Genetic linkage between a sexually selected trait and X chromosome meiotic drive

Previous studies on the stalk-eyed fly, Cyrtodiopsis dalmanni , have shown that males with long eye-stalks win contests and are preferred by females, and artificial selection on male relative eye span alters brood sex-ratios. Subsequent theory proposes that X-linked meiotic drive can catalyse the evolution of mate preferences when drive is linked to ornament genes. Here we test this prediction by mapping meiotic drive and quantitative trait loci (QTL) for eye span. To map QTL we genotyped 24 microsatellite loci using 1228 F2 flies from two crosses between lines selected for long or short eye span. The crosses differed by presence or absence of a drive X chromosome, X D , in the parental male. Linkage analysis reveals that X D dramatically reduces recombination between X and X D chromosomes. In the X D cross, half of the F2 males carried the drive haplotype, produced partially elongated spermatids and female-biased broods, and had shorter eye span. The largest QTL mapped 1.3 cM from drive on the X chromosome and explained 36% of the variation in male eye span while another QTL mapped to an autosomal region that suppresses drive. These results indicate that selfish genetic elements that distort the sex-ratio can influence the evolution of exaggerated traits.

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Transposable element control disrupted by meiotic drive in a stalk-eyed fly genome

10.1101/2020.09.23.310227 ◽

2020 ◽

Author(s):

Josephine A Reinhardt ◽

Richard H. Baker ◽

Aleksey V. Zimin ◽

Chloe Ladias ◽

Kimberly A Paczolt ◽

...

Keyword(s):

Sex Ratio ◽

Transposable Element ◽

X Chromosome ◽

Meiotic Drive ◽

Genetic Elements ◽

Selfish Genetic Elements ◽

Genome Defense ◽

Genomic Divergence ◽

Pirna Pathway ◽

Female Carriers

AbstractSome stalk-eyed flies in the genus Teleopsis carry selfish genetic elements that induce sex ratio (SR) meiotic drive and impact the fitness of male and female carriers. Here, we produce a chromosome-level genome assembly of the stalk-eyed fly, T. dalmanni, to elucidate the pattern of genomic divergence associated with the presence of drive elements. We find evidence for multiple nested inversions along the sex ratio haplotype and widespread differentiation and divergence between the inversion types along the entire X chromosome. In addition, the genome contains tens of thousands of transposable element (TE) insertions and hundreds of transcriptionally active TE families that have produced new insertions. Moreover, we find that many TE families are expressed at a significantly higher level in SR male testis, suggesting a molecular connection between these two types of selfish genetic elements in this species. We identify T. dalmanni orthologs of genes involved in genome defense via the piRNA pathway, including core members maelstrom, piwi and Argonaute3, that are diverging in sequence, expression or copy number between the SR and standard (ST) chromosomes, and likely influence TE regulation in flies carrying a sex ratio X chromosome.

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Genetic linkage analysis of the X chromosome in autism, with emphasis on the fragile X region

Psychiatric Genetics ◽

10.1097/00041444-200506000-00004 ◽

2005 ◽

Vol 15 (2) ◽

pp. 83-90 ◽

Cited By ~ 25

Author(s):

John B. Vincent ◽

Georg Melmer ◽

Patrick F. Bolton ◽

Steve Hodgkinson ◽

Debbie Holmes ◽

...

Keyword(s):

Linkage Analysis ◽

X Chromosome ◽

Genetic Linkage ◽

Fragile X ◽

Genetic Linkage Analysis

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Sex-ratio meiotic drive in Drosophila simulans: cellular mechanism, candidate genes and evolution

Biochemical Society Transactions ◽

10.1042/bst0340562 ◽

2006 ◽

Vol 34 (4) ◽

pp. 562-565 ◽

Cited By ~ 13

Author(s):

C. Montchamp-Moreau

Keyword(s):

Sex Ratio ◽

X Chromosome ◽

Natural Populations ◽

Meiotic Drive ◽

Female Offspring ◽

Drosophila Simulans ◽

X Chromosomes ◽

Individual Fitness ◽

Primary Sex Ratio ◽

Intragenomic Conflict

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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Faculty Opinions recommendation of Genetic linkage between a sexually selected trait and X chromosome meiotic drive.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1028728.342274 ◽

2005 ◽

Author(s):

Nina Wedell

Keyword(s):

X Chromosome ◽

Genetic Linkage ◽

Meiotic Drive

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PRELIMINARY CHARACTERIZATION OF "SEX RATIO" AND REDISCOVERY AND REINTERPRETATION OF "MALE SEX RATIO" IN DROSOPHILA AFFINIS

Genetics ◽

10.1093/genetics/71.4.597 ◽

1972 ◽

Vol 71 (4) ◽

pp. 597-606

Author(s):

