Red queen's race: rapid evolutionary dynamics of an expanding family of meiotic drive factors and their hpRNA suppressors

Meiotic drivers are a class of selfish genetic elements that are widespread across eukaryotes. Their activities are often detrimental to organismal fitness and thus trigger drive suppression to ensure fair segregation during meiosis. Accordingly, their existence is frequently hidden in genomes, and their molecular functions are little known. Here, we trace evolutionary steps that generated the Dox meiotic drive system in Drosophila simulans (Dsim), which distorts male:female balance (sex-ratio) by depleting male progeny. We show that Dox emerged via stepwise mobilization and acquisition of portions of multiple D. melanogaster genes, including the sperm chromatin packaging gene protamine. Moreover, we reveal novel Dox homologs in Dsim and massive, recent, amplification of Dox superfamily genes specifically on X chromosomes of its closest sister species D. mauritiana (Dmau) and D. sechellia (Dsech). The emergence of Dox superfamily genes is tightly associated with 1.688 family satellite repeats that flank de novo genomic copies. In concert, we find coordinated emergence and diversification of autosomal hairpin RNA/siRNAs loci that target subsets of Dox superfamily genes across simulans clade species. Finally, an independent set of protamine amplifications the Y chromosome of D. melanogaster indicates that protamine genes are frequent and recurrent players in sex chromosome dynamics. Overall, we reveal fierce genetic arms races between meiotic drive factors and siRNA suppressors associated with recent speciation.

Download Full-text

Meiotic drive mechanisms: lessons from Drosophila

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.1430 ◽

2019 ◽

Vol 286 (1913) ◽

pp. 20191430 ◽

Cited By ~ 8

Author(s):

Cécile Courret ◽

Ching-Ho Chang ◽

Kevin H.-C. Wei ◽

Catherine Montchamp-Moreau ◽

Amanda M. Larracuente

Keyword(s):

Small Rna ◽

Molecular Mechanisms ◽

Meiotic Drive ◽

Gene Duplications ◽

Arms Races ◽

Transport Pathways ◽

Selfish Genetic Elements ◽

Genetic Origins ◽

Drive Systems ◽

Rna Pathways

Meiotic drivers are selfish genetic elements that bias their transmission into gametes, often to the detriment of the rest of the genome. The resulting intragenomic conflicts triggered by meiotic drive create evolutionary arms races and shape genome evolution. The phenomenon of meiotic drive is widespread across taxa but is particularly prominent in the Drosophila genus. Recent studies in Drosophila have provided insights into the genetic origins of drivers and their molecular mechanisms. Here, we review the current literature on mechanisms of drive with an emphasis on sperm killers in Drosophila species. In these systems, meiotic drivers often evolve from gene duplications and targets are generally linked to heterochromatin. While dense in repetitive elements and difficult to study using traditional genetic and genomic approaches, recent work in Drosophila has made progress on the heterochromatic compartment of the genome. Although we still understand little about precise drive mechanisms, studies of male drive systems are converging on common themes such as heterochromatin regulation, small RNA pathways, and nuclear transport pathways. Meiotic drive systems are therefore promising models for discovering fundamental features of gametogenesis.

Download Full-text

Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism

Genes ◽

10.3390/genes11040374 ◽

2020 ◽

Vol 11 (4) ◽

pp. 374 ◽

Cited By ~ 1

Author(s):

Svetlana A. Romanenko ◽

Antonina V. Smorkatcheva ◽

Yulia M. Kovalskaya ◽

Dmitry Yu. Prokopov ◽

Natalya A. Lemskaya ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

De Novo ◽

Complex Structure ◽

X Chromosomes ◽

Single Chromosome ◽

Determination System ◽

Sex Determination System ◽

Mandarin Vole

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.

Download Full-text

Amplified Fragments of an Autosome-Borne Gene Constitute a Significant Component of the W Sex Chromosome of Eremias velox (Reptilia, Lacertidae)

Genes ◽

10.3390/genes12050779 ◽

2021 ◽

Vol 12 (5) ◽

pp. 779

Author(s):

Artem Lisachov ◽

Daria Andreyushkova ◽

Guzel Davletshina ◽

Dmitry Prokopov ◽

Svetlana Romanenko ◽

...

