Sexual conflict in wing size and shape in Drosophila melanogaster

Intralocus sexual conflict occurs when opposing selection pressures operate on loci expressed in both sexes, constraining the evolution of sexual dimorphism and displacing one or both sexes from their optimum. We eliminated intralocus conflict in Drosophila melanogaster by limiting transmission of all major chromosomes to males, thereby allowing them to win the intersexual tug‐of‐war. Here, we show that this male‐limited (ML) evolution treatment led to the evolution (in both sexes) of masculinized wing morphology, body size, growth rate, wing loading, and allometry. In addition to more male‐like size and shape, ML evolution resulted in an increase in developmental stability for males. However, females expressing ML chromosomes were less developmentally stable, suggesting that being ontogenetically more male‐like was disruptive to development. We suggest that sexual selection over size and shape of the imago may therefore explain the persistence of substantial genetic variation in these characters and the ontogenetic processes underlying them.     

Gene duplication in the evolution of sexual dimorphism

Males and females share most of the same genes, so selection in one sex will typically produce a correlated response in the other sex. Yet, the sexes have evolved to differ in a multitude of behavioral, morphological, and physiological traits. How did this sexual dimorphism evolve despite the presence of a common underlying genome? We investigated the potential role of gene duplication in the evolution of sexual dimorphism. Because duplication events provide extra genetic material, the sexes each might use this redundancy to facilitate sex‐specific gene expression, permitting the evolution of dimorphism. We investigated this hypothesis at the genome‐wide level in Drosophila melanogaster, using the presence of sex‐biased expression as a proxy for the sex‐specific specialization of gene function. We expected that if sexually antagonistic selection is a potent force acting upon individual genes, duplication will result in paralog families whose members differ in sex‐biased expression. Gene members of the same duplicate family can have different expression patterns in males versus females. In particular, duplicate pairs containing a male‐biased gene are found more frequently than expected, in agreement with previous studies. Furthermore, when the singleton ortholog is unbiased, duplication appears to allow one of the paralog copies to acquire male‐biased expression. Conversely, female‐biased expression is not common among duplicates; fewer duplicate genes are expressed in the female‐soma and ovaries than in the male‐soma and testes. Expression divergence exists more in older than in younger duplicates pairs, but expression divergence does not correlate with protein sequence divergence. Finally, genomic proximity may have an effect on whether paralogs differ in sex‐biased expression. We conclude that the data are consistent with a role of gene duplication in fostering male‐biased, but not female‐biased, gene expression, thereby aiding the evolution of sexual dimorphism.     

The devil in the details of life-history evolution: Instability and reversal of genetic correlations during selection on<Emphasis Type="Italic">Drosophila</Emphasis> development

The evolutionary relationships between three major components of Darwinian fitness, development rate, growth rate and preadult survival, were estimated using a comparison of 55 distinct populations ofDrosophila melanogaster variously selected for age-specific fertility, environmental-stress tolerance and accelerated development. Development rate displayed a strong net negative evolutionary correlation with weight at eclosion across all selection treatments, consistent with the existence of a size-versus-time tradeoff between these characters. However, within the data set, the magnitude of the evolutionary correlation depended upon the particular selection treatments contrasted. A previously proposed tradeoff between preadult viability and growth rate was apparent only under weak selection for juvenile fitness components. Direct selection for rapid development led to sharp reductions in both growth rates and viability. These data add to the mounting results from experimental evolution that illustrate the sensitivity of evolutionary correlations to (i) genotype-by-environment (G X E) interaction, (ii) complex functional-trait interactions, and (iii) character definition. Instability, disappearance and reversal of patterns of genetic covariation often occur over short evolutionary time frames and as the direct product of selection, rather than some stochastic process. We suggest that the functional architecture of fitness is a rapidly evolving matrix with reticulate properties, a matrix that we understand only poorly.     

Assessing the potential for an ongoing arms race within and between the sexes: selection and heritable variation

In promiscuous species, sexual selection generates two opposing male traits: offense (acquiring new mates and supplanting stored sperm) and defense (enforcing fidelity on one's mates and preventing sperm displacement when this fails). Coevolution between these traits requires both additive genetic variation and associated natural selection. Previous work with Drosophila melanogaster found autosomal genetic variation for these traits among inbred lines from a mixture of populations, but only nonheritable genetic variation was found within a single outbred population. These results do not support ongoing antagonistic coevolution between offense and defense, nor between either of these male traits and female reproductive characters. Here we use a new method (hemiclonal analysis) to study genomewide genetic variation in a large outbred laboratory population of D. melanogaster. Hemiclonal analysis estimates the additive genetic variation among random, genomewide haplotypes taken from a large, outbred, locally adapted laboratory population and determines the direction of the selection gradient on this variation. In contrast to earlier studies, we found low but biologically significant heritable variation for defensive and offensive offspring production as well as all their components (P1, fidelity, P2, and remating). Genetic correlations between these traits were substantially different from those reported for inbred lines. A positive genetic correlation was found between defense and offense, demonstrating that some shared genes influence both traits. In addition to this common variation, evidence for unique genetic variation for each trait was also found, supporting an ongoing coevolutionary arms race between defense and offense. Reproductive conflict between males can strongly influence female fitness. Correspondingly, we found genetic variation in both defense and offense that affected female fitness. No evidence was found for intersexual conflict in the context of male defense, but we found substantial intersexual conflict in the context of male offensive sperm competitive ability. These results indicate that conflict between competing males also promotes an associated arms race between the sexes.     

