Catherine Montchamp-Moreau

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.

THE SEX-RATIO TRAIT IN DROSOPHILA SIMULANS : GEOGRAPHICAL DISTRIBUTION OF DISTORTION AND RESISTANCE

The sex‐ratio trait we describe here in Drosophila simulans results from X‐linked meiotic drive. Males bearing a driving X chromosome can produce a large excess of females (about 90%) in their progeny. This is, however, rarely the case in the wild, where resistance factors, including autosomal suppressors and insensitive Y chromosomes, prevent the expression of the driver. In this study, we searched for drive and resistance factors in strains of Drosophila simulans collected all over the world. Driving X chromosomes were found in all populations whenever a good sample size was available. Their frequency may reach up to 60%. However, the presence of driving X chromosomes never results in an excess of females, due to the systematic co‐occurrence of resistance factors. The highest frequencies of driving X chromosomes were observed in islands, while populations from East and Central Africa (the supposed center of origin of the species) showed the highest level of resistance. The geographical pattern of drive and resistance factors, as well as the results of crosses between strains from different geographical areas, suggest that the sex‐ratio system described here has a unique and ancient origin in the species.

The Ecology and Evolutionary Dynamics of Meiotic Drive

Meiotic drivers are genetic variants that selfishly manipulate the production of gametes to increase their own rate of transmission, often to the detriment of the rest of the genome and the individual that carries them. This genomic conflict potentially occurs whenever a diploid organism produces a haploid stage, and can have profound evolutionary impacts on gametogenesis, fertility, individual behaviour, mating system, population survival, and reproductive isolation. Multiple research teams are developing artificial drive systems for pest control, utilising the transmission advantage of drive to alter or exterminate target species. Here, we review current knowledge of how natural drive systems function, how drivers spread through natural populations, and the factors that limit their invasion.

Evolution of the chromosomal location of rDNA genes in two Drosophila species subgroups: ananassae and melanogaster.

The evolution of the chromosomal location of ribosomal RNA gene clusters and the organization of heterochromatin in the Drosophila melanogaster group were investigated using fluorescence in situ hybridization and DAPI staining to mitotic chromosomes. The investigation of 18 species (11 of which were being examined for the first time) belonging to the melanogaster and ananassae subgroups suggests that the ancestral configuration consists of one nucleolus organizer (NOR) on each sex chromosome. This pattern, which is conserved throughout the melanogaster subgroup, except in D. simulans and D. sechellia, was observed only in the ercepeae complex within the ananassae subgroup. Both sex-linked NORs must have been lost in the lineage leading to D. varians and in the ananassae and bipectinata complexes, whereas new sites, characterized by intra-species variation in hybridization signal size, appeared on the fourth chromosome related to heterochromatic rearrangements. Nucleolar material is thought to be required for sex chromosome pairing and disjunction in a variety of organisms including Drosophila. Thus, either remnant sequences, possibly intergenic spacer repeats, are still present in the sex chromosomes which have lost their NORs (as observed in D. simulans and D. sechellia), or an alternative mechanism has evolved.Heredity advance online publication, 23 February 2005; doi:10.1038/sj.hdy.6800612

Sex-ratio distorter of Drosophila simulans reduces male productivity and sperm competition ability

The aim of the present study was to determine whether the effects of sex‐ratio segregation distorters on the fertility of male Drosophila simulans can explain the contrasting success of these X‐linked meiotic drivers in different populations of the species. We compared the fertility of sex‐ratio and wild‐type males under different mating conditions. Both types were found to be equally fertile when mating was allowed, with two females per male, during the whole period of egg laying. By contrast sex‐ratio males suffered a strong fertility disadvantage when they were offered multiple mates for a limited time, or in sperm competition conditions. In the latter case only, the toll on male fertility exceeded the segregation advantage of the distorters. These results indicate that sex‐ratio distorters can either spread or disappear from populations, depending on the mating rate. Population density is therefore expected to play a major role in the evolution of sex‐ratio distorters in this Drosophila species.