Keyword(s):

Sex Chromosome ◽

De Novo ◽

Unknown Origin ◽

Protein Product ◽

W Chromosome ◽

Protein Coding ◽

X Chromosomes ◽

Y Chromosomes ◽

Total Female ◽

Evolutionary Trajectories

Heteromorphic W and Y sex chromosomes often experience gene loss and heterochromatinization, which is frequently viewed as their “degeneration”. However, the evolutionary trajectories of the heterochromosomes are in fact more complex since they may not only lose but also acquire new sequences. Previously, we found that the heterochromatic W chromosome of a lizard Eremias velox (Lacertidae) is decondensed and thus transcriptionally active during the lampbrush stage. To determine possible sources of this transcription, we sequenced DNA from a microdissected W chromosome sample and a total female DNA sample and analyzed the results of reference-based and de novo assembly. We found a new repetitive sequence, consisting of fragments of an autosomal protein-coding gene ATF7IP2, several SINE elements, and sequences of unknown origin. This repetitive element is distributed across the whole length of the W chromosome, except the centromeric region. Since it retained only 3 out of 10 original ATF7IP2 exons, it remains unclear whether it is able to produce a protein product. Subsequent studies are required to test the presence of this element in other species of Lacertidae and possible functionality. Our results provide further evidence for the view of W and Y chromosomes as not just “degraded” copies of Z and X chromosomes but independent genomic segments in which novel genetic elements may arise.

Download Full-text

The chromosomal distribution of sex-biased microRNAs in Drosophila is non-adaptive

10.1101/2021.09.25.461796 ◽

2021 ◽

Author(s):

Antonio Marco

Keyword(s):

X Chromosome ◽

Evolutionary Dynamics ◽

Sex Chromosome ◽

De Novo ◽

Evolutionary Process ◽

Chromosomal Distribution ◽

Apparent Paradox ◽

Protein Coding ◽

Protein Coding Genes ◽

Short Rnas

Genes are often differentially expressed between males and females. In Drosophila melanogaster, the analysis of sex-biased microRNAs (short non-coding regulatory molecules) has revealed striking differences with protein-coding genes. Mainly, the X chromosome is enriched in male-biased microRNA genes, although it is depleted of male-biased protein-coding genes. The paucity of male-biased genes in the X chromosome is generally explained by an evolutionary process called demasculinization. I suggest that the excess of male-biased microRNAs in the X chromosome is due to high-rates of de novo emergence of microRNAs, a tendency of novel microRNAs in the X chromosome to be expressed in testis, and to a lack of a demasculinization process. To test this hypothesis I analysed the expression profile of microRNAs in males, females and gonads in D. pseudoobscura, in which an autosome translocated into the X chromosome effectively becoming part of a sex chromosome (neo-X). I found that the pattern of sex- biased expression is generally conserved between D. melanogaster and D. pseudoobscura. Also, orthologous microRNAs in both species conserve their chromosomal location, indicating that there is no evidence of demasculinization or other inter-chromosomal movement of microRNAs. D. pseudoobscura-specific microRNAs in the neo-X chromosome tend to be male-biased and particularly expressed in testis. In summary, the apparent paradox resulting from male-biased protein-coding genes depleted in the X chromosome and an enrichment in male-biased microRNAs is a consequence of different evolutionary dynamics between coding genes and short RNAs.

Download Full-text

Gene flow mediates the role of sex chromosome meiotic drive during complex speciation

10.1101/024711 ◽

2015 ◽

Cited By ~ 1

Author(s):

Colin D. Meiklejohn ◽

Emily L. Landeen ◽

Kathleen E. Gordon ◽

Thomas Rzatkiewicz ◽

Sarah B. Kingan ◽

...

Keyword(s):

Gene Flow ◽

Sex Chromosomes ◽

Population Genomics ◽

Sex Chromosome ◽

Hybrid Sterility ◽

Meiotic Drive ◽

Hybrid Male ◽

Selfish Genetic Elements ◽

Cryptic Sex

ABSTRACTDuring speciation, sex chromosomes often accumulate interspecific genetic incompatibilities faster than the rest of the genome. The drive theory posits that sex chromosomes are susceptible to recurrent bouts of meiotic drive and suppression, causing the evolutionary build-up of divergent cryptic sex-linked drive systems and, incidentally, genetic incompatibilities. To assess the role of drive during speciation, we combine high-resolution genetic mapping of X-linked hybrid male sterility with population genomics analyses of divergence and recent gene flow between the fruitfly species, Drosophila mauritiana and D. simulans. Our findings reveal a high density of genetic incompatibilities and a corresponding dearth of gene flow on the X chromosome. Surprisingly, we find that, rather than contributing to interspecific divergence, a known drive element has recently migrated between species, caused a strong reduction in local divergence, and undermined the evolution of hybrid sterility. Gene flow can therefore mediate the effects of selfish genetic elements during speciation.

