Female-biased Progeny Research Articles

Adaptation by the Brown Planthopper to Resistant Rice: A Test of Female-Derived Virulence and the Role of Yeast-like Symbionts.

Simple SummaryThe brown planthopper (Niliparvata lugens [Stål]) feeds on rice in Asia. Rice breeders have developed varieties with resistance to the planthopper; however, planthoppers quickly adapt to these varieties (called ‘virulence adaptation’). We examined the potential role during adaptation of endosymbionts that are passed by the female through the egg. We adapted planthoppers by exposure to resistant rice (IR62) for >20 generations, and crossed males or females from these adapted populations with non-adapted males and females that were reared on susceptible rice. Virulent males and females contributed to the virulence of their offspring as revealed through faster development rates, higher growth rates, greater numbers of female offspring, and an increased longevity of progeny on IR62 compared to the progeny of avirulent planthoppers on IR62; however, the female contribution to virulence was greater than that of the male. Reducing densities of YLS in adult planthoppers through heat treatment reduced their capacity to gain weight on IR62, irrespective of the virulence of parents, thereby suggesting that YLS derived from the female parent play a role in the vertical transfer of virulence; however, the effects were weak and IR62 seedlings were still more affected by heat-treated planthoppers with a virulent female parent than by heat-treated planthoppers with a virulent male parent or with avirulent parents only. Virulence is a complex state with multiple underlying mechanisms, some of which are derived only from the female parent.The adaptation by planthoppers to feed and develop on resistant rice is a challenge for pest management in Asia. We conducted a series of manipulative experiments with the brown planthopper (Nilaparvata lugens (Stål)) on the resistant rice variety IR62 (BPH3/BPH32 genes) to assess behavioral and bionomic changes in planthoppers exhibiting virulence adaptation. We also examined the potential role of yeast-like symbionts (YLS) in virulence adaptation by assessing progeny fitness (survival × reproduction) following controlled matings between virulent males or females and avirulent males or females, and by manipulating YLS densities in progeny through heat treatment. We found virulence-adapted planthoppers developed faster, grew larger, had adults that survived for longer, had female-biased progeny, and produced more eggs than non-selected planthoppers on the resistant variety. However, feeding capacity—as revealed through honeydew composition—remained inefficient on IR62, even after 20+ generations of exposure to the resistant host. Virulence was derived from both the male and female parents; however, females contributed more than males to progeny virulence. We found that YLS are essential for normal planthopper development and densities are highest in virulent nymphs feeding on the resistant host; however, we found only weak evidence that YLS densities contributed more to virulence. Virulence against IR62 in the brown planthopper, therefore, involves a complex of traits that encompass a series of behavioral, physiological, and genetic mechanisms, some of which are determined only by the female parent.

Reproductive success and progeny sex ratio of a laboratory colony of Anagyrus fusciventris (Hymenoptera: Encyrtidae)

ABSTRACT Anagyrus fusciventris (Girault) is a parasitoid of both Pseudococcus calceolariae (Maskell) and P. longispinus (Targioni Tozzetti), two economically important mealybug pests in New Zealand. A male-biased sex ratio was often observed in a laboratory colony of A. fusciventris. We investigated the effect of mating status on female A. fusciventris longevity, fecundity, progeny sex ratio and the rate of parasitism achieved under controlled laboratory conditions. In addition, the impact of host body size on progeny sex ratio was investigated. The progeny sex ratio of unmated (virgin) females (VF) and two types of mated females (24hM: opportunities for mating limited to 24 h or LtM – lifetime opportunities for mating) was tested under similar conditions. Results indicated that females can be reproductively active within 24 h. On average, 24hM females produced 23% female offspring while LtM females produced 45% females, suggesting that multiple mating is required for a balanced sex ratio. VF produced only male offspring through arrhenotokous parthenogenesis. When reared at 23°C and 16 h photoperiod, VF, 24hM and LtM females lived for 25, 44, 51 days, and parasitised 46, 67 and 87 mealybugs respectively. The average lifetime reproductive output (total number of offspring emerged) of VF, 24hM and LtM females was 41, 58 and 75 offspring, respectively. Female-biased progeny emerged from larger hosts while male-biased progeny often emerged from smaller hosts. Implications of these results are discussed in relation to opportunities to improve the quality of a laboratory colony with a balanced progeny sex ratio.

