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

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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The Sex-Ratio Trait in Drosophila simulans: Genetic Analysis of Distortion and Suppression

Genetics ◽

10.1093/genetics/147.2.635 ◽

1997 ◽

Vol 147 (2) ◽

pp. 635-642 ◽

Cited By ~ 1

Author(s):

Michel Cazemajor ◽

Claudie Landré ◽

Catherine Montchamp-Moreau

Keyword(s):

Sex Ratio ◽

Genetic Analysis ◽

High Frequency ◽

Natural Populations ◽

Meiotic Drive ◽

Drosophila Simulans ◽

Standard Strain ◽

Large Excess ◽

X Chromosomes ◽

Naturally Occurring

The sex-ratio trait described in several Drosophila species is a type of naturally occurring X-linked meiotic drive that causes males bearing a sex-ratio X chromosome to produce progenies with a large excess of females. We have previously reported the occurrence of sex-ratio X chromosomes in Drosophila simulans. In this species, because of the co-occurrence of drive suppressors, the natural populations and the derived laboratory strains show an equal sex-ratio even when sex-ratio X chromosomes are present at a high frequency. The presence of sex-ratio X chromosomes is established via crosses with a standard strain that is devoid of drive suppressors. In this article, we show first that the sex-ratio trait in D. simulans results from the action of several X-linked loci. Second we describe drive suppressors on each major autosome as well as on the Y chromosome. The Y-linked factors suppress the drive partially whereas the autosomal suppression can be complete.

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Sex-ratio Meiotic Drive in Drosophila simulans Is Related to Equational Nondisjunction of the Y Chromosome

Genetics ◽

10.1093/genetics/154.1.229 ◽

2000 ◽

Vol 154 (1) ◽

pp. 229-236

Author(s):

Michel Cazemajor ◽

Dominique Joly ◽

Catherine Montchamp-Moreau

Keyword(s):

Sex Ratio ◽

Y Chromosome ◽

Direct Evidence ◽

Sex Chromosome ◽

Meiotic Drive ◽

Female Offspring ◽

Drosophila Simulans ◽

Common Basis ◽

Naturally Occurring

Abstract The sex-ratio trait, an example of naturally occurring X-linked meiotic drive, has been reported in a dozen Drosophila species. Males carrying a sex-ratio X chromosome produce an excess of female offspring caused by a deficiency of Y-bearing sperm. In Drosophila simulans, such males produce ~70–90% female offspring, and 15–30% of the male offspring are sterile. Here, we investigate the cytological basis of the drive in this species. We show that the sex-ratio trait is associated with nondisjunction of Y chromatids in meiosis II. Fluorescence in situ hybridization (FISH) using sex-chromosome-specific probes provides direct evidence that the drive is caused by the failure of the resulting spermatids to develop into functional sperm. XYY progeny were not observed, indicating that few or no YY spermatids escape failure. The recovery of XO males among the progeny of sex-ratio males shows that some nullo-XY spermatids become functional sperm and likely explains the male sterility. A review of the cytological data in other species shows that aberrant behavior of the Y chromosome may be a common basis of sex-ratio meiotic drive in Drosophila and the signal that triggers differential spermiogenesis failure.

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"Sex ratio" meiotic drive in Drosophila testacea.

Genetics ◽

10.1093/genetics/126.3.651 ◽

1990 ◽

Vol 126 (3) ◽

pp. 651-656 ◽

Cited By ~ 9

Author(s):

A C James ◽

J Jaenike

Keyword(s):

Sex Ratio ◽

Genetic Factor ◽

Natural Populations ◽

Meiotic Drive ◽

Female Offspring ◽

Species Group ◽

Gene Arrangement ◽

Ecological Consequence ◽

Ratio Condition ◽

Female Bias

Abstract We document the occurrence of "sex ratio" meiotic drive in natural populations of Drosophila testacea. "Sex ratio" males sire greater than 95% female offspring. Genetic analysis reveals that this effect is due to a meiotically driven X chromosome, as in other species of Drosophila in which "sex ratio" has been found. In contrast to other drosophilids, the "sex ratio" and standard chromosomes of D. testacea do not differ in gene arrangement, implying that the effect may be due to a single genetic factor in this species. In all likelihood, the "sex ratio" condition has evolved independently in D. testacea and in the Drosophila obscura species group, as the loci responsible for the effect occur on different chromosomal elements. An important ecological consequence of "sex ratio" is that natural populations of D. testacea exhibit a strong female bias. Because D. testacea mates, oviposits, and feeds as adults and larvae on mushrooms, this species provides an excellent opportunity to study the selective factors in nature that prevent "sex ratio" chromosomes from increasing to fixation and causing the extinction of the species.