Download Full-text

GENETIC ANALYSIS OF SEX CHROMOSOMAL MEIOTIC MUTANTS IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/71.2.255 ◽

1972 ◽

Vol 71 (2) ◽

pp. 255-286

Author(s):

Bruce S Baker ◽

Adelaide T C Carpenter

Keyword(s):

X Chromosome ◽

Meiotic Division ◽

Sex Chromosome ◽

Meiotic Drive ◽

Chromosome 2 ◽

Fourth Chromosome ◽

X Chromosomes ◽

Meiotic Mutants ◽

Male Specific ◽

Chromosome Nondisjunction

ABSTRACT A total of 209 ethyl methanesulfonate-treated X chromosomes were screened for meiotic mutants that either (1) increased sex or fourth chromosome nondisjunction at either meiotic division in males; (2) allowed recombination in such males; (3) increased nondisjunction of the X chromosome at either meiotic division in females; or (4) caused such females, when mated to males heterozygous for Segregation-Distorter (SD) and a sensitive homolog to alter the strength of meiotic drive in males.—Twenty male-specific meiotic mutants were found. Though the rates of nondisjunction differed, all twenty mutants were qualitatively similar in that (1) they alter the disjunction of the X chromosome from the Y chromosome; (2) among the recovered sex-chromosome exceptional progeny, there is a large excess of those derived from nullo-XY as compared to XY gametes; (3) there is a negative correlation between the frequency of sex-chromosome exceptional progeny and the frequency of males among the regular progeny. In their effects on meiosis these mutants are similar to In(1)sc4Lsc8R, which is deleted for the basal heterochromatin. These mutants, however, have normal phenotypes and viabilities when examined as X/0 males, and furthermore, a mapping of two of the mutants places them in the euchromatin of the X chromosome. It is suggested that these mutants are in genes whose products are involved in insuring the proper functioning of the basal pairing sites which are deleted in In(1)sc4Lsc8R, and in addition that there is a close connection, perhaps causal, between the disruption of normal X-Y pairing (and, therefore, disjunction) and the occurrence of meiotic drive in the male.—Eleven mutants were found which increased nondisjunction in females. These mutants were characterized as to (1) the division at which they acted; (2) their effect on recombination; (3) their dominance; (4) their effects on disjunction of all four chromosome pairs. Five female mutants caused a nonuniform decrease in recombination, being most pronounced in distal regions, and an increase in first division nondisjunction of all chromosome pairs. Their behavior is consistent with the hypothesis that these mutants are defective in a process which is a precondition for exchange. Two female mutants were allelic and caused a uniform reduction in recombination for all intervals (though to different extents for the two alleles) and an increase in first-division nondisjunction of all chromosomes. Limited recombination data suggest that these mutants do not alter coincidence, and thus, following the arguments of Sandler et al. (1968), are defective in exchange rather than a precondiiton for exchange. A single female mutant behaves in a manner that is consistent with it being a defect in a gene whose functioning is essential for distributive pairing. Three of the female meiotic mutants cause abnormal chromosome behavior at a number of times in meiosis. Thus, nondisjunction at both meiotic divisions is increased, recombinant chromosomes nondisjoin, and there is a polarized alteration in recombination.—The striking differences between the types of control of meiosis in the two sexes is discussed and attention is drawn to the possible similarities between (1) the disjunction functions of exchange and the process specified by the chromosome-specific male mutants; and (2) the prevention of functional aneuploid gamete formation by distributive disjunction and meiotic drive.

Download Full-text

Bisection of the X chromosome disrupts the initiation of chromosome silencing during meiosis in Caenorhabditis elegans

Nature Communications ◽

10.1038/s41467-021-24815-0 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Yisrael Rappaport ◽

Hanna Achache ◽

Roni Falk ◽

Omer Murik ◽

Oren Ram ◽

...