Occurrence, Seasonal Abundance, and Superparasitism of Ooencyrtus kuvanae (Hymenoptera: Encyrtidae) as an Egg Parasitoid of the Spotted Lanternfly (Lycorma delicatula) in North America

The occurrence of egg parasitoid Ooencyrtus kuvanae (Howard) (Hymenoptera: Encyrtidae) on its new host, the spotted lanternfly (Lycorma delicatula (White) (Hemiptera: Fulgoridae)), was surveyed at 4 study plots in 2016 and 10 additional plots in 2017 in Pennsylvania through field collection and laboratory incubation. O. kuvanae adults were found on L. delicatula egg mass surfaces at two plots (ODSouth and Lutz) in 2016, but at none in 2017. The results of laboratory incubation showed that O. kuvanae adults were only recovered from host eggs collected at plot ODSouth in 2016, with adults emerging between 22 April and 2 May 2016 at 22 ± 1 °C, 40% ± 5% relative humidity (RH), and a 16:8 h photoperiod (light/dark). The overall parasitism at this study plot was 6.0% by egg mass and 1.2% by egg. Two oviposition sites contained parasitized L. delicatula eggs, with 12.3% (9.5–15.0%) host egg masses and 3.1% (1.3–5.0%) host eggs utilized by the parasitoid. O. kuvanae parasitism by egg was significantly higher on oviposition site ODSouth #7 than on ODSouth #8. No O. kuvanae adults were reared out of field-collected host eggs from the 10 plots in 2017. Seasonal abundance and superparasitism of O. kuvanae was examined at plot ODSouth in 2017. O. kuvanae-parasitized L. delicatula eggs were found on all four oviposition sites based on field monitoring of parasitoid adult emergence, resulting in a parasitism of 35.4% (18.8–55.6%) by egg mass and 2.2% (0.5–3.9%) by egg. No significant difference in parasitism by egg was observed among oviposition sites. O. kuvanae adults emerged in the field between 2 May and 1 June 2017. Superparasitism was confirmed for O. kuvanae on L. delicatula eggs based on parasitoid production (1.0–3.3 adults/parasitized egg) and adult exit holes (1–3 exit holes/parasitized egg). As the first parasitoid recorded from L. delicatula in North America, O. kuvanae has the potential to become an important biological control agent for L. delicatula in North America, with its well-synchronized life history in the spring, century-long field establishment, superparasitism, and female-biased progeny population. L. delicatula complements the gypsy moth well as an alternative host for O. kuvanae in the field.

Potential New Associations of North American Parasitoids With the Invasive Asian Longhorned Beetle (Coleoptera: Cerambycidae) for Biological Control.

The Asian longhorned beetle, Anoplophora glabripennis (Motschulsky), is a polyphagous wood-boring insect native to Asia. Since it invaded North America in the 1990s, the beetle has been continuously targeted by quarantines and eradication programs in the United States and Canada. We examined the potential for development of new species-associations between A. glabripennis and hymenopteran parasitoids collected from cerambycids and other wood-boring insects infesting red maple (Acer rubrum L.) trees in the mid-Atlantic region of the United States. Results of our study showed that five groups of braconid parasitoids (Ontsira mellipes Ashmead, Rhoptrocentrus piceus Marsh, Spathius laflammei Provancher, Heterospilus spp., and Atanycolus spp.) successfully attacked early instars of A. glabripennis larvae infesting red maple logs and produced both male and female progenies. One species, O. mellipes, was continuously reared on A. glabripennis larvae inserted inside small red maple sticks for over 50 generations, and produced female-biased progeny (∼6:1 female to male ratio) at each generation. Continuous rearing of O. mellipes on A. glabripennis larvae did not significantly increase the parasitism and mean number of progeny produced per parasitized host. Together, these findings demonstrate that some North American parasitoids may be able to develop new associations with A. glabripennis and thus should be further studied under semifield or field conditions for possible use in biocontrol.

