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

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 between a sexually selected trait and X chromosome meiotic drive

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2005.3183 ◽

2005 ◽

Vol 272 (1576) ◽

pp. 2097-2103 ◽

Cited By ~ 41

Author(s):

Philip M Johns ◽

L. LaReesa Wolfenbarger ◽

Gerald S Wilkinson

Keyword(s):

Sex Ratio ◽

Linkage Analysis ◽

X Chromosome ◽

Artificial Selection ◽

Genetic Linkage ◽

Meiotic Drive ◽

Mate Preferences ◽

Chromosome X ◽

Selfish Genetic Elements ◽

Autosomal Region

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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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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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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A kinesin Klp10A mediates cell cycle-dependent shuttling of Piwi between nucleus and nuage

10.1101/474049 ◽

2018 ◽

Author(s):

Zsolt G. Venkei ◽

Charlotte Choi ◽

Suhua Feng ◽

Steven E. Jacobsen ◽

John K. Kim ◽

...

Keyword(s):

Cell Cycle ◽

Transcriptional Silencing ◽

Central Spindle ◽

Genetic Elements ◽

Selfish Genetic Elements ◽

Transcript Cleavage ◽

Cycle Dependent ◽

Pirna Pathway

AbstractThe piRNA pathway protects germline genomes through transcript cleavage of selfish genetic elements, such as transposons, in the cytoplasm and their transcriptional silencing in the nucleus. Here, we describe a mechanism by which the nuclear and cytoplasmic arms of the silencing mechanism are linked. During mitosis of Drosophila spermatogonia, nuclear Piwi interacts with nuage, the compartment that mediates the cytoplasmic arm of piRNA-mediated silencing. At the end of mitosis, Piwi leaves nuage to return to the nucleus. We found that dissociation of Piwi from nuage occurs at the depolymerizing microtubules of the central spindle, mediated by a microtubule-depolymerizing kinesin Klp10A. Depletion of klp10A delays Piwi’s return to the nucleus and affects piRNA production, suggesting the importance of nuclear-cytoplasmic communication in piRNA biogenesis. We propose that cell cycle-dependent communication between the nuclear and cytoplasmic arms of the piRNA pathway plays important roles in coordinated piRNA production.

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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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Sex-ratio distorters and other selfish genetic elements: implications for biological control.

Genetics, evolution and biological control ◽

10.1079/9780851997353.0235 ◽

2009 ◽

pp. 235-252 ◽

Cited By ~ 5

Author(s):

R. Stouthamer

Keyword(s):

Biological Control ◽

Sex Ratio ◽

Genetic Elements ◽

Selfish Genetic Elements

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X-linked meiotic drive boosts population size and persistence

10.1101/2020.06.05.137224 ◽

2020 ◽

Author(s):

Carl Mackintosh ◽

Andrew Pomiankowski ◽

Michael F Scott

Keyword(s):

Extinction Risk ◽

Sex Ratios ◽

Full Range ◽

Meiotic Drive ◽

Population Level ◽

Genetic Elements ◽

Selfish Genetic Elements ◽

Population Sizes ◽

Selection For ◽

Male Carriers

ABSTRACTX-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Selection for these selfish sex chromosomes can lead to completely female populations, which cannot produce offspring and go extinct. However, at the population level, moderately female-biased sex ratios are optimal because relatively few males are required to fertilise all the females. We develop eco-evolutionary models for sex-linked meiotic drive alleles to investigate their full range of demographic effects. We find general conditions for the spread and fixation of X-drivers, accounting for transmission bias and other factors associated with the spread of X-drivers such as sperm competition and polyandry. Our results suggest driving X-alleles that do not reach fixation (or do not bias segregation excessively) will boost population sizes and persistence times by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. We suggest that researchers should look beyond extinction risk and consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

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X-linked meiotic drive can boost population size and persistence

Genetics ◽

10.1093/genetics/iyaa018 ◽

2020 ◽

Vol 217 (1) ◽

pp. 1-11

Author(s):

Carl Mackintosh ◽

Andrew Pomiankowski ◽

Michael F Scott

Keyword(s):

Population Size ◽

Sex Ratios ◽

Meiotic Drive ◽

Population Level ◽

Male Mating ◽

Genetic Elements ◽

Selfish Genetic Elements ◽

Sex Ratio Bias ◽

Ejaculate Size ◽

Male Mating Behavior

Abstract X-linked meiotic drivers cause X-bearing sperm to be produced in excess by male carriers, leading to female-biased sex ratios. Here, we find general conditions for the spread and fixation of X-linked alleles. Our conditions show that the spread of X-linked alleles depends on sex-specific selection and transmission rather than the time spent in each sex. Applying this logic to meiotic drive, we show that polymorphism is heavily dependent on sperm competition induced both by female and male mating behavior and the degree of compensation to gamete loss in the ejaculate size of drive males. We extend these evolutionary models to investigate the demographic consequences of biased sex ratios. Our results suggest driving X-alleles that invade and reach polymorphism (or fix and do not bias segregation excessively) will boost population size and persistence time by increasing population productivity, demonstrating the potential for selfish genetic elements to move sex ratios closer to the population-level optimum. However, when the spread of drive causes strong sex-ratio bias, it can lead to populations with so few males that females remain unmated, cannot produce offspring, and go extinct. This outcome is exacerbated when the male mating rate is low. We suggest that researchers should consider the potential for ecologically beneficial side effects of selfish genetic elements, especially in light of proposals to use meiotic drive for biological control.

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X-Linked Emery–Dreifuss Muscular Dystrophy: Study Of X-Chromosome Inactivation and Its Relation with Clinical Phenotypes in Female Carriers

Genes ◽

10.3390/genes10110919 ◽

2019 ◽

Vol 10 (11) ◽

pp. 919 ◽

Cited By ~ 1

Author(s):

Viggiano ◽

Madej-Pilarczyk ◽

Carboni ◽

Picillo ◽

Ergoli ◽

...

Keyword(s):

Muscular Dystrophy ◽

X Chromosome ◽

Clinical Symptoms ◽

Fibrous Tissue ◽

X Chromosome Inactivation ◽

Chromosome Inactivation ◽

Cardiac Conduction ◽

Asymptomatic Carriers ◽

Cardiac Symptoms ◽

Female Carriers

X-linked Emery–Dreifuss muscular dystrophy (EDMD1) affects approximately 1:100,000 male births. Female carriers are usually asymptomatic but, in some cases, they may present clinical symptoms after age 50 at cardiac level, especially in the form of conduction tissue anomalies. The aim of this study was to evaluate the relation between heart involvement in symptomatic EDMD1 carriers and the X-chromosome inactivation (XCI) pattern. The XCI pattern was determined on the lymphocytes of 30 symptomatic and asymptomatic EDMD1 female carriers—25 familial and 5 sporadic cases—seeking genetic advice using the androgen receptor (AR) methylation-based assay. Carriers were subdivided according to whether they were above or below 50 years of age. A variance analysis was performed to compare the XCI pattern between symptomatic and asymptomatic carriers. The results show that 20% of EDMD1 carriers had cardiac symptoms, and that 50% of these were ≥50 years of age. The XCI pattern was similar in both symptomatic and asymptomatic carriers. Conclusions: Arrhythmias in EDMD1 carriers poorly correlate on lymphocytes to a skewed XCI, probably due to (a) the different embryological origin of cardiac conduction tissue compared to lymphocytes or (b) the preferential loss of atrial cells replaced by fibrous tissue.

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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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