Sex-Ratio Meiotic Drive and Y-Linked Resistance in Drosophila affinis

Genetic elements that cheat Mendelian segregation by biasing transmission in their favor gain a significant fitness benefit. Several examples of sex-ratio meiotic drive, where one sex chromosome biases its own transmission at the cost of the opposite sex chromosome, exist in animals and plants. While the distorting sex chromosome gains a significant advantage by biasing sex ratio, the autosomes, and especially the opposite sex chromosome, experience strong selection to resist this transmission bias. In most well-studied sex-ratio meiotic drive systems, autosomal and/or Y-linked resistance has been identified. We specifically surveyed for Y-linked resistance to sex-ratio meiotic drive in Drosophila affinis by scoring the sex ratio of offspring sired by males with a driving X and one of several Y chromosomes. Two distinct types of resistance were identified: a restoration to 50/50 sex ratios and a complete reversal of sex ratio to all sons. We confirmed that fathers siring all sons lacked a Y chromosome, consistent with previously published work. Considerable variation in Y-chromosome morphology exists in D. affinis, but we showed that morphology does not appear to be associated with resistance to sex-ratio meiotic drive. We then used two X chromosomes (driving and standard) and three Y chromosomes (susceptible, resistant, and lacking) to examine fertility effects of all possible combinations. We find that both the driving X and resistant and lacking Y have significant fertility defects manifested in microscopic examination of testes and a 48-hr sperm depletion assay. Maintenance of variation in this sex-ratio meiotic drive system, including both the X-linked distorter and the Y-resistant effects, appear to be mediated by a complex interaction between fertility fitness and transmission dynamics.     

Experimental Population Genetics of Meiotic Drive Systems. III. Neutralization of Sex-Ratio Distortion in Drosophila through Sex-Chromosome Aneuploidy

Laboratory populations of Drosophila melanogaster were challenged by pseudo-Y drive, which mimics true Y-chromosome meiotic drive through the incorporation of Segregation Distorter (SD) in a T(Y;2) complex. This causes extreme sex-ratio distrotion and can ultimately lead to population extinction. Populations normally respond by the gradual accumulation of drive suppressors, and this reduction in strength of distortion allows the sex ratio to move closer to the optimal value of 1:1. One population monitored, however, was rapidly able to neutralize the effects of sex-ratio distortion by the accumulation of sex-chromosome aneuploids (XXY, XYY). This apparently occurs because XX-bearing eggs, produced in relatively high numbers (~4%) by XXY genotypes, become the main population source of females under strong Y-chromosome drive. Computer simulation for a discrete generation model incorporating random mating with differences in fitness and segregation permits several predictions that can be compared to the data. First, sex-chromosome aneuploids should rapidly attain equilibrium, while stabilizing the population at ~60% males. This sex ratio should be roughly independent of the strength of the meiotic drive. Moreover, conditions favoring the accumulation of drive suppressors (e.g., weak distortion, slow population extinction) are insufficient for maintaining aneuploidy, while conditions favoring aneuploidy (e.g., strong distortion, low production of females) lead to population extinction before drive suppressors can accumulate. Thus, the different mechanisms for neutralizing sex-ratio distortion are complementary. In addition, Y drive and sex-chromosome aneuploidy are potentially co-adaptive, since under some conditions neither will survive alone. Finally, these results suggest the possibility that genetic variants promoting sex-chromosome nondisjunction may have a selective advantage in natural populations faced with sex-ratio distortion.     

SUPPRESSION OF SEX-RATIO MEIOTIC DRIVE AND THE MAINTENANCE OF Y-CHROMOSOME POLYMORPHISM IN DROSOPHILA

Like several other species of Drosophila, D. quinaria is polymorphic for X-chromosome meiotic drive; matings involving males that carry a “sex-ratio” X chromosome (X^SR) result in the production of strongly female-biased offspring sex ratios (Jaenike 1996). A survey of isofemale lines of D. quinaria from several populations reveals that there is genetic variation for partial suppression of this meiotic drive. Crossing experiments show that there is Y-linked, and probably autosomal, variation for suppression of drive. Y-linked suppressors of X-chromosome drive have now been described in several species of Diptera. I develop a simple model for the maintenance of Y-chromosome polymorphism in species polymorphic for X-linked meiotic drive. One interesting feature of this model is that, if there is a stable Y-chromosome polymorphism, then the equilibrium frequency of the standard and sex-ratio X chromosomes is determined solely by Y-chromosome parameters, not by the fitness effects of the different X chromosomes on their carriers. This model suggests that Y-chromosome polymorphism may be easier to maintain than previously thought, and I hypothesize that karyotypic variation in Y chromosomes will be found to be associated with suppression of sex-ratio meiotic drive in other species of Drosophila.     

