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We ask if three decades and over 1 500 generations of divergent life history selection on age at reproduction has resulted in the evolution of reproductive isolation (RI) between laboratory populations of Drosophila melanogaster. We tested for premating, postmating-prezygotic and postzygotic reproductive isolation between 3 replicate population pairs. Large, evolved differences in body size between selection treatments suggested the potential for prezygotic barriers driven by sexual selection or physical incompatibilities between the sexes. Although a simple prediction would be preference for larger size, creating directional isolation, our results from individual mate choice trials indicate that populations from both selection treatments show a marked bias towards homotypic mate choice; indicative of prezygotic RI driven by sexual selection or sexual conflict. Hybridization between the focal populations resulted in the production of viable adult flies with intermediate size and developmental traits. We observed a suggestive but statistically non-significant trend of fitness decline in the F2 generation of hybrids, but no significant evidence suggesting the evolution of postmating-prezygotic or postzygotic RI. Our findings are in accord with extant literature that posits that premating RI evolves before postmating forms of RI.

We ask if three decades and over 1 500 generations of divergent life history selection on age at reproduction has resulted in the evolution of reproductive isolation (RI) between laboratory populations ofDrosophila melanogaster. We tested for premating, postmating-prezygotic and postzygotic reproductive isolation between 3 replicate population pairs. Large evolved differences in body size between selection treatments suggested the potential for prezygotic barriers driven by sexual selection or physical incompatibilities between the sexes. Although a simple prediction would be preference for larger size, creating directional isolation, our results from individual mate choice trials indicate that populations from both selection treatments show a marked bias towards homotypic mate choice; indicative of prezygotic RI driven by sexual selection or sexual conflict. Hybridization between the focal populations resulted in the production of viable adult flies with intermediate size and developmental traits. We observed a suggestive but statistically non-significant trend of fitness decline in the F2 generation of hybrids, but no significant evidence suggesting the evolution of postmating-prezygotic or postzygotic RI. Our findings are in accord with extant literature that posits that premating RI evolves before postmating forms of RI.

Intralocus sexual conflict generates a cost to mate choice: high-fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential "good genes" benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high-fitness males produced 11% more offspring compared to those mated to low-fitness males, and high-fitness females produced 34% more offspring than low-fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high-fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.

Many insects enter coma upon exposure to anoxia, a feature routinely exploited by experimentalists to handle them. But the genetic and physiological bases of anoxic coma induction and recovery are only partially understood, as are the long-term consequences for the animal's performance. We examined three populations of

Many insects enter coma upon exposure to anoxia, a feature routinely exploited by experimentalists to handle them. But the genetic and physiological bases of anoxic coma induction and recovery are only partially understood, as are the long-term consequences for the animal's performance. We examined three populations of Drosophila melanogaster (designated B) that have been inadvertently under selection for rapid recovery from CO2 exposure for nearly 40 years (around 1,000 generations) resulting from routine maintenance practices. We contrasted CO2 and N2 (presumed a less reactive gas) knockdown and recovery times of these B flies with six populations of common ancestry (A and C populations) that were not exposed to CO2 over the same period. We found that B populations showed faster and more consistent locomotor recovery than A or C populations after CO2 knockdown, a result also observed with N2 knockdown. A and C populations showed much higher variance in recovery time after CO2 exposure than after N2 exposure, suggesting gas-specific effects on pathways associated with locomotor recovery. While these selection treatments result in considerable variation in life history attributes and body size, with the characteristic intermediacy of B populations, their superiority in resistance to gas exposure and locomotor recovery suggests that it is a direct consequence of prior repeated exposure to anoxia, broadly, and CO2, specifically. Hence we describe a powerful new evolutionary model for the genetic and physiological investigation of anoxic coma in insects.

