Cytological Basis of "Sex Ratio" in
 Drosophila pseudoobscura

Novitski, E.; Peacock, W. J.; Engel, James Douglas

doi:10.1126/science.148.3669.516

Cited by 46 publications

(21 citation statements)

References 10 publications

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“…The meiotic drive system in Drosophila males can be classified by the timing of primary disorders which lead to sperm dysfunction: a meiotic defect in sex-ratio males (Novitski et al, 1965;Peacock et al, 1975;Cazemajor et al, 2000), a spermatid maturation defect in Segregation Distorter (Tokuyasu et al, 1977), and a sperm storage defect in females inseminated by C(2)EN/O males (Dernburg et al, 1996). In this study, we used sex chromosomespecific probes in FISH of spermatid chromosomes and directly demonstrated that those spermatids containing a Y chromosome exclusively failed to elongate in exf males.…”

Section: Discussionmentioning

confidence: 99%

“…This spermiogenic phenotype seems to be a secondary defect of meiotic failure, such as chromatin bridge or degeneration of the Y chromosome (Novitski et al, 1965;Peacock et al, 1975;Cazemajor et al, 2000). In exf males, meiotic division appeared to be normal and the primary defect was detected during post-meiotic development.…”

Section: Spermiogenic Failure In Drosophila Meiotic Drivementioning

confidence: 99%

“…It is generally found that females mated with sex-ratio males produce fewer sons, and this female-biased sex-ratio trait is assumed to result from loss or dysfunction of Y-sperm. Indeed, some studies show that sex-ratio males exhibit nondisjunction or degeneration of the Y chromosome during meiosis (Novitski et al, 1965;Cazemajor et al, 2000). In addition, disorganization and reduction of spermatids during spermiogenesis has been commonly observed in sex-ratio males (Policansky and Ellison, 1970;Hauschteck-Jungen and Maurer, 1976;Cobbs et al, 1991;MontchampMoreau and Joly, 1997).…”

Section: Introductionmentioning

confidence: 99%

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Elimination of Y chromosome-bearing spermatids during spermiogenesis in an autosomal sex-ratio mutant of Drosophila simulans

2013

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Sex ratio distortion, which is commonly abbreviated as sex-ratio, has been studied in many Drosophila species, but the mechanism remains largely unknown. Here, we report on the sex-ratio mutant of D. simulans named excess of females (exf). The third chromosomal recessive mutation results in a sex ratio of approximately 0.2 or less (males/total). Cytological observation demonstrated that meiosis appeared to be completed normally, but that most Y chromosome-bearing nuclei failed to elongate during spermiogenesis, as revealed by fluorescence in situ hybridization using sex chromosome-specific probes. These aberrant nuclei contained membranous inclusions as revealed by electron microscopic analysis. Most of the aberrant exf spermatids failed to individualize and mature, suggesting that a later stage of spermiogenesis is involved in prevention of production of sperm with abnormal morphology. On the one hand, in exf seminal vesicles, sperm nuclei with a length of 5-8.5 μm were occasionally observed, in addition to those with wild-type sperm dimensions, that is, a length of approximately 10 μm. Thus, spermatids with less severe nuclear defects can escape elimination and be released into the seminal vesicles as mature sperm. Furthermore, we constructed His2AvD-GFP and ProtamineB-eGFP transgenic lines in D. simulans, and examined the processes involved in replacement of chromatin proteins over a time course, according to nuclear morphology. We found that both normal and abnormal sperm heads demonstrated equal chromatin replacement during late spermiogenesis. Our results suggest that exf belongs to a unique class of meiotic drive systems in that (1) intranuclear membranous inclusions cause failure of nuclear shaping of Y-bearing spermatids without affecting the histone-protamine transition, and (2) a portion of the aberrant spermatids differentiate into mature sperm; these are transferred to and stored by females.

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Section: Discussionmentioning

confidence: 99%

Section: Spermiogenic Failure In Drosophila Meiotic Drivementioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Elimination of Y chromosome-bearing spermatids during spermiogenesis in an autosomal sex-ratio mutant of Drosophila simulans

2013

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“…Further details of these accumulation mechanisms, and of some other lesser known ones, are described in Jones and Rees (1982). In the wider context an analogy can be drawn between the drive mechanisms operating in B chromosome systems and those found for some other kinds of genetic elements located within the A chromosome complement. Mechanisms of meiotic drive in this wider sense, as reviewed by Zimmering et al (1970), involve various components of the A chromosome genome ranging from whole chromosomes, e.g., the X chromosome in some Drosophila groups (Novitski et a!., 1965); or parts of chromosomes, as in the preferential segregation to the functional megaspore of the large heterochromatic knob on abnormal chromosome 10 of maize (Rhoades, 1952), down to the level of the classic t allele polymorphism in natural populations of the house mouse, Mus musculus (Dun, 1953;Lewontin, 1968). In homozygous recessive combinations the t alleles are either lethal or they cause complete sterility-yet they are found in natural populations at high frequency.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of the B-chromosome polymorphism in rye. I. simulated populations

