SD-bearing sperm. The coadapted gene complex responsible for this transmission advantage spans the second chromosome centromere, consisting of three major and several minor interacting loci. To investigate the evolutionary history of this system, we surveyed levels of polymorphism and divergence at six genes that together encompass this pericentromeric region and span seven map units. Interestingly, there was no discernible divergence between SD and SD + chromosomes for any of these molecular markers. Furthermore, SD chromosomes harbored much less polymorphism than did SD + chromosomes. The results suggest that the SD system evolved recently, swept to appreciable frequencies worldwide, and carried with it the entire second chromosome centromeric region (roughly 10% of the genome). Despite its well-documented genetic complexity, this coadapted system appears to have evolved on a time scale that is much shorter than can be gauged using nucleotide substitution data. Finally, the large genomic region hitchhiking with SD indicates that a multilocus, epistatically selected system could affect the levels of DNA polymorphism observed in regions of reduced recombination.

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