Keyword(s):

Caenorhabditis Elegans ◽

Rna Polymerase Ii ◽

X Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Transcription Analysis ◽

X Chromosomes ◽

Unique Character ◽

Active Transcription ◽

Heterogametic Sex

AbstractDuring meiosis, gene expression is silenced in aberrantly unsynapsed chromatin and in heterogametic sex chromosomes. Initiation of sex chromosome silencing is disrupted in meiocytes with sex chromosome-autosome translocations. To determine whether this is due to aberrant synapsis or loss of continuity of sex chromosomes, we engineered Caenorhabditis elegans nematodes with non-translocated, bisected X chromosomes. In early meiocytes of mutant males and hermaphrodites, X segments are enriched with euchromatin assembly markers and active RNA polymerase II staining, indicating active transcription. Analysis of RNA-seq data showed that genes from the X chromosome are upregulated in gonads of mutant worms. Contrary to previous models, which predicted that any unsynapsed chromatin is silenced during meiosis, our data indicate that unsynapsed X segments are transcribed. Therefore, our results suggest that sex chromosome chromatin has a unique character that facilitates its meiotic expression when its continuity is lost, regardless of whether or not it is synapsed.

Download Full-text

Male Sterility and Meiotic Drive Associated With Sex Chromosome Rearrangements in Drosophila: Role of X-Y Pairing

Genetics ◽

10.1093/genetics/149.1.143 ◽

1998 ◽

Vol 149 (1) ◽

pp. 143-155 ◽

Cited By ~ 3

Author(s):

Bruce D McKee ◽

Kathy Wilhelm ◽

Cynthia Merrill ◽

Xiao-jia Ren

Keyword(s):

Male Sterility ◽

Sex Chromosome ◽

Meiotic Drive ◽

Repeated Sequence ◽

Meiotic Pairing ◽

Intergenic Spacers ◽

Male Specific ◽

The Relationship ◽

Novel Model

Abstract In Drosophila melanogaster, deletions of the pericentromeric X heterochromatin cause X-Y nondisjunction, reduced male fertility and distorted sperm recovery ratios (meiotic drive) in combination with a normal Y chromosome and interact with Y-autosome translocations (T(Y;A)) to cause complete male sterility. The pericentromeric heterochromatin has been shown to contain the male-specific X-Y meiotic pairing sites, which consist mostly of a 240-bp repeated sequence in the intergenic spacers (IGS) of the rDNA repeats. The experiments in this paper address the relationship between X-Y pairing failure and the meiotic drive and sterility effects of Xh deletions. X-linked insertions either of complete rDNA repeats or of rDNA fragments that contain the IGS were found to suppress X-Y nondisjunction and meiotic drive in Xh−/Y males, and to restore fertility to Xh−/T(Y;A) males for eight of nine tested Y-autosome translocations. rDNA fragments devoid of IGS repeats proved incapable of suppressing either meiotic drive or chromosomal sterility. These results indicate that the various spermatogenic disruptions associated with X heterochromatic deletions are all consequences of X-Y pairing failure. We interpret these findings in terms of a novel model in which misalignment of chromosomes triggers a checkpoint that acts by disabling the spermatids that derive from affected spermatocytes.

Download Full-text

Absence of X-chromosome dosage compensation in the primordial germ cells of Drosophila embryos

Scientific Reports ◽

10.1038/s41598-021-84402-7 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Ryoma Ota ◽

Makoto Hayashi ◽

Shumpei Morita ◽

Hiroki Miura ◽

Satoru Kobayashi

Keyword(s):

X Chromosome ◽

Germ Cells ◽

Dosage Compensation ◽

Sex Chromosome ◽

Primordial Germ Cells ◽

Histone H4 ◽

X Chromosomes ◽

Essential Components ◽

Msl Complex ◽

Male Specific

AbstractDosage compensation is a mechanism that equalizes sex chromosome gene expression between the sexes. In Drosophila, individuals with two X chromosomes (XX) become female, whereas males have one X chromosome (XY). In males, dosage compensation of the X chromosome in the soma is achieved by five proteins and two non-coding RNAs, which assemble into the male-specific lethal (MSL) complex to upregulate X-linked genes twofold. By contrast, it remains unclear whether dosage compensation occurs in the germline. To address this issue, we performed transcriptome analysis of male and female primordial germ cells (PGCs). We found that the expression levels of X-linked genes were approximately twofold higher in female PGCs than in male PGCs. Acetylation of lysine residue 16 on histone H4 (H4K16ac), which is catalyzed by the MSL complex, was undetectable in these cells. In male PGCs, hyperactivation of X-linked genes and H4K16ac were induced by overexpression of the essential components of the MSL complex, which were expressed at very low levels in PGCs. Together, these findings indicate that failure of MSL complex formation results in the absence of X-chromosome dosage compensation in male PGCs.

Download Full-text

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.

Download Full-text