Influence of Food Supplements on the Reproductive Potential of the Parasitoid,Dinarmus basalis(Rondani) (Hymenoptera: Pteromalidae) onCallosobruchus chinensis(L.) (Coleoptera: Bruchidae)

Two adult food supplements, namely 10 % solutions of honey and sugar, were tested to evaluate the reproductive potential of the pteromalid parasitoid, Dinarmus basalis, on Callosobruchus chinensis (L.). Distilled water was fed as untreated control. The highest adult longevity was found when fed with 10 % honey solution (male 19.3 ± 0.68, female 27.9 ± 0.81 days) while the lowest was recorded when fed with distilled water (male 14.4±0.80, female 19.7±0.57 days). Females produced overall 143.6±0.52, 184.8±0.54 and 211.35±0.57 offspring when fed with water, sugar and honey, respectively. The total fecundities were 194.3±0.60, 245.85±0.63 and 273.9±0.66 per female when fed with water, sugar and honey, respectively. Time of development of the parasitoid was faster when females were fed with honey as compared to other food supplements. Sex ratios indicated that the parasitoid produced female-biased progenies. Dinarmus basalis produced progeny throughout their life sequentially and therefore it is synovigenic. The honey-fed female parasitoids showed the best performance with increased fecundity and longevity over the other food supplement.

Effect of beebread on the reproductive performance of Cotesia vestalis

The hypothesis that non-host-feeding synovigenic parasitoids are more likely to rely entirely upon teneral protein reserves for future egg and offspring production was tested in the present study. Protein-rich beebread was mixed with honey to form a paste (honey-beebread) and reproductive parameters of Cotesia vestalis were compared among females that were fed honey with or without beebread. Oviposition period lasted 3 and 8 days in unfed (but water-provided) and fed wasps, respectively. Satiated parasitoids attained peak offspring production within the first 2 days of eclosion, and production dropped sharply after 4 days. Wasps provided with honey-beebread produced more offspring and a more female-biased progeny than conspecifics that were raised on honey. In addition, posteclosion egg maturation progressed irrespective of diet and maximum egg load (102 mature eggs) was attained within 48 h of parasitoid emergence. Obtained results showed that supplementary protein sources could enhance some aspects of reproductive performance in non-host-feeding synovigenic parasitoids.

Female resistance behaviour and progeny sex ratio in two Bradysia species (Diptera: Sciaridae) with paternal genome elimination

The relationship between female mating preferences and sex allocation has received considerable theoretical and empirical support. Typically, choosier females adjust their progeny sex ratio towards sons, who inherit the attractive traits of their father. However, in species with paternal genome elimination, where male sperm do not contain the paternal genome, predictions for the direction of progeny sex ratio biases and their relationship with female choosiness are atypical. Paternal genome elimination also creates a potential for male-female conflict over sex allocation, and any influence of female mate choice on sex ratio outcomes have interesting implications for sexually antagonistic coevolution. Within the Sciaridae (Diptera) are species that produce single-sex progeny (monogenic species) and others in which progeny comprise both sexes (digenic species). Paternal genome elimination occurs in both species. We explore female mate resistance behaviour in a monogenic and digenic species of mushroom gnat from the genus Bradysia. Our experiments confirmed our theoretical predictions, revealing that in the monogenic and digenic species, females producing female-biased progeny were more likely to have resisted at least one mating attempt.

Environmental influence on primary sex ratio in a dioecious plant

The proximity of mates can influence mating opportunities and the quantity and quality of offspring, especially in dioecious plant species. Progeny sex ratios modulated by environmental conditions is one of the most radical ways in which offspring quality may be influenced, yet it has rarely been reported in plants. A mechanism proposed to influence progeny sex ratios in dioecious plants involves competition between female- and male-determining microgametophytes (certation) as a result of variation in pollination intensity. However, the role of selective fertilization in dioecious plants is controversial and has not been demonstrated under field conditions. Here we investigate whether natural variation in the spatial arrangement of females and males influences pollination intensity and progeny sex ratios in the wind-pollinated herb Rumex nivalis. Based on previous experimental manipulation of pollination intensity in this species, we predicted that maternal parents in close proximity to males would produce more strongly female-biased progeny sex ratios. We tested this prediction in six alpine populations in Switzerland by measuring the distance between focal females and neighboring males and assessing pollen loads and seed sex ratios of maternal parents. In four of the six populations, females positioned in close proximity to males captured more pollen and exhibited more female-biased sex ratios. Our results demonstrate that demographic aspects of the maternal mating environment can influence progeny sex ratios. The most probable explanation for biased primary sex ratios in Rumex is selective fertilization resulting from pollen tube competition.

