Genetics of Drosophila simulans male mating discrimination in crosses with D. melanogaster

The genetic bases of sexual isolation between Drosophila melanogaster and D. simulans have been mainly studied in females, and there is little information about the role of the males in interspecific mating discrimination. Using D. simulans synthetic lines with compound chromosomes from a population of the Seychelles Islands (high frequency of interspecific mating) and a multimarker strain (low frequency), we show that D. simulans males play an important role in discriminating D. melanogaster females. The genetics of male discrimination fits well with the inheritance mode of a single locus, dominant for sexual isolation, located in chromosome II near the net mutation (2L-0.0). The heterospecific mating success of the male was not related to his sexual vigor. The specific load of male cuticular hydrocarbons was counted as a possible source of discrimination used by the D. melanogaster female.     

Genetic analysis of female mating recognition between Drosophila ananassae and Drosophila pallidosa: application of interspecific mosaic genome lines

Drosophila ananassae and Drosophila pallidosa are closely related species that can produce viable and fertile hybrids of both sexes, although strong sexual isolation exists between the two species. Females are thought to discriminate conspecific from heterospecific males based on their courtship songs. The genetic basis of female discrimination behavior was analyzed using isogenic females from interspecific mosaic genome lines that carry homozygous recombinant chromosomes. Multiple regression analysis indicated a highly significant effect of the left arm of chromosome 2 (2L) on the willingness of females to mate with D. ananassae males. Not only 2L but also the left arm of chromosome X (XL) and the right arm of chromosome 3 (3R) had significant effects on the females' willingness to mate with D. pallidosa males. All regions with strong effects on mate choice have chromosome arrangements characterized by species-specific inversions. Heterospecific combinations of 2L and 3R have previously been suggested to cause postzygotic reproductive isolation. Thus, genes involved in premating as well as postmating isolation are located in or near chromosomal inversions. This conclusion is consistent with the recently proposed hypothesis that "speciation genes" accumulate at a higher rate in non-recombining genome regions when species divergence occurs in the presence of gene flow.     

Quantitative trait loci for sexual isolation between Drosophila simulans and D. mauritiana

Sexual isolating mechanisms that act before fertilization are often considered the most important genetic barriers leading to speciation in animals. While recent progress has been made toward understanding the genetic basis of the postzygotic isolating mechanisms of hybrid sterility and inviability, little is known about the genetic basis of prezygotic sexual isolation. Here, we map quantitative trait loci (QTL) contributing to prezygotic reproductive isolation between the sibling species Drosophila simulans and D. mauritiana. We mapped at least seven QTL affecting discrimination of D. mauritiana females against D. simulans males, three QTL affecting D. simulans male traits against which D. mauritiana females discriminate, and six QTL affecting D. mauritiana male traits against which D. simulans females discriminate. QTL affecting sexual isolation act additively, are largely different in males and females, and are not disproportionately concentrated on the X chromosome: The QTL of greatest effect are located on chromosome 3. Unlike the genetic components of postzygotic isolation, the loci for prezygotic isolation do not interact epistatically. The observation of a few QTL with moderate to large effects will facilitate positional cloning of genes underlying sexual isolation.     

Evidence for no sexual isolation between Drosophila albomicans and D. nasuta

Sexual isolation, the reduced tendency to mate, is one of the reproductive barriers that prevent gene flow between different species. Various species‐specific signals during courtship contribute to sexual isolation between species. Drosophila albomicans and D. nasuta are closely related species of the nasuta subgroup within the Drosophila immigrans group and are distributed in allopatry. We analyzed mating behavior and courtship as well as cuticular hydrocarbon profiles within and between species. Here, we report that these two species randomly mated with each other. We did not observe any sexual isolation between species or between strains within species by multiple‐choice tests. Significant difference in the courtship index was detected between these two species, but males and females of both species showed no discrimination against heterospecific partners. Significant quantitative variations in cuticular hydrocarbons between these two species were also found, but the cuticular hydrocarbons appear to play a negligible role in both courtship and sexual isolation between these two species. In contrast to the evident postzygotic isolation, the lack of sexual isolation between these two species suggests that the evolution of premating isolation may lag behind that of the intergenomic incompatibility, which might be driven by intragenomic conflicts.     