There is concern that waste waters containing manufactured metal nanoparticles (NPs) originating from consumer goods, will find their way into streams and larger water bodies. Aquatic invertebrates could be vulnerable to such pollution, and here we have used fruit flies, Drosophila melanogaster, as a model invertebrate, to test for the effect of NPs on fitness. Both copper NP and microparticle (MP)-containing medium slowed development, reduced adult longevity and decreased sperm competition. In contrast, ingestion of silver resulted in a significant reduction in developmental success only if the metal particles were nanosized. Ag NP-treatments resulted in reduced developmental success as assessed by larval and pupal survival as well as larval climbing ability, but there was no impact of silver on adult longevity and little effect on reproductive success. However, Cu NPs generally appeared to be no more toxic to this invertebrate model than the bulk counterpart. The impact of silver ingestion in larvae was further investigated by 454 pyrosequencing of the 16S rRNA genes of the midgut flora. There was a striking reduction in the diversity of the gut microbiota of Ag NP-treated larvae with a rise in the predominance of Lactobacillus brevis and a decrease in Acetobacter compared to control or Ag MP-treatment groups. Importantly, these experiments show that perturbation of the microbial assemblage within a metazoan model may contribute to Ag NP-mediated toxicity. These observations have implications for impact assessments of nanoparticles as emerging contaminants.

Intralocus sexual conflict generates a cost to mate choice: high-fitness partners transmit genetic variation that confers lower fitness to offspring of the opposite sex. Our earlier work in the fruit fly, Drosophila melanogaster, revealed that these indirect genetic costs were sufficient to reverse potential "good genes" benefits of sexual selection. However, mate choice can also confer direct fitness benefits by inducing larger numbers of progeny. Here, we consider whether direct benefits through enhanced fertility could offset the costs associated with intralocus sexual conflict in D. melanogaster. Using hemiclonal analysis, we found that females mated to high-fitness males produced 11% more offspring compared to those mated to low-fitness males, and high-fitness females produced 34% more offspring than low-fitness females. These direct benefits more than offset the reduction in offspring fitness caused by intralocus sexual conflict, creating a net fitness benefit for each sex to pairing with a high-fitness partner. Our findings highlight the need to consider both direct and indirect effects when investigating the fitness impacts of mate choice. Direct fitness benefits may shelter sexually antagonistic alleles from selection, suggesting a novel mechanism for the maintenance of fitness variation.

Adult reproductive success can account for a large fraction of male fitness, however, we know relatively little about the susceptibility of reproductive traits to mutation-accumulation (MA). Estimates of the mutational rate of decline for adult fitness and its components are controversial in Drosophila melanogaster , and post-copulatory performance has not been examined. We therefore separately measured the consequences of MA for total male reproductive success and its major pre-copulatory and post-copulatory components: mating success and sperm competitive success. We also measured juvenile viability, an important fitness component that has been well studied in MA experiments. MA had strongly deleterious effects on both male viability and adult fitness, but the latter declined at a much greater rate. Mutational pressure on total fitness is thus much greater than would be predicted by viability alone. We also noted a significant and positive correlation between all adult traits and viability in the MA lines, suggesting pleiotropy of mutational effect as required by ‘good genes’ models of sexual selection.

Earlier research by W.R. Rice showed that experimentally limiting gene expression to males in Drosophila melanogaster leads to the rapid evolution of higher fitness. Using a similar male-limited (ML) selection protocol, we confirmed that result and showed that eliminating intralocus sexual conflict results in a comprehensive remodeling of the sexually dimorphic phenotype. However, despite starting from laboratory-evolved descendants of the same founder population used in earlier work, we found no evidence for the increased performance in sperm competition or increased postmating harm to females previously demonstrated. We employed females with both ancestral population genotypes and those of the special "clone generator" females used in ML selection. Despite strong differences in sperm storage or usage patterns between these females, there was no detectable adaptation by males to the specific female stock used in the selection protocol. The lack of evolution of postcopulatory traits suggests either that requisite genetic variation was eliminated by long-term domestication of the base population, or that complex male-by-male-by-female interactions made these traits unavailable to selection. The different evolutionary outcomes produced by two very similar experiments done at different time points underscores the potential for cryptic adaptation in the laboratory to qualitatively affect inferences made using quantitative genetic methodologies.