Female-driven mechanisms, ejaculate size and quality contribute to the lower fertility of sex-ratio distorter males in Drosophila simulans

BackgroundSex-ratio meiotic drive refers to the preferential transmission of the X chromosome by XY males. The loss of Y-bearing sperm is caused by an X-linked distorter and results in female-biased progeny. The fertility of sex-ratio (SR) males expressing the distorter is usually strongly reduced compared to wild-type males, especially when they are in competition. The aim of this study was to identify the post-copulatory mechanisms that lower the fertility of SR males in Drosophila simulans. Parameters contributing to male fertility were measured in single and double mating conditions.ResultsThe most detrimental effect on SR males fertility is due to the size of their ejaculate which is half that of wild-type males. Sperm viability and sperm use by the females are also reduced. Sex-ratio males are poor sperm competitors in both offence and defence. We found evidence for sperm release from the female reproductive tract that specifically affects SR males. It results in the removal of stored sperm from a first SR mate without the action of the sperm of the second male. In addition, females mated once with an SR male remate more frequently with wild-type males.ConclusionThe paternity reduction of SR males in competitive conditions is greater than that attributable to their low sperm production and could prevent the spread of distorter X chromosomes in populations when multiple mating occur. The female-driven mechanisms are shown to play a major role both throughout the post-copulatory selective process and increased polyandry. The variation in male reproductive performance may drive the evolution of sexual learning capability of females.

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.

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.

POLLINATION INTENSITY INFLUENCES SEX RATIOS IN DIOECIOUS RUMEX NIVALIS, A WIND-POLLINATED PLANT

Determining the mechanisms governing sex-ratio variation in dioecious organisms represents a central problem in evolutionary biology. It has been proposed that in plants with sex chromosomes competition between pollen tubes of female- versus male-determining microgametophytes (certation) causes female-biased primary sex ratios. Experimental support for this hypothesis is limited and recent workers have cast doubt on whether pollen-tube competition can modify sex ratios in dioecious plants. Here we investigate the influence of variation in pollination intensity on sex ratios in Rumex nivalis, a wind-pollinated alpine herb with strongly female-biased sex ratios. In a garden experiment, we experimentally manipulated pollination intensity using three concentric rings of female recipient plants at different distances from a central group of male pollen donors. This design enabled us to test the hypothesis that increasing pollen load size, by intensifying gametophyte competition, promotes female-biased sex ratios in R. nivalis. We detected a significant decline in pollen load at successive distance classes with concomitant reductions in seed set. Sex ratios of progeny were always female biased, but plants at the closest distance to male donors exhibited significantly greater female bias than more distant plants. The amount of female bias was positively correlated with the seed set of inflorescences. Hand pollination of stigmas resulted in approximately 100-fold higher stigmatic pollen loads than wind-pollinated stigmas and produced exceptionally female-biased progenies (female frequency = 0.96). Our results are the first to demonstrate a functional relation between stigmatic pollen capture, seed set, and sex ratio and suggest that certation can contribute towards female-biased sex ratios in dioecious plants.