Matthews

Jones

1982

Heredity

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A computer model has been developed to simulate the transmission characteristics of the B chromosomes in rye, and to provide a basis on which to identify, and to understand, the main factors responsible for determining the equilibrium B-frequency levels in open pollinating populations. The model has been devised by expressing the behaviour of the Bs, at various phases of the life cycle, in terms of mathematical equations. These equations contain parameters which determine the behaviour of the Bs at meiosis, pollen grain (and egg cell) mitosis and during the development of gametes and sporophytes.By exploring a range of values for the parameters it has been possible to ascertain that variation in the amount of meiotic elimination of Bs, as well as in their direction rate during nondisjunction in the pollen grain and egg cell, influence the final B-frequency equilibrium. Variation in the rate of nondisjunction on the other hand, affects the number of generations required to attain equilibrium more than the final equilibrium itself. Selection against gametes and plants containing Bs, even at levels which are higher than can reasonably be expected to occur naturally, cannot prevent the accumulation of Bs within populations, provided that high rates of directed nondisjunction are also occurring.The results are discussed in relation to the B chromosome polymorphism in natural populations of rye.

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“…Failure of Y-chromatids to properly segregate at meiosis II is also seen in the Drosophila pseudoobscura SR system (27); in the D. simulans Winters sex-ratio system chromatin fails to condense in the head of developing Y-bearing spermatids (19). In this context, it is notable that the D. melanogaster Y chromosome has acquired a new gene predicted to organize heterochromatin (28).…”

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confidence: 98%

Heterochromatin and genetic conflict

Meiklejohn¹

2016

Proc. Natl. Acad. Sci. U.S.A.

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Meiosis is a dangerous business. The two alleles in diploid organisms share an evolutionary interest in the survival and reproduction of their host individual; however, as soon as they segregate into haploid gametes, these alleles find themselves competing for transmission to the next generation (1). In males, the development of all four meiotic products into functional gametes fosters the evolution of alleles that disrupt the development or viability of gametes carrying the alternate allele. Systems that distort Mendelian segregation (hence, segregation distorters) typically comprise at least two loci: a trans-acting drive locus (such as a gene that encodes a poison) that targets alleles that are sensitive to the poison at a second, linked locus (2). A major impediment to the evolution of segregation distorters is the requirement that the poisonous allele be tightly linked to resistant alleles at the target locus; otherwise, distorters will commit suicide when paired with a sensitive allele (3). As a result, segregation distorters on autosomes are invariably associated with inversions that suppress recombination between the distorter and target loci. In contrast, heteromorphic sex chromosomes, where the Y chromosome is highly degenerated, can facilitate the evolution of segregation distorters because the X and Y frequently share little homologous sequence and do not recombine along most or all of their length. Thus, sex-chromosome segregation distorters that distort the sex ratio of the progeny of males that carry them (hence, sex-ratio distorters) are predicted to evolve frequently (4). The presence of sex-ratio distorters in populations selects for resistant Y chromosomes and autosomal suppressors that restore male fertility and a balanced sex ratio, and may lead to either balanced polymorphisms or open-ended arms races between loci that function in the male germ line (5). A recent study in PNAS has identified a gene required for sex-ratio distortion in Drosophila simulans (6), providing novel insight into the genetic and molecular mechanisms used by these selfish elements and their effects on genome evolution and species formation.The recurrent evolution of sex-ratio distorters and suppressors may contribute to otherwise puzzling observations regarding the genetics and evolution of spermatogenesis in animals with XY sex chromosomes. First, at least 10% of protein-coding genes in the Drosophila melanogaster genome are expressed solely in the male germ line, and ∼two-thirds of all D. melanogaster genes whose expression is restricted to a single tissue are expressed specifically in testes. In contrast, less than 1% of the D. melanogaster genome is specified for function during oogenesis (7). Thus, in Drosophila, an extraordinarily large fraction of the genome is dedicated to spermatogenesis. Second, in both Diptera and mammals, testis-specific genes show exceptionally high rates of regulatory and protein sequence evolution (8, 9), comprise the majority of new lineage-or species-specific genes (10), and these ne...

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Cytological Basis of "Sex Ratio" in Drosophila pseudoobscura

Cited by 46 publications

References 10 publications

Elimination of Y chromosome-bearing spermatids during spermiogenesis in an autosomal <i>sex-ratio</i> mutant of <i>Drosophila simulans</i>

Elimination of Y chromosome-bearing spermatids during spermiogenesis in an autosomal <i>sex-ratio</i> mutant of <i>Drosophila simulans</i>

Dynamics of the B-chromosome polymorphism in rye. I. simulated populations

Heterochromatin and genetic conflict

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