Stronger selection on males has the potential to lower the deleterious mutation load of females, reducing the cost of sex. However, few studies have directly quantified the strength of selection for both sexes. As the magnitude of inbreeding depression (ID) is related to the strength of selection, we measured the cost of inbreeding for both males and females in a laboratory population of Drosophila melanogaster. Using a novel technique for inbreeding, we found significant ID for both juvenile viability and adult fitness in both sexes. The genetic variation responsible for this depression in fitness appeared to be recessive for adult fitness (h=0.11) and partially additive for juvenile viability (h=0.29). ID was identical across the sexes in terms of juvenile viability but was significantly more deleterious for males than females as adults, even though female X-chromosome homogamety should predispose them to a higher inbreeding load. We estimated the strength of selection on adult males to be 1.24 greater than on adult females, and this appears to be a consequence of selection arising from competition for mates. Combined with the generally positive intersexual genetic correlation for inbred lines, our results suggest that the mutation load of sexual females could be meaningfully reduced by stronger selection acting on males.

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.

Evolutionary conflict has been investigated at many levels of organization, from interactions between loci within a genome to the coevolution of species. Here we review evidence for intersexual ontogenetic conflict, a type of conflict that has received relatively little attention both theoretically and empirically. It is manifest during development when expression of the same allele, on average, moves one sex towards, and the other sex away from, its phenotypic optimum. We first introduce this type of conflict with an illustrative example and assess conditions for maintaining polymorphism for alleles underlying the conflict. We then summarize evidence from our own experiments with Drosophila melanogaster that show substantial genome-wide sexually antagonistic fitness variation. Finally we discuss evidence from other organisms and some of the ramifications of widespread polymorphism for sexually antagonistic fitness variation.

Theory predicts that intralocus sexual conflict can constrain the evolution of sexual dimorphism, preventing each sex from independently maximizing its fitness. To test this idea, we limited genome‐wide gene expression to males in four replicate Drosophila melanogaster populations, removing female‐specific selection. Over 25 generations, male fitness increased markedly, as sexually dimorphic traits evolved in the male direction. When male‐evolved genomes were expressed in females, their fitness displayed a nearly symmetrical decrease. These results suggest that intralocus conflict strongly limits sex‐specific adaptation, promoting the maintenance of genetic variation for fitness. Populations may carry a heavy genetic load as a result of selection for separate genders.

Six sister populations ofDrosophila melanogasterkept under identical environmental conditions for greater than 600 generations were reciprocally crossed to investigate the incidence of population divergence in allopatry. Population crosses directly influenced fitness, mating frequency, and sperm competition patterns. Changes in both female remating rate and the outcome of male sperm competition (P1, P2) in response to foreign males were consistent with intersexual coevolution. Moreover, seven of the 30 crosses between foreign mates resulted in significant reductions in female fitness, whereas two resulted in significant increases, compared to local matings. This tendency for foreign males to reduce female fitness may be interpreted as evidence for either sexually antagonistic coevolution or the disruption of mutualistic interactions. However, instances in which female fitness improved via cohabitation with foreign males may better reveal sexual conflict, signalling release from the cost of interacting with locally adapted males. By this metric, female reproduction inD. melanogasteris strongly constrained by local adaptation by males, a situation that would promote antagonistic coevolution between the sexes. We conclude that sexual selection can promote population differentiation in allopatry and that sexual conflict is likely to have played a role in population differentiation in this study system.

Summary In two fruit fly species, in vivo observations of competing sperm reveal how differences in sperm size, female behavior and reproductive architecture promote retention of same-species sperm. Sexual selection continues after mating and may play an important role in speciation.

Explaining the maintenance of genetic variation in characters associated with Darwinian fitness is a preoccupation of evolutionary biologists. Spatial or temporal variation in the environment can certainly promote polymorphism, yet even populations of 'model organisms', like fruit flies, kept on invariant protocols for hundreds of generations in the laboratory often show fitness variation that exceeds what would be expected from the input of new mutations alone. Such observations suggest either complexities of selection or of genetic architecture, and offer a powerful tool for the study of mechanisms that promote stable polymorphism. In this issue of Molecular Ecology, Zhang et al. (2013) report examples of nontransitivity in the outcome of postcopulatory sexual selection in the fruit fly, Drosophila, that follow the rules of the popular stalemate-breaking game roshambo - or rock, paper, scissors (RPS). The important feature of RPS is that while each strategy beats one other, it in turn is beaten by the third. Using chromosome extraction lines, the authors confirm earlier findings that the outcome of postcopulatory sexual selection via sperm competition for a male depends, in part, upon the competitor male's genotype. But taking it one step further, they demonstrate the nontransitivities between males required for circular RPS cycles in sperm competition between males, and are able to identify at least four associated loci. Because the postmating phenotype involves hundreds of potentially interacting peptides and receptors, this is an important step to understanding the persistence of variation in a critical component of male fitness.