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Sex-Ratio Drive in Drosophila simulans: Variation in Segregation Ratio of X Chromosomes From a Natural Population

Genetics ◽

10.1093/genetics/162.3.1221 ◽

2002 ◽

Vol 162 (3) ◽

pp. 1221-1231 ◽

Cited By ~ 1

Author(s):

Catherine Montchamp-Moreau ◽

Michel Cazemajor

Keyword(s):

Sex Ratio ◽

Natural Population ◽

X Chromosome ◽

Sex Ratios ◽

Segregation Ratio ◽

Drosophila Simulans ◽

Chromosome Polymorphism ◽

X Chromosomes ◽

Clear Cut ◽

Pattern Of Variation

Abstract The sex-ratio trait that exists in a dozen Drosophila species is a case of naturally occurring X chromosome drive that causes males to produce female-biased progeny. Autosomal and Y polymorphism for suppressors are known to cause variation in drive expression, but the X chromosome polymorphism has never been thoroughly investigated. We characterized 41 X chromosomes from a natural population of Drosophila simulans that had been transferred to a suppressor-free genetic background. We found two clear-cut groups of chromosomes, sex-ratio and standard. The sex-ratio X chromosomes differed in their segregation ratio (81-96% females in the progeny), the less powerful drivers being less stable in their expression. A sib analysis, using a moderate driver, indicated that within-X variation in drive expression depended on genetic (autosomal) or epigenetic factors and that the age of the males also affected the trait. The other X chromosomes produced equal or roughly equal sex ratios, but again with significant variation. The continuous pattern of variation observed within both groups suggested that, in addition to a major sex-ratio gene, many X-linked loci of small effect modify the segregation ratio of this chromosome and are maintained in a polymorphic state. This was also supported by the frequency distribution of sex ratios produced by recombinant X chromosomes.

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Polymorphism for Y-Linked Suppressors of sex-ratio in Two Natural Populations of Drosophila mediopunctata

Genetics ◽

10.1093/genetics/146.3.891 ◽

1997 ◽

Vol 146 (3) ◽

pp. 891-902 ◽

Cited By ~ 4

Author(s):

Antonio Bernardo Carvalho ◽

Suzana Casaccia Vaz ◽

Louis Bernard Klaczko

Keyword(s):

Population Genetics ◽

Population Dynamics ◽

Natural Selection ◽

Sex Ratio ◽

Numerical Simulations ◽

Natural Populations ◽

Meiotic Drive ◽

X Chromosomes ◽

Variable Expression ◽

Y Chromosomes

In several Drosophila species there is a trait known as “sex-ratio”: males carrying certain X chromosomes (called “SR”) produce female biased progenies due to X-Y meiotic drive. In Drosophila mediopunctata this trait has a variable expression due to Y-linked suppressors of sex-ratio expression, among other factors. There are two types of Y chromosomes (suppressor and nonsuppressor) and two types of SR chromosomes (suppressible and unsuppressible). Sex-ratio expression is suppressed in males with the SRsuppressible/Ysuppressor genotype, whereas the remaining three genotypes produce female biased progenies. Now we have found that ∼10–20% of the Y chromosomes from two natural populations 1500 km apart are suppressors of sex-ratio expression. Preliminary estimates indicate that Ysuppressor has a meiotic drive advantage of 6% over Ynonsuppressor. This Y polymorphism for a nonneutral trait is unexpected under current population genetics theoly. We propose that this polymorphism is stabilized by an equilibrium between meiotic drive and natural selection, resulting from interactions in the population dynamics of X and Y alleles. Numerical simulations showed that this mechanism may stabilize nonneutral Y polymorphisms such as we have found in D. mediopunctata.

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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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Hybrid dysgenesis-induced quantitative variation on the X chromosome of Drosophila melanogaster.