Characterization of assortative mating in medaka: Mate discrimination cues and factors that bias sexual preference

Somatolactin alpha (SLα) is a peptide hormone that regulates skin color, and SLα-deficient and SLα-excess strains have been established in medaka (Oryzias latipes). Their skin colors differ conspicuously and males prefer to mate with females from the same strain. Pre-mating sexual isolation in this model vertebrate provides an ideal platform for investigating the molecular mechanisms of mate choice. Thus, we studied the sensory cues utilized by these fish to discriminate the same and different strains. When males were given a choice under monochromatic light, where the skin colors differed only in terms of brightness but not in hue, mating occurred but it was not assortative. This suggests that: (1) a visual cue is essential for mate discrimination rather than odor or acoustic cues; (2) the visual cue is color and not shape, size, or motion; and (3) the color cue needs to be perceived as the relative balance of brightness at multiple wavelengths rather than the brightness at a specific wavelength. In addition, we introduced another skin-color mutation into the SLα-excess strain and found that this new strain and the original SLα-excess strain, which also overexpressed SLα but exhibited distinct skin colors, preferred different colors. This demonstrates that SLα is not a primary determinant of sexual preference. The symmetrically biased sexual preferences of the SLα-deficient and SLα-excess strains may be acquired postnatally depending on their individual skin color or that of tank mates.     

Copy number variation in Y chromosome multicopy genes is linked to a paternal parent-of-origin effect on CNS autoimmune disease in female offspring

BackgroundThe prevalence of some autoimmune diseases is greater in females compared with males, although disease severity is often greater in males. The reason for this sexual dimorphism is unknown, but it may reflect negative selection of Y chromosome-bearing sperm during spermatogenesis or male fetuses early in the course of conception/pregnancy. Previously, we showed that the sexual dimorphism in experimental autoimmune encephalomyelitis (EAE) is associated with copy number variation (CNV) in Y chromosome multicopy genes. Here, we test the hypothesis that CNV in Y chromosome multicopy genes influences the paternal parent-of-origin effect on EAE susceptibility in female mice.ResultsWe show that C57BL/6 J consomic strains of mice possessing an identical X chromosome and CNV in Y chromosome multicopy genes exhibit sperm head abnormalities and female-biased sex ratio. This is consistent with X-Y intragenomic conflict arising from an imbalance in CNV between homologous X:Y chromosome multicopy genes. These males also display paternal transmission of EAE to female offspring and differential loading of microRNAs within the sperm nucleus. Furthermore, in humans, families of probands with multiple sclerosis similarly exhibit a female-biased sex ratio, whereas families of probands affected with non-sexually dimorphic autoimmune diseases exhibit unbiased sex ratios.ConclusionsThese findings provide evidence for a mechanism at the level of the male gamete that contributes to the sexual dimorphism in EAE and paternal parent-of-origin effects in female mice, raising the possibility that a similar mechanism may contribute to the sexual dimorphism in multiple sclerosis.

Electronic supplementary material

The online version of this article (doi:10.1186/s13059-015-0591-7) contains supplementary material, which is available to authorized users.     

The genetic basis of prezygotic reproductive isolation between Drosophila santomea and D. yakuba due to mating preference

Sexual isolating mechanisms that act before fertilization are often considered the most important genetic barriers leading to speciation in animals. While progress has been made toward understanding the genetic basis of the postzygotic isolating mechanisms of hybrid sterility and inviability, little is known about the genetic basis of prezygotic sexual isolation. Here, we map quantitative trait loci (QTL) contributing to prezygotic reproductive isolation between the sibling species Drosophila santomea and D. yakuba. We mapped at least three QTL affecting discrimination of D. santomea females against D. yakuba males: one X-linked and one autosomal QTL affected the likelihood of copulation, and a second X chromosome QTL affected copulation latency. Three autosomal QTL also affected mating success of D. yakuba males with D. santomea. No epistasis was detected between QTL affecting sexual isolation. The QTL do not overlap between males and females and are not disproportionately concentrated on the X chromosome. There was some overlap in map locations of QTL affecting sexual isolation between D. santomea and D. yakuba with QTL affecting sexual isolation between D. simulans and D. mauritiana and with QTL affecting differences in pigmentation between D. santomea and D. yakuba. Future high-resolution mapping and, ultimately, positional cloning, will reveal whether these traits do indeed have a common genetic basis.     