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 of Drosophila 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.

We provide evidence from comparisons of populations of Drosophila that evolutionary correlations between longevity and stress resistance break down over the course of laboratory evolution. Using 15 distinct evolutionary regimes, we created 75 populations that were differentiated for early fecundity, longevity, starvation resistance, desiccation resistance, and developmental time. In earlier experiments, selection for postponed aging produced increases in stress resistance, whereas selection for increased stress resistance produced increases in longevity. Direct estimates of correlations also indicated an antagonistic relationship between early fecundity on one hand and longevity or stress resistance on the other. Laboratory evolution of extreme values of stress resistance, however, led to a breakdown in these evolutionary relationships. There was no evidence that these significant changes in correlation resulted from genotype-by-environment interactions or inbreeding. These findings suggest that correlations between functional characters are not necessarily durable features of a species, and that short-term evolutionary responses cannot be extrapolated reliably to longer-term evolutionary patterns.

Theory predicts that recombination will increase the effectiveness of natural selection. A Drosophila melanogaster model system was developed that increased experimental power with the use of high experimental replication, explicit tracking of individual genes, and high but natural levels of background selection. Each of 34 independent experiments traced the fate of a newly arisen mutation located within genome-wide, synthetic chromosomes that were propagated with or without recombination. An intrinsic advantage to recombination was demonstrated by the finding that the realized strength of selection on new mutations was markedly increased when recombination was present.

In many species, the Y (or W) chromosome carries relatively few functional genes. This observation motivates the null hypothesis that the Y will be a minor contributor to genetic variation for fitness. Previous data and theory supported the null hypothesis, but evidence presented here shows that the Y of Drosophila melanogaster is a major determinant of a male's total fitness, with standing genetic variation estimated to be 68% of that of an entire X/autosome genomic haplotype. Most Y-linked genes are expressed during spermatogenesis, and correspondingly, we found that the Y influences fitness primarily through its effect on a male's reproductive success (sperm competition and/or mating success) rather than his egg-to-adult viability. But the fitness of a Y highly depended on the genetic makeup of its bearer, reverting from high to low in different genetic backgrounds. This pattern leads to large epistatic (inconsistent among backgrounds) but no additive (consistent among backgrounds) Y-linked genetic variance for fitness. On a microevolutionary scale, the observed large epistatic variation on the Y substantially reduces heritable variation for fitness among males, and on a macroevolutionary scale, the Y produces strong selection for genomic rearrangements that move interacting genes onto the nonrecombining region of the Y.

We investigated physiological characters associated with water balance in laboratory populations of Drosophila melanogaster selected for resistance to desiccating conditions for over 100 generations. Five replicate, outbred, desiccation-selected (D) populations were compared with their control (C) populations. Water loss rates of female D flies were approximately 40 % lower than those of C females. Although excretory water loss was reduced in desiccation-selected flies, it comprised less than 10 % of total water loss, indicating that the D populations have evolved reduced cuticular and/or respiratory water loss rates. Total surface lipid amounts did not differ between the C and D flies. Cuticular hydrocarbons from D flies were longer than those from C flies and melted at slightly higher temperatures, possibly contributing to reduced water loss rates. Desiccation-selected flies contained approximately 30 % more bulk water than controls, as well as more glycogen. However, total metabolic water stores did not differ between the stocks owing to higher lipid levels in the C populations. The ability to tolerate water loss, as measured by water content at the time of death, did not differ between D and C flies. Thus, evolution of increased desiccation resistance has occurred by multiple physiological mechanisms, but some potential adaptive differences have not evolved.