Meiotic drive alters sperm competitive ability in stalk-eyed flies.

Meiotic drive results when sperm carrying a driving chromosome preferentially survive development. Meiotic drive should therefore influence sperm competition because drive males produce fewer sperm than non-drive males. Whether meiotic drive also influences the competitive ability of sperm after ejaculation is unknown. Here we report the results from reciprocal crosses that are designed for estimating the sperm precedence of male stalk-eyed flies (Cyrtodiopsis whitei) with or without X-linked meiotic drive. We find that nearly half of all sex-ratio males, as compared with 14% of non-sex-ratio males, fail to produce young in a reciprocal cross. Furthermore, the proportion of progeny sired by a sex-ratio male in a female jointly inseminated by a non-sex-ratio male was less than expected from the number of sperm transferred. These effects are not due to differential sperm storage by females because, after a single mating with a sex-ratio male, all females stored sperm and because two sex-ratio males share paternity after jointly mating with a female. In addition to demonstrating a new mechanism of sperm competition, these results provide insight into the maintenance of sex-ratio polymorphisms. Sex-ratio males have less than one-half the fertility of non-sex-ratio males, as is required in order for frequency-dependent selection on males to produce a stable sex-ratio polymorphism.     

Evidence for Extensive Genetic Differentiation between the Sex-Ratio and the Standard Arrangement of DROSOPHILA PSEUDOOBSCURA and D. PERSIMILIS and Identification of Hybrid Sterility Factors

This study deals with sex-ratio genes tightly linked within the Sex-Ratio inversion. By taking advantage of the fact that the Sex-Ratio chromosome of Drosophila persimilis [SR(B)] is homosequential to the Standard chromosome of D. pseudoobscura [ST(A)], we carried out two reciprocal introgression experiments. Individual segments of SR(B) or ST(A) were introgressed into the genome of D. pseudoobscura or D. persimilis, respectively. Males possessing a hybrid SR(B)-ST(A) X chromosome and a genetic background derived from either of the two species were tested for fertility and sex-ratio expression.—It was found that, in terms of the meiotic drive genes, the Sex-Ratio chromosome differs extensively from the Standard chromosome. Because recombinations of these genes result in a complete loss of sex-ratio expression, this finding lends strong support to the hypothesis of gene coadaptation. Coadaptation, in this context, is the advantage of being transmitted preferentially. In light of this finding, the evolution of the sex-ratio system in these two sibling species is discussed.—Introgression experiments also yielded information about hybrid sterility. With reciprocal introgression, sterility interactions were found to be "asymmetric." The asymmetry is fully expected from the viewpoint of evolution of postmating reproductive isolation.     

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

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.     

Experimental and Theoretical Analysis of the "Sex-Ratio" Polymorphism in DROSOPHILA PSEUDOOBSCURA

The Sex-ratio chromosome (SR) is a widespread, multiply inverted rearrangement of the X chromosome present in several species of Drosophila. Male carriers transmit mostly X-bearing sperm. In the absence of strong counteracting selection, SR is expected to increase rapidly to fixation, causing extinction. The present study incorporates a selection-components analysis of SR in laboratory populations, using the closely linked Esterase-5 locus as a marker. Estimated fitnesses show directional viability selection against SR in both males and females, heterosis for fertility and no significant effects on virility, the male adult component of fitness. Estimated fitnesses satisfy conditions for protected polymorphism and accurately predict gene-frequency trajectories in experimental populations. A model of SR gene-frequency evolution is developed, which incorporates sex-linkage, meiotic drive, viability, fertility and virility selecton. We show that conditions for protected polymorphisms are not unduly restrictive and that differential fitness among males is not sufficient for protected polymorphism, irrespective of the degree of meiotic drive.     

Sex Chromosome Meiotic Drive in Stalk-Eyed Flies

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 (X(d)). Relatively high frequencies of X(d) 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 X(d). 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 X(d), modifying Y chromosomes (Y(m)) 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 X(d) on the operational sex ratio and the intensity of sexual selection in these extremely sexually dimorphic flies.     

Sex-ratio meiotic drive in Drosophila simulans is related to equational nondisjunction of the Y chromosome

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 approximately 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.     