POLLINATION INTENSITY INFLUENCES SEX RATIOS IN DIOECIOUS RUMEX NIVALIS, A WIND-POLLINATED PLANT

Determining the mechanisms governing sex-ratio variation in dioecious organisms represents a central problem in evolutionary biology. It has been proposed that in plants with sex chromosomes competition between pollen tubes of female- versus male-determining microgametophytes (certation) causes female-biased primary sex ratios. Experimental support for this hypothesis is limited and recent workers have cast doubt on whether pollen-tube competition can modify sex ratios in dioecious plants. Here we investigate the influence of variation in pollination intensity on sex ratios in Rumex nivalis, a wind-pollinated alpine herb with strongly female-biased sex ratios. In a garden experiment, we experimentally manipulated pollination intensity using three concentric rings of female recipient plants at different distances from a central group of male pollen donors. This design enabled us to test the hypothesis that increasing pollen load size, by intensifying gametophyte competition, promotes female-biased sex ratios in R. nivalis. We detected a significant decline in pollen load at successive distance classes with concomitant reductions in seed set. Sex ratios of progeny were always female biased, but plants at the closest distance to male donors exhibited significantly greater female bias than more distant plants. The amount of female bias was positively correlated with the seed set of inflorescences. Hand pollination of stigmas resulted in ∼100-fold higher stigmatic pollen loads than wind-pollinated stigmas and produced exceptionally female-biased progenies (female frequency = 0.96). Our results are the first to demonstrate a functional relation between stigmatic pollen capture, seed set, and sex ratio and suggest that certation can contribute towards female-biased sex ratios in dioecious plants.

Reproduction and progeny of Silene latifolia (Caryophyllaceae) as affected by atmospheric CO2 concentration

Sexual dimorphism in plants has been known for over two millennia. However, little is known about how male and female reproduction of dioecious species will respond to anthropogenic environmental perturbations. Using growth chambers, the effects of CO(2) enrichment on male and female reproduction in Silene latifolia were examined and whether parental CO(2) environment affected progeny germination and sex ratio. Reproduction of male and female S. latifolia was enhanced by a similar magnitude at elevated CO(2). Over the growing season, males produced 16 times as many flowers as females did fruits per plant, but no difference in reproductive biomass between genders was observed at ambient or elevated CO(2). Germination of seeds produced by plants grown at different CO(2) concentrations was significantly different. Female seeds from higher CO(2)-grown plants tended to emerge earlier than those from ambient-CO(2)-grown plants, but emergence of male seeds was little affected. Overall, seeds from elevated-CO(2)-grown plants had 20% higher germination and were more female-biased than those from ambient-CO(2)-grown plants. Because of the enhanced reproduction and more female-biased progeny under elevated CO(2), the population structure of this cosmopolitan weedy species will likely be altered in a future environment.

Evolution of autosomal suppression of the sex-ratio trait in Drosophila.

The sex-ratio trait is the production of female-biased progenies due to X-linked meiotic drive in males of several Drosophila species. The driving X chromosome (called SR) is not fixed due to at least two stabilizing factors: natural selection (favoring ST, the nondriving standard X) and drive suppression by either Y-linked or autosomal genes. The evolution of autosomal suppression is explained by Fisher's principle, a mechanism of natural selection that leads to equal proportion of males and females in a sexually reproducing population. In fact, sex-ratio expression is partially suppressed by autosomal genes in at least three Drosophila species. The population genetics of this system is not completely understood. In this article we develop a mathematical model for the evolution of autosomal suppressors of SR (sup alleles) and show that: (i). an autosomal suppressor cannot invade when SR is very deleterious in males (c < (1)/(3), where c is the fitness of SR/Y males); (ii). "SR/ST, sup/+" polymorphisms occur when SR is partially deleterious ( approximately 0.3 < c < 1); while (iii). SR neutrality (c = 1) results in sup fixation and thus in total abolishment of drive. So, surprisingly, as long as there is any selection against SR/Y males, neutral autosomal suppressors will not be fixed. In that case, when a polymorphic equilibrium exists, the average female proportion in SR/Y males' progeny is given approximately by ac + 1 - a + a (2) c + 1 (2) + 1 - 4ac /4ac, where a is the fitness of SR/ST females.