The measurement of trade-offs may be complicated when selection exploits multiple avenues of adaptation or multiple life-cycle stages. We surveyed 10 populations of Drosophila melanogaster selected for increased resistance to starvation for 60 generations, their paired controls, and their mutual ancestors (a total of 30 outbred populations) for evidence of physiological and life-history trade-offs that span life-cycle stages. The directly selected lines showed an impressive response to starvation selection, with mature adult females resisting starvation death 4-6 times longer than unselected controls or ancestors-up to a maximum of almost 20 days. Starvation-selected flies are already 80% more resistant to starvation death than their controls immediately upon eclosion, suggesting that a significant portion of their selection response was owing to preadult growth and acquisition of metabolites relevant to the stress. These same lines exhibited significantly longer development and lower viability in the larval and pupal stages. Weight and lipid measurements on one of the starvation-selected treatments (SB1-5), its control populations (CB1_5), and their ancestor populations (B1_5) revealed three important findings. First, starvation resistance and lipid content were linearly correlated; second, larval lipid acquisition played a major role in the evolution of adult starvation resistance; finally, increased larval growth rate and lipid acquisition had a fitness cost exacted in reduced viability and slower development. This study implicates multiple life-cycle stages in the response to selection for the stress resistance of only one stage. Our starvation-selected populations illustrate a case that may be common in nature. Patterns of genetic correlation may prove misleading unless multiple pleiotropic interconnections are resolved.

Sexually dimorphic traits are likely to have evolved through sexually antagonistic selection. However, recent empirical data suggest that intralocus sexual conflict often persists, even when traits have diverged between males and females. This implies that evolved dimorphism is often incomplete in resolving intralocus conflict, providing a mechanism for the maintenance of genetic variance in fitness-related traits. We used experimental evolution in Drosophila melanogaster to directly test for ongoing conflict over a suite of sexually dimorphic cuticular hydrocarbons (CHCs) that are likely targets of sex-specific selection. Using a set of experimental populations in which the transmission of genetic material had been restricted to males for 82 generations, we show that CHCs did not evolve, providing experimental evidence for the absence of current intralocus sexual conflict over these traits. The absence of ongoing conflict could indicate that CHCs have never been the target of sexually antagonistic selection, although this would require the existing dimorphism to have evolved via completely sexlinked mutations or as a result of former, but now absent, pleiotropic effects of the underlying loci on another trait under sexually antagonistic selection. An alternative interpretation, and which we believe to be more likely, is that the extensive CHC sexual dimorphism is the result of past intralocus sexual conflict that has been fully resolved, implying that these traits have evolved genetic independence between the sexes and that genetic variation in them is therefore maintained by alternative mechanisms. This latter interpretation is consistent with the known roles of CHCs in sexual communication in this species and with previous studies suggesting the genetic independence of CHCs between males and females. Nevertheless, direct estimates of sexually antagonistic selection will be important to fully resolve these alternatives.

Trade-offs among life-history traits are often thought to constrain the evolution of populations. Here we report the disappearance of a trade-off between early fecundity on the one hand, and late-life fecundity, starvation resistance, and longevity on the other, over 10 yr of laboratory selection for late-life reproduction. Whereas the selected populations showed an initial depression in early-life fecundity, they later converged upon the controls and then surpassed them. The evolutionary loss of the trade-off among life-history traits is considered attributable to the following factors: (1) the existence of differences in the culture regimes of the short- and long- generation populations other than the demographic differences deliberately imposed; (2) adaptation of one or both of these sets of populations to the unique aspects of their culture regimes; (3) the existence of an among-environment trade-off in the expression of early fecundity in the two culture regimes, as reflected in assays that mimic those regimes. The trade-off between early and late-life reproductive success, as manifest among divergently selected populations, is apparent or not de- pending on the assay environment. This demonstration that strong genotype-by-environment interactions can obscure a fundamental trade-off points to the importance of controlling all aspects of the culture regime of experimental populations and the difficulty of doing so even in the labo- ratory.

Sex chromosomes differ from other chromosomes in the striking divergence they often show in size, structure, and gene content. Not only do they possess genes controlling sex determination that are restricted to either the X or Y (or Z or W) chromosomes, but in many taxa they also include recombining regions. In these ‘pseudoautosomal regions' (PARs), sequence homology is maintained by meiotic pairing and exchange in the heterogametic sex. PARs are unique genomic regions, exhibiting some features of autosomes, but they are also influenced by their partial sex linkage. Here we review the distribution and structure of PARs among animals and plants, the theoretical predictions concerning their evolutionary dynamics, the reasons for their persistence, and the diversity and content of genes that reside within them. It is now clear that the evolution of the PAR differs in important ways from that of genes in either the non-recombining regions of sex chromosomes or the autosomes.