Factors of maintaining chromosome polymorphism in common vole Microtus arvalis pallas, 1779: Reduced fertility and meiotic drive

The common vole Microtus arvalis (the form obscurus) exhibits polymorphism of a pericentric inversion in chromosome pair 5 throughout the species range. In the Urals populations, the frequency of an acrocentric variant of the heteromorphic chromosome is very low (on average 3.2%) and virtually does not change annually. The factors of maintaining stable chromosomal polymorphism in the common vole were studied under conditions of a laboratory colony. Heterozygous and homozygous for the acrocentric chromosome females showed a significant reduction of the reproductive output irrespective of the male karyotype. This effect was manifested mostly in litter size at birth. A number of cytogenetic and exophenotypic characteristics, as well as parent-offspring transmission of this chromosome in crosses of various types, were examined. We have found meiotic drive in favor of the acrocentric, as a result of which the frequency of the acrocentric (without taking into account the postnatal mortality) totaled over all cross variants (0.48) was significantly higher than that expected with random segregation (0.42). It is likely that meiotic drive of the acrocentric largely compensates for the reduced fertility of its carriers, being among the factors of maintaining it in natural populations.     

The Y chromosomes of Drosophila simulans are highly polymorphic for their ability to suppress sex-ratio drive

The sex-ratio trait, known in several species of Drosophila including D. simulans, results from meiotic drive of the X chromosome against the Y. Males that carry a sex-ratio X chromosome produce strongly female-biased progeny. In D. simulans, drive suppressors have evolved on the Y chromosome and on the autosomes. Both the frequency of sex-ratio X and the strength of the total drive suppression (Y-linked and autosomal) vary widely among geographic populations of this worldwide species. We have investigated the pattern of Y-linked drive suppression in six natural populations representative of this variability. Y-linked suppressors were found to be a regular component of the suppression, with large differences between populations in the mean level of suppression. These variations did not correspond to differences in frequency of discrete types of Y chromosomes, but to a more or less wide continuum of phenotypes, from nonsuppressor to partial or total suppressor. We concluded that a large diversity of Y-linked suppressor alleles exists in D. simulans and that some populations are highly polymorphic. Our results support the hypothesis that a Y-chromosome polymorphism can be easily maintained by a balance between meiotic drive and the cost of drive suppression.     

Phylogeography of sex ratio and multiple mating in stalk-eyed flies from southeast Asia

The factors maintaining sex chromosome meiotic drive, or sex ratio (SR), in natural populations remain uncertain. Coevolution between segregation distortion and modifiers should produce transient SR distortion while selection can result in a stable polymorphism. We hypothesize that if SR is maintained by selection, then phylogenetically related populations should exhibit similar SR frequency and intensity. Furthermore, when drive is present, females should mate with multiple males more often both to insure fertility and to increase the probability of producing male progeny. In this paper we report on variation in SR frequency and multiple mating among seven populations and three species of stalk-eyed flies, genus Cyrtodiopsis, from southeast Asia. Using a phylogenetic hypothesis based on 1100 bp of mtDNA sequence we find that while sex chromosome meiotic drive is present in all populations of C. whitei and C. dalmanni, the frequency and intensity of drive only differs between populations or species with greater than 4.8% sequence divergence. The frequency of females mating with multiple males is higher in populations with SR. In addition, SR males mate less often, possibly to compensate for sperm depletion. Our results suggest that sex chromosome drive is maintained by balancing selection in populations of C. whitei and C. dalmanni. Nevertheless, coevolution between drive and suppressors deserves further study.     

Sex-ratio distortion in Drosophila simulans: co-occurence of a meiotic drive and a suppressor of drive

A sex-ratio distortion factor was found at high frequency in D. simulans strains from Seychelles and New Caledonia. This factor is poorly or not expressed within those strains which are resistant to it. Its presence was detected by crossing females from New Caledonia or the Seychelles with males from a different geographic origin. Most of the F1 males obtained produced an excess of females (up to 99%) in their progeny. The two strains are infected with Wolbachia, but these micro-organisms are not involved in the sex-ratio distortion. The sex-ratio factor is shown to be an X-linked meiotic driver; nuclear resistance factor(s) act by suppressing the drive. It is likely that the same X-located driver invaded the two populations, which subsequently developed resistance factor(s) against it.     

TO WHAT EXTENT DO DIFFERENT TYPES OF SEX RATIO DISTORTERS INTERFERE?