Influence of Diet on Life History and Predatory Capacity of Amblyseius zaheri Yousef &amp; El-Brolossy (Acari: Phytoseiidae)

Laboratory experiments were conducted to investigate the effect of diet on the biology and predation capacity of the phytoseiid mite Amblyseius zaheri Yousef & El-Brolossy. The predatory mite was able to develop and reproduce when fed on nymphs of the twospotted spider mite Tetranychus urticae Koch, nymphs of the citrus brown mite Eutetranychus orientalis Klein, motile stages of the eriophyid mite Eriophyes dioscoridis Soliman & Abou-Awad, eggs of the scale insect Parlatoria ziziphus Lucas, nymphs of the whitefly Bemisia tabaci (Genn.) and pollen grains of date palm, Phoenix dactylifera. The predatory mite’s development was fastest on a diet of nymphs of Er. dioscoridis. All of the diets led to a female-biased progeny, which was most pronounced in predators fed on date palm pollen. The results are discussed in light of the biological control capacity of the phytoseiid mite.

Mother's mitochondria and optimal offspring sex ratio

In certain cases, predicted by evolutionary theory of sex-allocation and confirmed by empirical evidence, animals adaptively change their progeny sex-ratio according to individual circumstances. Here we argue that a similar response of offspring sex-ratio must exist in relation to genetic variation of mothers’ mitochondria, as a consequence of maternal inheritance of these organelles and of their influence on fitness resulting from their crucial role in metabolism. In fact, a mathematical analysis of evolutionary dynamics of sex-allocation mutants demonstrates that natural selection promotes an evolutionarily stable allocation policy where mothers with defective mitochondria generate only sons, while those with optimal mitochondria have female biased progenies.

Incidência natural e biologia de Trichogramma atopovirilia Oatman &amp; Platner, 1983 (Hymenoptera, Trichogrammatidae) em ovos de Anticarsia gemmatalis Hübner, 1818 (Lepidoptera, Noctuidae)

Trichogramma atopovirilia Oatman & Platner is an egg parasitoid of the corn earworm Helicoverpa zea (Boddie) (Lepidoptera, Noctuidae), and has recently been collected from eggs of Anticarsia gemmatalis Hubner on soybeans. In order to evaluate the suitability of A. gemmatalis eggs as hosts of T. atopovirilia, field surveys were conducted in 1999 and 2000 on corn and soybeans, and a colony of the parasitoid was established in laboratory. At 25 oC, development from oviposition to emergence lasted nine days and a sex-ratio of 0.58 (females:males) was obtained. Females lived significantly longer (11.4 days) when kept in ovipositional activity, than in the absence of host eggs (6.6 days). Total fecundity averaged 104.5 parasitized eggs, resulting in the emergence of 138.3 descendents. Mean daily fecundity was highest (30 eggs/female) on the first day. Oviposition continued until one day before the death of the females, however 70% of the eggs were laid during the first four days after emergence. A female-biased progeny was produced during the first three days of oviposition, whereas further ovipositions were male-biased. Females lived significantly longer when exposed to host eggs in comparison to females deprived of eggs. The results show that eggs of A. gemmatalis are suitable for the development of T. atopovirilia, and this parasitoid should be considered in future programs of biological control of the velvetbean caterpillar.

The evolution of autosomal suppressors of sex-ratio drive in Drosophila simulans.

Sex-ratio drive, which results in males siring female-biased progeny, has been reported in several Drosophila species, including D. simulans. It is caused by X-linked drivers that prevent the production of Y-bearing sperm. In natural populations of D. simulans, the drivers are usually cryptic, because their spread has elicited the evolution of drive suppressors. We investigated autosomal suppression in flies from Madagascar, Réunion and Kenya. Autosomal suppressors were found in all three places, indicating that they are a regular component of drive suppression over this geographic area, where strong Y-linked suppressors also occur. These suppressors were suspected of being polymorphic in Madagascar and Réunion and proved to be polymorphic in Kenya. We developed a model simulating the evolution of neutral autosomal suppressors in order to explore the effects of the number of suppressor genes, their relative strength and the co-occurrence of Y-linked suppressors. The most interesting prediction of the model is that when suppression is multigenic, suppressor loci can remain polymorphic despite the absence of balancing selection if an equal sex-ratio is restored in the population before the suppressor alleles become fixed at all loci. The model also emphasises the importance of the sterility of distorters' sons in suppressor dynamics.

Sex-ratio drive in Drosophila simulans: variation in segregation ratio of X chromosomes from a natural population.

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.