Intralocus sexual conflict and the genetic architecture of sexually dimorphic traits in Prochyliza xanthostoma (Diptera: Piophilidae)

Because homologous traits of males and females are likely to have a common genetic basis, sex-specific selection (often resulting from sexual selection on one sex) may generate an evolutionary tug-of-war known as intralocus sexual conflict, which will constrain the adaptive divergence of the sexes. Theory suggests that intralocus sexual conflict can be mitigated through reduction of the intersexual genetic correlation (rMF), predicting negative covariation between rMF and sexual dimorphism. In addition, recent work showed that selection should favor reduced expression of alleles inherited from the opposite-sex parent (intersexual inheritance) in traits subject to intralocus sexual conflict. For traits under sexual selection in males, this should be manifested either in reduced maternal heritability or, when conflict is severe, in reduced heritability through the opposite-sex parent in offspring of both sexes. However, because we do not know how far these hypothesized evolutionary responses can actually proceed, the importance of intralocus sexual conflict as a long-term constraint on adaptive evolution remains unclear. In this study, we investigated the genetic architecture of sexual and nonsexual morphological traits in Prochyliza xanthostoma. The lowest rMF and greatest dimorphism were exhibited by two sexual traits (head length and antenna length) and, among all traits, the degree of sexual dimorphism was correlated negatively with rMF. Moreover, sexual traits exhibited reduced maternal heritabilities, and the most strongly dimorphic sexual trait (antenna length) was heritable only through the same-sex parent in offspring of both sexes. Our results support theory and suggest that intralocus sexual conflict can be resolved substantially by genomic adaptation. Further work is required to identify the proximate mechanisms underlying these patterns.     

Sexual antagonism and the evolution of X chromosome inactivation

In most female mammals, one of the two X chromosomes is inactivated early in embryogenesis. Expression of most genes on this chromosome is shut down, and the inactive state is maintained throughout life in all somatic cells. It is generally believed that X-inactivation evolved as a means of achieving equal gene expression in males and females (dosage compensation). Following degeneration of genes on the Y chromosome, gene expression on X chromosomes in males and females is upregulated. This results in closer to optimal gene expression in males, but deleterious overexpression in females. In response, selection is proposed to favor inactivation of one of the X chromosomes in females, restoring optimal gene expression. Here, we make a first attempt at shedding light on this intricate process from a population genetic perspective, elucidating the sexually antagonistic selective forces involved. We derive conditions for the process to work and analyze evolutionary stability of the system. The implications of our results are discussed in the light of empirical findings and a recently proposed alternative hypothesis for the evolution of X-inactivation.     

Sexual isolation between Drosophila melanogaster females and D. simulans males: sexual maturation of males

Isofemale lines of D. simulans were examined to determine the age of sexual maturity of males with conspecific females, and for the frequency of hybridization with D. melanogaster females. Males started to mature sexually on the first day after eclosion but their ability to mate slowly increased during the following day. The estimates of both the age sexual maturation started and the switch from immature to mature males were strongly dependent on the female genotypes used in the tests. No clear differences in speed of maturation were apparent between male lines. In contrast, differences in frequency of hybridization with D. melanogaster females did occur. From the above results it is concluded that the differential hybridization success of male D. simulans lines is not related to the speed at which males mature sexually.

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Résumé Des lignées isofemelles de D. simulans ont été examinées pour déterminer l'âge de la maturité sexuelle des mâles avec des femelles conspécifiques et pour établir la fréquence de l'hybridation avec des femelles de D. melanogaster. Les mâles ont commencé à être sexuellement mûrs le premier jour après l'émergence, mais leur aptitude à la copulation a augmenté lentement pendant le jour suivant. Les estimations, tant de l'âge du début de la maturation sexuelle que de l'âge du passage de mâle immature à mâle sexuellement mûr dépendaient étroitement des génotypes des femelles utilisées dans les expériences. Il n'y avait pas de différences nettes entre les lignées de mâles. Par contre, des différences dans les fréquences d'hybridation avec les femelles de D. melanogaster ont été observées. De ces résultats, on peut conclure que les différences dans la réussite des hybridations des lignées de mâles de D. simulans n'étaient pas dues à la vitesse de maturation sexuelle des mâles.