Within the Diptera, two different selfish genetic elements are known to cause the production of female-biased sex ratios: maternally inherited bacteria that kill male zygotes (male-killers), and X chromosomes causing the degeneration of Y-bearing sperm in males (meiotic drive). We here develop a mathematical model for the dynamics of these two sex-ratio distorters where they co-occur. We show that X chromosome meiotic drive elements can be expected to substantially lower the equilibrium frequency of male-killers and can even lead to their extinction. Conversely, male-killers can also decrease the equilibrium frequency of X drivers and cause their extinction. Thus, we predict that there will be some complementarity in the incidence of X chromosome meiotic drive and male-killing in natural populations, with a lower than expected number of species bearing both elements.     

Male sterility and meiotic drive associated with sex chromosome rearrangements in Drosophila. Role of X-Y pairing.

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.     

The role of recombination and selection in the modifier theory of sex-ratio distortion

The equilibrium configurations for a two-locus multialle model of sex-linked meiotic drive are studied with regard to the recombination fraction:limit cycles can occur in the case of small recombination while stable equilibrium points associated with linkage equilibrium can exist for an intermediate range of recombination values depending on the equilibrium sex ratio, linkage disequilibrium at nearby equilibrium points taking turn with loser linkage. The evolutionary dynamics in two-locus sex-ratio distortion systems is enlightened: while equilibria with a sex ratio closer to 1/2 are more likely to be stable with respect to perturbations on the frequencies of sex-ratio distorters that are represented at equilibrium, such equilibria are also more vulnerable to the invasion of mutant distorters when there is some degree of linkage with the sex-determining locus. For X-linked multimodifier systems of sex-ratio distortion, differential fertilities and viabilities are incorporated and a maximum principle is suggested.     

Sex Chromosome Drive

Sex chromosome drivers are selfish elements that subvert Mendel''s first law of segregation and therefore are overrepresented among the products of meiosis. The sex-biased progeny produced then fuels an extended genetic conflict between the driver and the rest of the genome. Many examples of sex chromosome drive are known, but the occurrence of this phenomenon is probably largely underestimated because of the difficulty to detect it. Remarkably, nearly all sex chromosome drivers are found in two clades, Rodentia and Diptera. Although very little is known about the molecular and cellular mechanisms of drive, epigenetic processes such as chromatin regulation could be involved in many instances. Yet, its evolutionary consequences are far-reaching, from the evolution of mating systems and sex determination to the emergence of new species.Meiotic drivers are selfish genetic elements that subvert Mendelian segregation during gametogenesis for their own benefit. They are passed on to most, if not all, of the functional gametes produced by heterozygotes. Therefore, drivers can increase in frequency and invade populations even if they reduce individual fitness, which is usually the case. The drivers are typically expressed in one sex, of which fertility is impaired. This also has deleterious consequences for the opposite sex and is expected to promote adaptations to counteract drive through sexual selection and sexual conflict. Furthermore, sex-linked meiotic drivers expressed in the heterogametic sex typically lead to biased offspring sex ratios, which represents an additional cost and can exacerbate the sexual conflict.Morgan et al. (1925) were the first to observe sex-biased offspring, which turned out to be caused by a sex-linked meiotic driver. Unfortunately, the Drosophila affinis strain was lost before any conclusive study could be performed. Later, Gershenson (1928) found that the offspring of some Drosophila obscura males were female biased. He showed that these males carried an X-linked genetic element (hereafter “sex ratio” or SR) responsible for the sex-ratio distortion, and showed that the SR did not affect the viability of the male offspring but acted as a gametic killer of Y-bearing sperm. Gamete killing or disabling is observed in males; in females, meiotic drive is usually a result of centromere competition for access to the egg.In its original definition (from Gershenson''s work and others), the term meiotic drive applies to the consequences of the mechanics of the meiotic divisions (Sandler and Novitski 1957). Here, under the term “sex chromosome drive,” we will include more broadly any case of preferential transmission that results directly or indirectly from an event that took place before, during, or after meiosis. Sex chromosome drive is different from sex-ratio adjustment, in which the favored chromosome is not the actor of its drive (West and Sheldon 2002). As emphasized by Sandler and Novitski (1957), it is also different from selection in the haploid phase as a consequence of the gamete''s intrinsic fitness.Only a few dozen cases of sex chromosome drive have been described, mainly in Drosophila and other Diptera (reviewed in Jaenike 2001; Burt and Trivers 2006). One possible explanation for the rarity of reported cases is that a biased sex ratio is not evolutionarily stable. Fisher (1930) predicted that natural selection will favor a 1:1 sex ratio, and that any deviation will be counterselected. This means that variants with counteracting effects can be selected at unlinked loci. Consistent with this prediction, autosomal drive suppressors and resistant Y chromosomes have been found in several Drosophila species (De Carvalho and Klaczko, 1994; Carvalho et al. 1997; Cazemajor et al. 1997). Three different cryptic X-linked SR systems have been described in the same species (Drosophila simulans: Paris, Winters, and Durham systems), showing that they can evolve repeatedly and be completely neutralized in the wild, remaining undetectable unless appropriate genetic crosses are performed (Merçot et al. 1995; Tao et al. 2001, 2007a). D. simulans also teaches us that the time window leading up to neutralization can be very narrow (Bastide et al. 2013). However, variants that enhance distortion can be selected if they are linked to the distorter. Inversions should prevent recombination with nondriving X chromosomes and keep together the loci that interact to induce drive, as found in D. pseudoobscura (Wu and Beckenbach 1983). These examples illustrate the extended genetic conflict that can result from the evolution of sex chromosome drive.Among the known cases of sex chromosome drive, X chromosome drive is much more common than Y chromosome drive. This may be because Y-linked drivers are always expressed, at each generation, unlike X-linked drivers. All else being equal, Y chromosome drive spreads faster and leads to a higher risk of extinction owing to the lack of females (Hamilton 1967). Furthermore, when the sex chromosomes are well differentiated, the Y chromosome usually has many fewer genes, which may provide fewer opportunities for a driver to evolve. On the other hand, heteromorphic sex chromosomes are expected to facilitate the evolution of meiotic drive. Indeed, the more divergent the sex chromosomes are, the less they recombine, reducing the risk of producing a suicide chromosome that carries both the driver and a sensitive allele at the target locus (Charlesworth and Hartl 1978; Frank 1991; Hurst and Pomiankowski 1991).     