Enhancing mating performance after juvenile hormone treatment in Anastrepha fraterculus: a differential response in males and females acts as a physiological sexing system

Methoprene (a mimic of juvenile hormone) treatment can reduce the time required for sexual maturation in Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae) males under laboratory conditions, supporting its use as a treatment for sterile males within the context of the sterile insect technique (SIT). We evaluated sexual behaviour, mating competitiveness of methoprene-treated males, and female readiness to mate after methoprene-treatment in field cages. The study involved two strains of A. fraterculus from Argentina and Peru, which show several polymorphisms in relation to their sexual behaviour. We also analyzed whether methoprene treatment affected male and/or female behaviour in the same way in these two strains. Methoprene-treated males were equally competitive with untreated mature males, and became sexually competitive 6 days after emergence (3–4 days earlier than untreated males). In contrast, methoprene did not induce sexual maturation in females or, at least, it did not induce a higher rate of mating in 7-day-old females. These results were observed both for the Argentina and the Peru strains. Altogether, our results indicate that methoprene treatment produces sexually competitive males in field cages. In the absence of a genetic sexing system, and when sterile males and females of A. fraterculus are released simultaneously, the fact that females do not respond as do males to the methoprene treatment acts as a physiological sexing effect. Therefore, in the presence of mainly sexually immature sterile females, released sexually mature sterile males would have to disperse in search of wild fertile females, thereby greatly reducing matings among the released sterile insects and thus enhancing sterile insect technique efficiency.     

Genetics of sexual isolation based on courtship song between two sympatric species: Drosophila ananassae and D. pallidosa

Sexual isolation has been considered one of the primary causes of speciation and its genetic study has the potential to reveal the genetics of speciation. In Drosophila, the importance of courtship songs in sexual isolation between closely related species has been well investigated, but studies analysing the genetic basis of the difference in the courtship songs associated with sexual isolation are less well documented. Drosophila ananassae and Drosophila pallidosa are useful for studies of sexual isolation, because of their sympatric distribution and absence of postmating isolation. Courtship songs are known to play a crucial role in sexual isolation between these two species, and the female discrimination behaviour against the courting male has been revealed to be controlled by a very narrow region on the second chromosome. In this study we investigated the genetic basis controlling the song differences associated with their sexual isolation, using intact and wingless males with chromosomes substituted between species. The results obtained from F₁ hybrid males between these species indicate the dominance of the song characters favoured by D. pallidosa females. In addition, the results obtained from backcross F₂ males indicate that chromosome 2 had a major effect on the control of the song characters associated with sexual isolation.     

X-chromosome dosage affects male sexual behavior

Sex differences in the brain and behavior are primarily attributed to dichotomous androgen exposure between males and females during neonatal development, as well as adult responses to gonadal hormones. Here we tested an alternative hypothesis and asked if sex chromosome complement influences male copulatory behavior, a standard behavior for studies of sexual differentiation. We used two mouse models with non-canonical associations between chromosomal and gonadal sex. In both models, we found evidence for sex chromosome complement as an important factor regulating sex differences in the expression of masculine sexual behavior. Counter intuitively, males with two X-chromosomes were faster to ejaculate and display more ejaculations than males with a single X. Moreover, mice of both sexes with two X-chromosomes displayed increased frequencies of mounts and thrusts. We speculate that expression levels of a yet to be discovered gene(s) on the X-chromosome may affect sexual behavior in mice and perhaps in other mammals.     

GENETIC VARIATION FOR FEMALE MATE DISCRIMINATION IN DROSOPHILA MELANOGASTER

Comparisons between the Canton-S and Tai-Y strains of Drosophila melanogaster (both wild type) revealed variation in female mate discrimination based on chemical courtship signals present as hydrocarbons on the male cuticle. Mating tests indicated that 7-tricosene, which is the primary hydrocarbon on the Canton-S male cuticle but is nearly absent from Tai-Y, was a significant component of the signal. The discrimination was asymmetrical in that Canton-S females clearly distinguished between the two types of males in no-choice tests, but Tai-Y females did not. F₁ females expressed an intermediate ability to discriminate, and female progeny of backcrosses expressed a mating phenotype very similar to that of the parental strain to which the backcross was made. Analysis of independent effects from the X and both major autosomes indicated that the discrimination is controlled by gene(s) on chromosome 3.     