Genetics ◽

10.1093/genetics/124.3.627 ◽

1990 ◽

Vol 124 (3) ◽

pp. 627-636

Author(s):

C Q Lai ◽

T F Mackay

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Quantitative Traits ◽

Natural Populations ◽

Quantitative Variation ◽

Hybrid Dysgenesis ◽

X Chromosomes ◽

Bristle Number ◽

Seven Generations ◽

Polygenic Variation

Abstract To determine the ability of the P-M hybrid dysgenesis system of Drosophila melanogaster to generate mutations affecting quantitative traits, X chromosome lines were constructed in which replicates of isogenic M and P strain X chromosomes were exposed to a dysgenic cross, a nondysgenic cross, or a control cross, and recovered in common autosomal backgrounds. Mutational heritabilities of abdominal and sternopleural bristle score were in general exceptionally high-of the same magnitude as heritabilities of these traits in natural populations. P strain chromosomes were eight times more mutable than M strain chromosomes, and dysgenic crosses three times more effective than nondysgenic crosses in inducing polygenic variation. However, mutational heritabilities of the bristle traits were appreciable for P strain chromosomes passed through one nondysgenic cross, and for M strain chromosomes backcrossed for seven generations to inbred P strain females, a result consistent with previous observations on mutations affecting quantitative traits arising from nondysgenic crosses. The new variation resulting from one generation of mutagenesis was caused by a few lines with large effects on bristle score, and all mutations reduced bristle number.

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SEX RATIO DISTORTION CAUSED BY MEIOTIC DRIVE IN A MOSQUITO, Culex pipiens L

Genetics ◽

10.1093/genetics/88.3.427 ◽

1978 ◽

Vol 88 (3) ◽

pp. 427-446

Author(s):

Theresa Luine Sweeny ◽

A Ralph Barr

Keyword(s):

Sex Ratio ◽

Chromosome Pair ◽

Culex Pipiens ◽

Recessive Gene ◽

Meiotic Drive ◽

Female Offspring ◽

Large Excess ◽

Daughter Cells ◽

Ratio Distortion ◽

Sex Ratio Distortion

ABSTRACT A genetic factor, distorter (d), has been discovered that upsets the normal sex ratio of 1:1 and results in a large excess of males in Culex pipiens. The effect can be explained by a sex-linked, recessive gene. Males homozygous for the gene (Md/md) produce few female offspring; the effect is not due to postzygotic mortality. During the first meiotic division in spermatogenesis, the shortest chromosome pair, which, according to Jost and Laven (1971), is associated with sex determination, can be seen to be abnormal. In a high proportion of spermatocysts, one of the dyads of the shortest bivalent fragments, and the pieces are distributed irregularly to the daughter cells. It is believed that the female-determining chromosomes fragment. This would give rise to an excess of male-determining sperm. The possible usefulness of this factor for control or for experimental purposes is discussed.

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Sex ratios in natural populations of Drosophila pseudoobscura from Mexico

Genetika ◽

10.2298/gensr1203491s ◽

2012 ◽

Vol 44 (3) ◽

pp. 491-498 ◽

Cited By ~ 1

Author(s):

Victor Salceda ◽

Carolina Arceo-Maldonado

Keyword(s):

Sex Ratio ◽

Sex Chromosome ◽

Natural Populations ◽

Diploid Species ◽

Drosophila Pseudoobscura ◽

Adult Offspring ◽

Equal Proportion ◽

X Chromosomes ◽

The Individual ◽

Number Of Males

Most species show an equal proportion of individuals of both sexes. In diploid species sex ratio is determined by a genic balance between sex chromosomes. In Drosophila sex is determined by the ratio of X- chromosomes versus autosomes and in some species of the genus it is related to the presence of an inversion in the sex chromosome. The present work analyses the sex ratio in 27 natural populations of Drosophila pseudoobscura that inhabit Mexico. Female flies captured in nature were counted and their sex ratio calculated and been called generation P, then cultured individualy, allowed to leave adult offspring which was quantified in order to get its sex ratio and designated generation F1. sex ratio was calculated using the expression: number of males times 100 divided by the number of females proposed by Darwin (1871). The sex ratio of each population was taken using the average of all the individual counts from each sample. The values found varied among different generations and populations, so for generation P their values varieded 37.4 to 190.4 and in generation F1 from 31.3 up to 96.4 males for each 100 females. According to their geographical distribution four North to South transects were arranged and in them means varied from 60.8 to 81.7 males for each 100 females. All this means that in Mexican population are more females than males, exceptionally more males than females.

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