Robert A Voelker

Keyword(s):

Sex Ratio ◽

Y Chromosome ◽

X Chromosome ◽

Sex Ratios ◽

Meiotic Drive ◽

General Consideration ◽

Female Progeny ◽

Chromosome Sequence ◽

Male Sex

ABSTRACT In D. affinis "sex ratio" (sr), a form of meiotic drive characterized by the production of mostly or only female progeny by certain males, is associated with two different X chromosome sequences, XS-I XL-II and XS-II XL-IV. The behavior of the two sequences differed, depending on the Y chromosome constitution, being either Y L or 0. Males with sequence XS-II XL-IV and Y L produced progenies with nearly normal sex ratios; males with the same X chromosome sequence but in the absence of a Y chromosome in some cases gave progenies with nearly normal sex ratios but in other cases gave progenies which tended toward phenotypic sr. Males with sequence XS-I XL-II and Y L gave progenies which were characteristically sr (0.97–0.98 females); in the absence of a Y chromosome males with this sequence produced progenies which were virtually all-male. This latter finding is presumably identical to Novitski's (1947) "male sex ratio" (msr). The interpretation offered here attributes msr to an interaction between sr sequence XS-I XL-II and the 0 condition. A general consideration of the available data on sr in D. affinis is presented.

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X-linked CNV and skewed X-chromosome inactivation

Nauchno-prakticheskii zhurnal «Medicinskaia genetika» ◽

10.25557/2073-7998.2020.03.19-21 ◽

2020 ◽

pp. 19-21

Author(s):

Е.А. Фонова ◽

Е.Н. Толмачева ◽

А.А. Кашеварова ◽

М.Е. Лопаткина ◽

К.А. Павлова ◽

...

Keyword(s):

Cell Proliferation ◽

Intellectual Disability ◽

X Chromosome ◽

Copy Number ◽

Copy Number Variations ◽

X Chromosome Inactivation ◽

Chromosome Inactivation ◽

Chromosome X ◽

Skewed X Chromosome Inactivation

Смещение инактивации Х-хромосомы может быть следствием и маркером нарушения клеточной пролиферации при вариациях числа копий ДНК на Х-хромосоме. Х-сцепленные CNV выявляются как у женщин с невынашиванием беременности и смещением инактивации Х-хромосомы (с частотой 33,3%), так и у пациентов с умственной отсталостью и смещением инактивацией у их матерей (с частотой 40%). A skewed X-chromosome inactivation can be a consequence and a marker of impaired cell proliferation in the presence of copy number variations (CNV) on the X chromosome. X-linked CNVs are detected in women with miscarriages and a skewed X-chromosome inactivation (with a frequency of 33.3%), as well as in patients with intellectual disability and skewed X-chromosome inactivation in their mothers (with a frequency of 40%).

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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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Sex Chromosome Meiotic Drive in Stalk-Eyed Flies

Genetics ◽

10.1093/genetics/147.3.1169 ◽

1997 ◽

Vol 147 (3) ◽

pp. 1169-1180 ◽

Cited By ~ 6

Author(s):

Daven C Presgraves ◽

Emily Severance ◽

Gerald S Willrinson

Keyword(s):

Sex Ratio ◽

Sex Chromosome ◽

Sex Ratios ◽

Natural Populations ◽

Meiotic Drive ◽

Operational Sex Ratio ◽

Genetic Modifiers ◽

Ratio Distortion ◽

The Impact ◽

Sex Ratio Distortion

Meiotically driven sex chromosomes can quickly spread to fixation and cause population extinction unless balanced by selection or suppressed by genetic modifiers. We report results of genetic analyses that demonstrate that extreme female-biased sex ratios in two sister species of stalk-eyed flies, Cyrtodiopsis dalmanni and C. whitei, are due to a meiotic drive element on the X chromosome (Xd). Relatively high frequencies of Xd in C. dalmanni and C. whitei (13–17% and 29%, respectively) cause female-biased sex ratios in natural populations of both species. Sex ratio distortion is associated with spermatid degeneration in male carriers of Xd. Variation in sex ratios is caused by Y-linked and autosomal factors that decrease the intensity of meiotic drive. Y-linked polymorphism for resistance to drive exists in C. dalmanni in which a resistant Y chromosome reduces the intensity and reverses the direction of meiotic drive. When paired with Xd, modifying Y chromosomes (Ym) cause the transmission of predominantly Y-bearing sperm, and on average, production of 63% male progeny. The absence of sex ratio distortion in closely related monomorphic outgroup species suggests that this meiotic drive system may predate the origin of C. whitei and C. dalmanni. We discuss factors likely to be involved in the persistence of these sex-linked polymorphisms and consider the impact of Xd on the operational sex ratio and the intensity of sexual selection in these extremely sexually dimorphic flies.

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