     

The genetic architecture of sexual conflict: male harm and female resistance in Callosobruchus maculatus

Males harm females during mating in a range of species. This harm is thought to evolve because it is directly or indirectly beneficial to the male, despite being costly to his mate. The resulting sexually antagonistic selection can cause sexual arms races. For sexually antagonistic co-evolution to occur, there must be genetic variation for traits involved in female harming and susceptibility to harm, but even then intersexual genetic correlations could facilitate or impede sexual co-evolution. Male Callosobruchus maculatus harm their mates during copulation by damaging the female's reproductive tract. However, there have been no investigations of the genetic variation in damage or in female susceptibility to damage, nor has the genetic covariance between these characters been assessed. Here, we use a full-sib/half-sib breeding design to show that male damage is heritable, whereas female susceptibility to damage is much less so. There is also a substantial positive genetic correlation between the two, suggesting that selection favouring damaging males will increase the prevalence of susceptible females. We also provide evidence consistent with intralocus sexual conflict in this species.     

Transgenerational effects of sexual interactions and sexual conflict: non-sires boost the fecundity of females in the following generation

The consequences of sexual interactions extend beyond the simple production of offspring. These interactions typically entail direct effects on female fitness, but may also impact the life histories of later generations. Evaluating the cross-generational effects of sexual interactions provides insights into the dynamics of sexual selection and conflict. Such studies can elucidate whether offspring fitness optima diverge across sexes upon heightened levels of sexual interaction among parents. Here, we found that, in Drosophila melanogaster, components of reproductive success in females, but not males, were contingent on the nature of sexual interactions experienced by their mothers. In particular, maternal sexual interactions with non-sires enhanced female fecundity in the following generation. This highlights the importance of non-sire influences of sexual interactions on the expression of offspring life histories.     

Direct and correlated responses to selection for desiccation resistance: a comparison of Drosophila melanogaster and D. simulans

Replicate lines of Drosophila melanogaster and D. simulans originating from the same location in Australia were selected at two selection intensities (50%, 85% mortality) for increased resistance to desiccation, and scored for correlated responses to see if similar physiological changes were associated with the selection responses. Realized heritabilities were much higher in D. melanogaster. Selected lines of both species were more resistant than control lines to starvation and a toxic ethanol concentration. Both species also showed similar correlated responses for traits underlying the selection response: selected lines lost water at a slower rate and had reduced activity levels in a dry environment, but they did not differ in wet or dry body weight or in water content. For D. melanogaster, realized heritabilities for lines selected at 85% mortality were higher than for lines selected at 50% mortality, but there was no effect of selection intensity for D. simulans. Comparative studies of this nature may be useful in predicting the extent to which species can adapt to stress in the wild.     

The ecology of sexual conflict: ecologically dependent parallel evolution of male harm and female resistance in Drosophila melanogaster

The prevalence of sexual conflict in nature, along with the potentially stochastic nature of the resulting coevolutionary trajectories, makes it an important driver of phenotypic divergence and speciation that can operate even in the absence of environmental differences. The majority of empirical work investigating sexual conflict's role in population divergence/speciation has therefore been done in uniform environments and any role of ecology has largely been ignored. However, theory suggests that natural selection can constrain phenotypes influenced by sexual conflict. We use replicate populations of Drosophila melanogaster adapted to alternative environments to test how ecology influences the evolution of male effects on female longevity. The extent to which males reduce female longevity, as well as female resistance to such harm, both evolved in association with adaptation to the different environments. Our results demonstrate that ecology plays a central role in shaping patterns of population divergence in traits under sexual conflict.     

Sexual Isolation Between Drosophila Melanogaster, D. Simulans and D. Mauritiana: Sex and Species Specific Discrimination

The sexual isolation among the related species Drosophila melanogaster, D. simulans and D. mauritiana is asymmetrical. While D. mauritiana males mate well with both D. melanogaster and D. simulans females, females of D. mauritiana discriminate strongly against males of these two species. Similarly, D. simulans males mate with D. melanogaster females but the reciprocal cross is difficult. Interspecific crosses between several populations of the three species were performed to determine if (i) males and females of the same species share a common sexual isolation genetic system, and (ii) males (or females) use the same genetic system to discriminate against females (or males) of the other two species. Results indicate that although differences in male and female isolation depend on the populations tested, the isolation behaviour between a pair of species is highly correlated despite the variations. However, the rank order of the isolation level along the populations was not correlated in both sexes, which suggests that different genes act in male and female sexual isolation. Neither for males nor for females, the isolation behaviour of one species was paralleled in the other two species, which indicates that the genetic systems involved in this trait are species-pair specific. The implications of these results are discussed. This revised version was published online in August 2006 with corrections to the Cover Date.     

