Sex-ratio System Research Articles

The fate of a suppressed X-linked meiotic driver: experimental evolution in Drosophila simulans.

Sex-ratio (SR) meiotic drivers are X-linked selfish genetic elements that promote their own transmission by preventing the production of Y-bearing sperm, which usually lowers male fertility. The spread of SR drivers in populations is expected to trigger the evolution of unlinked drive suppressors, a theoretically predicted co-evolution that has been observed in nature. Once completely suppressed, the drivers are expected either to decline if they still affect the fitness of their carriers, or to evolve randomly and possibly get fixed if the suppressors eliminate their deleterious effects. To explore this issue, we used the Paris sex-ratio system of Drosophila simulans in which drive results from the joint effect of two elements on the X chromosome: a segmental duplication and a deficient allele of the HP1D2 gene. We set up six experimental populations starting with 2/3 of X chromosomes carrying both elements (XSR) in a fully suppressing background. We let them evolve independently during almost a hundred generations under strong sexual competition, a condition known to cause the rapid disappearance of unsuppressed Paris XSR in previous experimental populations. In our study, the fate of XSR chromosomes varied among populations, from extinction to their maintenance at a frequency close to the starting one. While the reasons for these variable outcomes are still to be explored, our results show that complete suppression can prevent the demise of an otherwise deleterious XSR chromosome, turning a genetic conflict into cooperation between unlinked loci. Observations in natural populations suggest a contrasting fate of the two elements: disappearance of the duplication and maintenance of deficient HP1D2 alleles.

X-chromosome meiotic drive in Drosophila simulans: a QTL approach reveals the complex polygenic determinism of Paris drive suppression.

Meiotic drivers are selfish genetic elements that promote their own transmission into the gametes, which results in intragenomic conflicts. In the Paris sex-ratio system of Drosophila simulans, drivers located on the X chromosome prevent the segregation of the heterochromatic Y chromosome during meiosis II, and hence the production of Y-bearing sperm. The resulting sex-ratio bias strongly impacts population dynamics and evolution. Natural selection, which tends to restore an equal sex ratio, favors the emergence of resistant Y chromosomes and autosomal suppressors. This is the case in the Paris sex-ratio system where the drivers became cryptic in most of the natural populations of D. simulans. Here, we used a quantitative trait locus (QTL) mapping approach based on the analysis of 152 highly recombinant inbred lines (RILs) to investigate the genetic determinism of autosomal suppression. The RILs were derived from an advanced intercross between two parental lines, one showing complete autosomal suppression while the other one was sensitive to drive. The confrontation of RIL autosomes with a reference XSR chromosome allowed us to identify two QTLs on chromosome 2 and three on chromosome 3, with strong epistatic interactions. Our findings highlight the multiplicity of actors involved in this intragenomic battle over the sex ratio.

Sequence Analysis of the Segmental Duplication Responsible for ParisSex-RatioDrive inDrosophila simulans

Sex-ratio distorters are X-linked selfish genetic elements that facilitate their own transmission by subverting Mendelian segregation at the expense of the Y chromosome. Naturally occurring cases of sex-linked distorters have been reported in a variety of organisms, including several species of Drosophila; they trigger genetic conflict over the sex ratio, which is an important evolutionary force. However, with a few exceptions, the causal loci are unknown. Here, we molecularly characterize the segmental duplication involved in the Paris sex-ratio system that is still evolving in natural populations of Drosophila simulans. This 37.5 kb tandem duplication spans six genes, from the second intron of the Trf2 gene (TATA box binding protein-related factor 2) to the first intron of the org-1 gene (optomotor-blind-related-gene-1). Sequence analysis showed that the duplication arose through the production of an exact copy on the template chromosome itself. We estimated this event to be less than 500 years old. We also detected specific signatures of the duplication mechanism; these support the Duplication-Dependent Strand Annealing model. The region at the junction between the two duplicated segments contains several copies of an active transposable element, Hosim1, alternating with 687 bp repeats that are noncoding but transcribed. The almost-complete sequence identity between copies made it impossible to complete the sequencing and assembly of this region. These results form the basis for the functional dissection of Paris sex-ratio drive and will be valuable for future studies designed to better understand the dynamics and the evolutionary significance of sex chromosome drive.