Co-adaptation of pheromone production and behavioural responses in Drosophila melanogaster males

In Drosophila melanogaster, male courtship behaviour is genetically controlled and is influenced by sex pheromones. 7-tricosene (7-T) induces a dose-dependent inhibition of male-male courtship, whereas 7,11-dienes stimulate male courtship of females. There is a geographical quantitative variation in the production of two predominant male hydrocarbons, 7-T and 7-pentacosene (7-P). We have previously found that 7-P, the main hydrocarbon from males of West African strains, stimulates males that mainly produce 7-T. Using both 'natural' and genetically engineered strains, we find that genetic factors coding for low levels of 7-P in males have co-evolved with factor(s) coding for male responses to high levels of 7-P. These two phenotypes are coded by factors on different chromosomes: the intraspecific polymorphism for the production of 7-T and 7-P is largely controlled by chromosome 2, whereas the variation in courtship towards 7-P-rich males is largely controlled by chromosome 3. The polymorphism of male courtship towards 7-P-rich males shows no correlation with the variation in male responses to female flies.     

根田鼠气味识别的性二型

以新鲜尿和粪作气味源,在行为选择箱中观察根田鼠的行为识别模式,结果表明：雌鼠对陌生同性尿、粪气味源行为识别的差异不显,雄鼠对陌生同性尿、粪气味源的行为识别在多个指标上存在显差异;根田鼠对陌生异性尿、粪的行为响应模式无明显差异;除嗅舔时间外,雌、雄鼠对粪气味的行为识别在其他指标上不存在明显差异;比较雌、雄鼠对尿刺激的行为识别发现,雄鼠对尿刺激的访问频次和反标记显大于雌鼠,雌性嗅舔时间显大于雄性,其他方面二之间并无显差异。因此,雌、雄性根田鼠对粪气味的行为识别模式不存在性别差异;对尿气味的行为识别模式存在性别差异。     

Genetic architecture of variation in sex-comb tooth number in Drosophila simulans

The sex comb on the forelegs of Drosophila males is a secondary sexual trait, and the number of teeth on these combs varies greatly within and between species. To understand the relationship between the intra- and interspecific variation, we performed quantitative trait locus (QTL) analyses of the intraspecific variation in sex-comb tooth number. We used five mapping populations derived from two inbred Drosophila simulans strains that were divergent in the number of sex-comb teeth. Although no QTLs were detected on the X chromosome, we identified four QTLs on the second chromosome and three QTLs on the third chromosome. While identification and estimated effects of the second-chromosome QTLs depend on genetic backgrounds, significant and consistent effects of the two third-chromosome QTLs were found in two genetic backgrounds. There were significant epistatic interactions between a second-chromosome QTL and a third-chromosome QTL, as well as between two second-chromosome QTLs. The third-chromosome QTLs are concordant with the locations of the QTLs responsible for the previously observed differences in sex-comb tooth number between D. simulans and D. mauritiana.     

On the prospects of using balanced sex-linked lethals for insect pest control

Summary A new method is suggested for controlling species of insect pests in which the female is heterogametic. This method, involving the use of balanced lethals on the Z chromosome, causes the death of females in the embryonic stage. The method has already been tested in practical sericulture for the production of entirely male progeny of the silkworm. The method requires the construction of two strains of the pest, one carrying two balanced nonallelic but closely located lethals on the Z chromosome, and another with two other pairs of lethals of the same type. In the hybrid progeny from the crosses between the two strains, 100% of the female embryos would die, thus making it possible to release only males without any laborious procedure for sex discrimination. In the progeny from the crosses between the released males and females from the natural population, again 100% of females would die, but the males would survive and when they mated — 62.5% of the female progeny would die. This rate would decline to 34.4 and 16.6% in the sons and grandsons respectively. The repeated release of hybrid males would lead to a progressive increase, with each successive generation, in the percentage of female mortality in the natural population until its total extinction.     