Signature of Selective Sweep Associated With the Evolution of sex-ratio Drive in Drosophila simulans

In several Drosophila species, the XY Mendelian ratio is disturbed by X-linked segregation distorters (sexratio drive). We used a collection of recombinants between a nondistorting chromosome and a distorting X chromosome originating from the Seychelles to map a candidate sex-ratio region in Drosophila simulans using molecular biallelic markers. Our data were compatible with the presence of a sex-ratio locus in the 7F cytological region. Using sequence polymorphism at the Nrg locus, we showed that sex-ratio has induced a strong selective sweep in populations from Madagascar and Réunion, where distorting chromosomes are close to a 50% frequency. The complete association between the marker and the sex-ratio phenotype and the near absence of mutations and recombination in the studied fragment after the sweep event indicate that this event is recent. Examples of selective sweeps are increasingly reported in a number of genomes. This case identifies the causal selective force. It illustrates that all selective sweeps are not necessarily indicative of an increase in the average fitness of populations.

THE Y CHROMOSOMES OF DROSOPHILA SIMULANS ARE HIGHLY POLYMORPHIC FOR THEIR ABILITY TO SUPPRESS SEX-RATIO DRIVE

Abstract 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.

Wolbachia segregation rate in Drosophila simulans naturally bi-infected cytoplasmic lineages

Wolbachia are maternally transmitted endocellular bacteria infecting several arthropod species. In order to study Wolbachia segregation rate, Drosophila simulans females from an Indo-Pacific population (Seychelles) bi-infected by the two Wolbachia variants wHa and wNo were backcrossed to uninfected males in two conditions. In the first case, Seychelles males from a stock cured from its Wolbachia by tetracycline treatment were used. In the second case, the males came from a naturally uninfected Tunisian population. It was found that (i) the two Wolbachia variants can segregate, so that bi-infected females can produce a few offspring infected only by wHa or wNo. This occurs in both backcross conditions. (ii) Segregation leads more frequently to wHa than to wNo mono-infection. (iii) Wolbachia transmission is lower when the Seychelles genome is introgressed by the Tunisian genome, suggesting that host genomic factors might influence infection fate.

Abnormal spermiogenesis is associated with the X-linked sex-ratio trait in Drosophila simulans

The sex-ratio trait, known in several Drosophila species, results from X-linked meiotic drive that affects Y-bearing sperm and causes males to produce female-biased progeny. We describe spermiogenesis in three types of D. simulans males: wild-type, sex-ratio, and males that bear driver X chromosomes but do not express the sex-ratio trait because of autosomal and Y-linked suppression. Sex-ratio males show numerous spermatid nuclei in abnormal positions throughout their cysts, which occurs rarely, if ever, in the two other types. The degree of the spermiogenic failure in sex-ratio males is correlated with the bias towards females in their progeny. This proves that the trait is a case of meiotic drive and strongly suggests that the abnormal spermatids are Y-bearing ones. The number of cysts per testis, hence the production of X-bearing sperm, is not increased in sex-ratio males. Implications for the spread of the sex-ratio trait in natural populations of D. simulans are discussed.

Rapid Rise and Fall of Selfish Sex-Ratio X Chromosomes in Drosophila simulans: Spatiotemporal Analysis of Phenotypic and Molecular Data

Sex-ratio drive, which has been documented in several Drosophila species, is induced by X-linked segregation distorters. Contrary to Mendels law of independent assortment, the sex-ratio chromosome (X(SR)) is inherited by more than half the offspring of carrier males, resulting in a female-biased sex ratio. This segregation advantage allows X(SR) to spread in populations, even if it is not beneficial for the carriers. In the cosmopolitan species D. simulans, the Paris sex-ratio is caused by recently emerged selfish X(SR) chromosomes. These chromosomes have triggered an intragenomic conflict, and their propagation has been halted over a large area by the evolution of complete drive suppression. Previous molecular population genetics analyses revealed a selective sweep indicating that the invasion of X(SR) chromosomes was very recent in Madagascar (likely less than 100 years ago). Here, we show that X(SR) chromosomes are now declining at this location as well as in Mayotte and Kenya. Drive suppression is complete in the three populations, which display little genetic differentiation and share swept haplotypes, attesting to a common and very recent ancestry of the X(SR) chromosomes. Patterns of DNA sequence variation also indicate a fitness cost of the segmental duplication involved in drive. The data suggest that X(SR) chromosomes started declining first on the African continent, then in Mayotte, and finally in Madagascar and strongly support a scenario of rapid cycling of X chromosomes. Once drive suppression has evolved, standard X(ST) chromosomes locally replace costly X(SR) chromosomes in a few decades.