Sexual selection and the evolution of secondary sexual traits: sex comb evolution in Drosophila

Sexual selection can drive rapid evolutionary change in reproductive behaviour, morphology and physiology. This often leads to the evolution of sexual dimorphism, and continued exaggerated expression of dimorphic sexual characteristics, although a variety of other alternative selection scenarios exist. Here, we examined the evolutionary significance of a rapidly evolving, sexually dimorphic trait, sex comb tooth number, in two Drosophila species. The presence of the sex comb in both D. melanogaster and D. pseudoobscura is known to be positively related to mating success, although little is yet known about the sexually selected benefits of sex comb structure. In this study, we used experimental evolution to test the idea that enhancing or eliminating sexual selection would lead to variation in sex comb tooth number. However, the results showed no effect of either enforced monogamy or elevated promiscuity on this trait. We discuss several hypotheses to explain the lack of divergence, focussing on sexually antagonistic coevolution, stabilizing selection via species recognition and nonlinear selection. We discuss how these are important, but relatively ignored, alternatives in understanding the evolution of rapidly evolving sexually dimorphic traits.     

Sure facts, speculations, and open questions about the evolution of transposable element copy number

Transposable elements (TEs) are sequences capable of multiplying in their host's genome. They survive by increasing copy numbers due to transpositions, and natural selection washes them out because hosts with heavier loads of TEs have lower fitness. The available phylogenetic evidence supports the view that TEs have existed in living organisms for hundreds of millions of years. A fundamental question facing the field is how can an equilibrium be attained between transposition and selection which allows these parasitic genetic elements to persist for such a long time period? To answer this question, it is necessary to understand how the rate of TE transposition is controlled and to describe the mechanisms with which natural selection opposes TE accumulation. Perhaps the best models for such a study are copia and gypsy retrotransposons in Drosophila. Their average rate of transposition in nature is between 10^?5 ? 10^?4 transpositions per copy per generation. Unlike nature, transposition rates vary widely, from zero to 10^?2, between laboratory lines. This variability in transposition rate is controlled by host genes. It is probable that in nature TE site heterogeneity is caused by frequent transpositions in rare flies with permissive alleles, and no transpositions happen in the rest of flies. The average rate of TE transposition in nature may thus depend on the frequency of permissive alleles, which is a function of the rate of mutation from restrictive to permissive alleles, the mechanism and the strength of selection opposing TE multiplication, and population size. Thus, evolution of the frequency of permissive alleles of genes controlling transposition must be accounted for to understand evolution of TE copy numbers.     

Inbreeding and extinction: The effect of environmental stress and lineage

Human activities are simultaneously decreasing the size of wildlife populations (causing inbreeding) and increasing the level of stress that wildlife populations must face. Inbreeding reduces population fitness and increases extinction risk. However, very little information on the impact of stressful environments on extinction risk under inbreeding is available. We evaluated the impact of full sib inbreeding on extinction risk, using Drosophila melanogaster, in a benign and three stressful environments. The three stressful environments involved the addition to the medium of copper sulfate, methanol or alternating copper sulfate and methanol. There were 128 replicate populations for each of the four treatments. Under inbreeding, extinction rates were significantly higher in all three stressful environments compared with the benign environment. The percent extinct at generation eight (F = 0.826) for the four treatments were: 62.5% in the benign environment, 75.8%in the copper sulfate environment, 82.8% in the methanol environment, and 83.6% in the variable stress environment. However, the extinction rate in the variable stress environment did not differ significantly from the constant stress environments. Highly significant differences, among lineages, in extinction risk were detected. The results of this study indicate that wild populations are more vulnerable to inbreeding than indicated by extrapolation from captive environments.     

High Stressful Temperature and Genetic Variation of Five Quantitative Traits in Drosophila Melanogaster

Variation of five quantitative traits (thorax length, wing length, sternopleural bristle number, developmental time and larva-to-adult viability) was studied in Drosophila melanogaster reared at standard (25°C) and high stressful (32°C) temperatures using half-sib analysis. In all traits, both phenotypic and environmental variances increased at 32°C. For genetic variances, only two statistically significant differences between temperature treatments were found: the among-sire variance of viability and the among-dam variance of developmental time were higher under stress. Among-sire genetic variances and evolvabilities were generally higher at 32°C but narrow sense heritabilities were not. The results of the present work considered in the context of other studies in D. melanogaster indicate different patterns of genetic variation between stressful and nonstressful environments for the traits examined. Data on thorax length and viability agree with the hypothesis that genetic variance can be increased under extreme environmental conditions. This revised version was published online in July 2006 with corrections to the Cover Date.