Positive Selection of Deleterious Alleles through Interaction with a Sex-Ratio Suppressor Gene in African Buffalo: A Plausible New Mechanism for a High Frequency Anomaly

Although generally rare, deleterious alleles can become common through genetic drift, hitchhiking or reductions in selective constraints. Here we present a possible new mechanism that explains the attainment of high frequencies of deleterious alleles in the African buffalo (Syncerus caffer) population of Kruger National Park, through positive selection of these alleles that is ultimately driven by a sex-ratio suppressor. We have previously shown that one in four Kruger buffalo has a Y-chromosome profile that, despite being associated with low body condition, appears to impart a relative reproductive advantage, and which is stably maintained through a sex-ratio suppressor. Apparently, this sex-ratio suppressor prevents fertility reduction that generally accompanies sex-ratio distortion. We hypothesize that this body-condition-associated reproductive advantage increases the fitness of alleles that negatively affect male body condition, causing genome-wide positive selection of these alleles. To investigate this we genotyped 459 buffalo using 17 autosomal microsatellites. By correlating heterozygosity with body condition (heterozygosity-fitness correlations), we found that most microsatellites were associated with one of two gene types: one with elevated frequencies of deleterious alleles that have a negative effect on body condition, irrespective of sex; the other with elevated frequencies of sexually antagonistic alleles that are negative for male body condition but positive for female body condition. Positive selection and a direct association with a Y-chromosomal sex-ratio suppressor are indicated, respectively, by allele clines and by relatively high numbers of homozygous deleterious alleles among sex-ratio suppressor carriers. This study, which employs novel statistical techniques to analyse heterozygosity-fitness correlations, is the first to demonstrate the abundance of sexually-antagonistic genes in a natural mammal population. It also has important implications for our understanding not only of the evolutionary and ecological dynamics of sex-ratio distorters and suppressors, but also of the functioning of deleterious and sexually-antagonistic alleles, and their impact on population viability.     

Organization of the sex-ratio meiotic drive region in Drosophila simulans

Sex-ratio meiotic drive is the preferential transmission of the X chromosome by XY males, which occurs in several Drosophila species and results in female-biased progeny. Although the trait has long been known to exist, its molecular basis remains completely unknown. Here we report a fine-mapping experiment designed to characterize the major drive locus on a sex-ratio X chromosome of Drosophila simulans originating from the Seychelles (XSR6). This primary locus was found to contain two interacting elements at least, both of which are required for drive expression. One of them was genetically tracked to a tandem duplication containing six annotated genes (Trf2, CG32712, CG12125, CG1440, CG12123, org-1), and the other to a candidate region located approximately 110 kb away and spanning seven annotated genes. RT-PCR showed that all but two of these genes were expressed in the testis of both sex-ratio and standard males. In situ hybridization to polytene chromosomes revealed a complete association of the duplication with the sex-ratio trait in random samples of X chromosomes from Madagascar and Reunion.     

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 1.3cM 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.