X-chromosome meiotic drive in Drosophila simulans: a QTL approach reveals the complex polygenic determinism of Paris drive suppression

The sex-ratio trait, reported in a dozen Drosophila species, is a type of naturally occurring meiotic drive in which the driving elements are located on the X chromosome. Typically, as the result of a shortage of Y-bearing spermatozoa, males carrying a sex-ratio X chromosome produce a large excess of female offspring. The presence of sex-ratio chromosomes in a species can have considerable evolutionary consequences, because they can affect individual fitness and trigger extended intragenomic conflict. Here, I present the main results of the study performed in Drosophila simulans. In this species, the loss of Y-bearing spermatozoa is related to the inability of the Y chromosome sister-chromatids to separate properly during meiosis II. Fine genetic mapping has shown that the primary sex-ratio locus on the X chromosome contains two distorter elements acting synergistically, both of which are required for drive expression. One element has been genetically mapped to a tandem duplication. To infer the natural history of the trait, the pattern of DNA sequence polymorphism in the surrounding chromosomal region is being analysed in natural populations of D. simulans harbouring sex-ratio X chromosomes. Initial results have revealed the recent spread of a distorter allele.

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XChromosome Effect on Maternal Recombination and Meiotic Drive in the Mouse

Genetics ◽

10.1093/genetics/161.4.1651 ◽

2002 ◽

Vol 161 (4) ◽

pp. 1651-1659 ◽

Cited By ~ 4

Author(s):

Elena de la Casa-Esperón ◽

J Concepción Loredo-Osti ◽

Fernando Pardo-Manuel de Villena ◽

Tammi L Briscoe ◽

Jan Michel Malette ◽

...

Keyword(s):

Mouse Chromosome ◽

X Chromosome ◽

Meiotic Recombination ◽

Meiotic Drive ◽

X Chromosome Inactivation ◽

Chromosome Inactivation ◽

Chromosome 11 ◽

Genome Wide ◽

Mouse Chromosome 11 ◽

Segregation Of Chromosomes

AbstractWe observed that maternal meiotic drive favoring the inheritance of DDK alleles at the Om locus on mouse chromosome 11 was correlated with the X chromosome inactivation phenotype of (C57BL/ 6-Pgk1a × DDK)F1 mothers. The basis for this unexpected observation appears to lie in the well-documented effect of recombination on meiotic drive that results from nonrandom segregation of chromosomes. Our analysis of genome-wide levels of meiotic recombination in females that vary in their X-inactivation phenotype indicates that an allelic difference at an X-linked locus is responsible for modulating levels of recombination in oocytes.

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Reduced Polymorphism Associated with X Chromosome Meiotic Drive in the Stalk-Eyed Fly Teleopsis dalmanni

PLoS ONE ◽

10.1371/journal.pone.0027254 ◽

2011 ◽

Vol 6 (11) ◽

pp. e27254 ◽

Cited By ~ 9

Author(s):

Sarah J. Christianson ◽

Cara L. Brand ◽

Gerald S. Wilkinson

Keyword(s):

X Chromosome ◽

Meiotic Drive

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DoesStellateCause Meiotic Drive inDrosophila melanogaster?

Genetics ◽

10.1093/genetics/161.4.1551 ◽

2002 ◽

Vol 161 (4) ◽

pp. 1551-1559 ◽

Cited By ~ 1

Author(s):

Massimo Belloni ◽

Patrizia Tritto ◽

Maria Pia Bozzetti ◽

Gioacchino Palumbo ◽

Leonard G Robbins

Keyword(s):

Drosophila Melanogaster ◽

Y Chromosome ◽

X Chromosome ◽

Evolutionary History ◽

Active Element ◽

Meiotic Drive

AbstractDrosophila melanogaster males deficient for the crystal (cry) locus of the Y chromosome that carry between 15 and 60 copies of the X-linked Stellate (Ste) gene are semisterile, have elevated levels of nondisjunction, produce distorted sperm genotype ratios (meiotic drive), and evince hyperactive transcription of Ste in the testes. Ste seems to be the active element in this system, and it has been proposed that the ancestral Ste gene was “selfish” and increased in frequency because it caused meiotic drive. This hypothetical evolutionary history is based on the idea that Ste overexpression, and not the lack of cry, causes the meiotic drive of cry– males. To test whether this is true, we have constructed a Ste-deleted X chromosome and examined the phenotype of Ste–/cry– males. If hyperactivity of Ste were necessary for the transmission defects seen in cry– males, cry– males completely deficient for Ste would be normal. Although it is impossible to construct a completely Ste– genotype, we find that Ste–/cry– males have exactly the same phenotype as Ste+/cry– males. The deletion of all X chromosome Ste copies not only does not eliminate meiotic drive and nondisjunction, but it also does not even reduce them below the levels produced when the X carries 15 copies of Ste.

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Selective Sweeps in a 2-Locus Model for Sex-Ratio Meiotic Drive in Drosophila simulans

Molecular Biology and Evolution ◽

10.1093/molbev/msm269 ◽

2007 ◽

Vol 25 (2) ◽

pp. 409-416 ◽

Cited By ~ 16

Author(s):

Nicolas Derome ◽

Emmanuelle Baudry ◽

David Ogereau ◽

Michel Veuille ◽

Catherine Montchamp-Moreau

Keyword(s):

Sex Ratio ◽

Meiotic Drive ◽

Drosophila Simulans ◽

Selective Sweeps ◽

Locus Model

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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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Molecular signature of epistatic selection: interrogating genetic interactions in the sex-ratio meiotic drive of Drosophila simulans

Genetics Research ◽

10.1017/s0016672309000147 ◽

2009 ◽

Vol 91 (3) ◽

pp. 171-182 ◽

Cited By ~ 2

Author(s):

LUIS-MIGUEL CHEVIN ◽

HÉLOÏSE BASTIDE ◽

CATHERINE MONTCHAMP-MOREAU ◽

FRÉDÉRIC HOSPITAL

Keyword(s):

Sex Ratio ◽

Initial Conditions ◽

Meiotic Drive ◽

Real Data ◽

Genomic Region ◽

Drosophila Simulans ◽

Stochastic Simulations ◽

Molecular Signature ◽

Fine Scale ◽

Rich Data

SummaryFine scale analyses of signatures of selection allow assessing quantitative aspects of a species' evolutionary genetic history, such as the strength of selection on genes. When several selected loci lie in the same genomic region, their epistatic interactions may also be investigated. Here, we study how the neutral polymorphism pattern was shaped by two close recombining loci that cause ‘sex-ratio’ meiotic drive in Drosophila simulans, as an example of strong selection with potentially strong epistasis. We compare the polymorphism data observed in a natural population with the results of forward stochastic simulations under several contexts of epistasis between the candidate loci for the drive. We compute the likelihood of different possible scenarios, in order to determine which configuration is most consistent with the data. Our results highlight that fine scale analyses of well-chosen candidate genomic regions provide information-rich data that can be used to investigate the genotype–phenotype–fitness map, which can hardly be studied in genome-wide analyses. We also emphasize that initial conditions and time of observation (here, time after the interruption of a partial selective sweep) are crucial parameters in the interpretation of real data, while these are often overlooked in theoretical studies.

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