IMPROVING MATING PERFORMANCE OF MASS-REARED STERILE MEDITERRANEAN FRUIT FLIES (DIPTERA: TEPHRITIDAE) THROUGH CHANGES IN ADULT HOLDING CONDITIONS: DEMOGRAPHY AND MATING COMPETITIVENESS

Mass rearing conditions affect the mating behavior of Mediterranean fruit flies (medflies) Ceratitis capitata (Wiedemann). We evaluated the effect of slight changes in the adult holding conditions of adult flies maintained for egg production on their mating performance. Colonization was initiated from wild flies collected as larvae from infested coffee berries (Coffea arabica L.). When pupae were close to adult emergence, they were randomly divided into 3 groups and the emerging adults were reared under the following conditions: (1) Metapa System (MS, control), consisting of 70 × 45 × 15 cm aluminum frame, mesh covered cages, with a density of 2,200 flies per cage and a 1:1 initial sex ratio; (2) Insert System (IS), with the same type of cage, and the same fly density and sex ratio as in the MS treatment, but containing twelve Plexiglas® pieces (23 × 8.5 cm) to provide additional horizontal surface areas inside the cage; and (3) Sex-ratio System (SS), same as IS, but in this case the initial male: female ratio was 4:1. Three d later, newly emerged females were introduced, so the ratio became 3:1 and on the 6th d another group of newly emerged females was added to provide a 2:1 final sex ratio, at which the final density reached 1,675 flies per cage. The eggs collected from each of the 3 treatments were reared independently following standard procedures and the adults were held under the same experimental conditions. This process was repeated for over 10 to 13 generations (1 year). The experiment was repeated 3 times in 3 consecutive years, starting each replicate with a new collection of wild flies. Life tables were constructed for each treatment at the parental, 3rd, 6th, and 9th generations. Standard quality control parameters (pupation at 24 h, pupal weight, adult emergence, and flight ability), were estimated for each treatment every third generation in the third year. For the last generation each year, mating competitiveness was evaluated in field cage tests with wild flies. As colonization progressed, life expectancy and fecundity rates increased in the 3 rearing systems. There was no significant difference in standard quality control parameters among the 3 rearing systems. Wild males always achieved more matings than any of the mass reared males. Mating competitiveness of males from the IS, although surprisingly not from the SS, was significantly greater than that of males from the MS. Our results indicate that these slight changes in the adult holding conditions can significantly reduce the harmful effects of mass rearing on the mating performance of sterile flies.

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.

A Comparative Approach to the Population-Genetics Theory of Segregation Distortion

Mathematical models of four well-known naturally occurring systems of segregation distortion are compared. These include the sex-ratio chromosome of Drosophila pseudoobscura, the Segregation Distorter (SD) complex of D. melanogaster, the t locus in Mus musculus, and the sex-ratio system in Aedes aegypti. Dynamics of these models are compared with the classical one-locus multiple-allele viability system. For the SD complex and the sex-ratio model of A. aegypti, the role of recombination is reviewed. Departures from Mendelian segregation cause fascinating irregularities in the relationship between linkage and linkage disequilibrium, as well as in predictions for the evolution of recombination itself.

VIRILITY DEFICIENCY AND THE SEX-RATIO TRAIT IN DROSOPHILA PSEUDOOBSCURA. II. MULTIPLE MATING AND OVERALL VIRILITY SELECTION

Previous studies on fitness components of Drosophila have shown the over-whelming importance of virility selection. In this study, virility selection is further partitioned into two components-one with respect to virgin females and the other with respect to nonvirgin females. The relative importance of the two components to the overall virility selection depends on the remating tendency of females which is investigated here. A theoretical model is then proposed to estimate virility selection under the condition of frequent female remating. The model is tested experimentally. When this model is applied to the Sex-Ratio system of D. pseudoobscura, Sex-Ratio males are found to suffer substantial virility reduction. The significance of this finding to the Sex-Ratio problem is discussed.

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.