Seeking a Sex‐Specific Coolidge Effect in a Simultaneous Hermaphrodite

In polygamous mating systems, a capability to discriminate against familiar mates may be beneficial to both sexes. Polyandrous females, for instance, may enhance the odds of finding sires with optimal genetic compatibility or high genetic quality by mating with multiple different males; polygynous males, in addition, may more efficiently invest their limited ejaculates across multiple (rather than single) females. The Coolidge effect facilitates this kind of mate discrimination, as sexual motivation declines across consecutive copulations with a familiar partner but resurrects with a novel mate. In simultaneous hermaphrodites, we expect the Coolidge effect to show sex role‐dependent patterns and vary with previous sex‐specific mating activity. Using the promiscuous hermaphroditic sea slug Chelidonura sandrana, we investigated (1) whether sexual motivation indeed declines when repeatedly exposed to familiar partners, (2) whether the Coolidge effect occurs in a sex‐specific manner and (3) whether ejaculation is strategic with respect to partner familiarity. We found neither mating latency, nor penis intromission duration, mating propensity or the frequency of sex role alternations to vary significantly with treatments. Furthermore, slugs did not donate larger ejaculates to novel than to familiar partners. Partner novelty thus elicited no detectable response in sexual motivation or mating effort in C. sandrana. We suggest that the sea slugs' promiscuous mating system in often large mating aggregations makes mate discrimination based on novelty obsolete in comparison with more relevant criteria such as partner body size or mating history.     

Evolutionary implications of developmental instability in parthenogenetic Drosophila mercatorum. II. Comparison of two strains with identical genotypes,but different modes of reproduction

Developmental instability is particularly pronounced in parthenogenetic strains of Drosophila mercatorum. All parthenogenetically produced eggs in a given strain have the same genotype, but even when reared in the same environment, only approximately 5% of the eggs initiating development ever reach adulthood. A sexual analogue of a parthenogenetic strain was created to investigate the basis of this developmental instability. The two strains have identical genotypes (except for the Y chromosome in males of the sexual strain) and differ only in mode of reproduction. The sexual strain had a much lower rate of developmental instability than the parthenogenetic strain, suggesting that the instability is caused by the mode of reproduction per se and is not due to homozygosity, disruption of coadapted gene complexes, or any other feature of the parthenogenetic genome. The increased rate of abortion with parthenogenetic reproduction is caused by a proportional increase in the normal panoply of errors that occur in sexual reproduction but at a much lower rate. Attempts to establish other sexual analogues of laboratory parthenogenetic strains revealed different male sterility factors within several parthenogenetic genomes that could potentially act to prevent hybridization with sexually reproducing ancestors during the incipient stages in the evolution of an entirely parthenogenetic lineage.     

A Z‐linked sterility locus causes sexual abstinence in hybrid females and facilitates speciation in Spodoptera frugiperda

In the fall armyworm, Spodoptera frugiperda (Lepidoptera, Noctuidae), two sympatric strains have been recognized that have been termed corn strain (C) and rice strain (R), referring to their most common host plants. Both strains are reproductively isolated via a distinct prezygotic barrier as well as via an intriguing postzygotic phenomenon: when R females have mated with C males, the resulting RC hybrid females exhibit dramatically reduced fertility independent of their mating partner. Here, we demonstrate that the reduced fertility is caused by the fact that these females refrain from mating, that is, females are behaviorally sterile. We identified a Z‐chromosomally linked sterility locus that is most likely incompatible with yet to be identified autosomal (or cytoplasmic) factors, leading to the observed sexual abstinence. Within‐chromosome mapping revealed the sterility locus to be located in an area of strongly reduced interstrain recombination.     

The Allure of the Distinctive: Reduced Sexual Responsiveness of Female Guppies to 'Redundant' Male Colour Patterns

Frequency-dependent mating behaviour has the potential to maintain genetic variation in characteristics of organisms. The colour patterns of guppies ( Poecilia reticulata ) provide an example of one of the most extreme genetically based polymorphisms known in nature, for which frequency-dependent mate choice could be a mechanism. Numerous studies have shown that female guppies base mating preferences on male colour patterns and there is evidence that females prefer to mate with males displaying novel or unfamiliar colour patterns. This preference could lead to frequency-dependent mating success in males. Nevertheless, the possibility that female sexual responsiveness itself may depend on the frequency of male types has not been tested systematically in guppies or any other species. This study examined the sexual responses of female guppies in experimental groups consisting of two males with similar (redundant) and two males with different (unique) colour patterns. We found that female guppies were much more likely to respond sexually to the displays of unique males than to those of redundant males. Further, there was no effect of orange colouration on female responsiveness as has been documented for this population in several previous studies, thus, discrimination against redundant male types appears to have overridden directional selection based on colour pattern characteristics. This discrimination against redundant male types could in turn lead to frequency-dependent mating success in males and maintenance of colour pattern polymorphism.