Intralocus sexual conflict occurs when males and females experience sex-specific selection on a shared genome. With several notable exceptions, intralocus sexual conflict has been investigated in constant environments to which the study organisms have had an opportunity to adapt. However, a change in the environment can result in differential or even opposing selection pressures on males and females, creating sexual conflict. We used experimental evolution to explore the interaction between intralocus sexual conflict, sexual dimorphism and environmental variation in Drosophila melanogaster. Six populations were selected for adult desiccation resistance (D), with six matched control populations maintained in parallel (C). After 46 generations, the D populations had increased in survival time under arid conditions by 68% and in body weight by 20% compared to the C populations. The increase in size was the result of both extended development and faster growth rate of D juveniles. Adaptation to the stress came at a cost in terms of preadult viability and female fecundity. Because males are innately less tolerant of desiccation stress, very few D males survived desiccation-selection; while potentially a windfall for survivors, these conditions mean that most males’ fitness was determined posthumously. We conjectured that selection for early maturation and mating in males was in conflict with selection for survival and later reproduction in females. Consistent with this prediction, the sexes showed different patterns of age-specific desiccation resistance and resource acquisition, and there was a trend towards increasingly female-biased sexual size dimorphism. However, levels of desiccation resistance were unaffected, with D males and females increasing in parallel. Either there is a strong positive genetic correlation between the sexes that limits independent evolution of desiccation resistance, or fitness pay-offs from the strategy of riding out the stress bout are great enough to sustain concordant selection on the two sexes. We discuss the forces that mould fitness in males under a regimen where trade-offs between survival and reproduction may be considerable.

Background: Intralocus sexual conflict can inhibit the evolution of each sex towards its own fitness optimum. In a previous study, we confirmed this prediction through the experimental removal of female selection pressures in Drosophila melanogaster, achieved by limiting the expression of all major chromosomes to males. Compared to the control populations (C1-4) where the genomes are exposed to selection in both sexes, the populations with male-limited genomes (ML1-4) showed rapid increases in male fitness, whereas the fitness of females expressing ML-evolved chromosomes decreased [1]. Methodology/Principal Findings: Here we examine the behavioural phenotype underlying this sexual antagonism. We show that males expressing the ML genomes have a reduced courtship level but acquire the same number of matings. On the other hand, our data suggest that females expressing the ML genomes had reduced attractiveness, stimulating a lower rate of courtship from males. Moreover, females expressing ML genomes tend to display reduced yeast-feeding behaviour, which is probably linked to the reduction of their fecundity. Conclusion/Significance: These results suggest that reproductive behaviour is shaped by opposing selection on males and females, and that loci influencing attractiveness and foraging were polymorphic for alleles with sexually antagonistic expression patterns prior to ML selection. Hence, intralocus sexual conflict appears to play a role in the evolution of a wide range of fitness-related traits and may be a powerful mechanism for the maintenance of genetic variation in fitness.

This chapter discusses the relationship between sexual conflict and sexual dimorphism. It presents evidence that intralocus sexual conflict is a widespread and potentially important contributor to several basic evolutionary phenomena, including the evolution of sexual dimorphism. Accumulating evidence suggests that intralocus sexual conflict creates a significant gender load in populations, reducing fitness in both sexes and preventing or slowing attainment of sex-specific optimal trait values. The chapter argues that the complexities of tuning individual gene expression to each sex separately explain why sexual dimorphism usually produces intergradation between the sexes, and why there is so much diversity in sexual form, function, and preference. However, in spite of these important effects, intralocus sexual conflict is expected to be difficult to detect and quantify. The chapter discusses these problems and presents prospects for future research directions.

Two recent studies provide provocative experimental findings about the potential influence of kin recognition and cooperation on the level of sexual conflict inDrosophila melanogaster. In both studies, male fruit flies apparently curbed their mate-harming behaviours in the presence of a few familiar or related males, suggesting some form of cooperation mediated by kin selection. In one study, the reduction in agonistic behaviour by brothers apparently rendered them vulnerable to dramatic loss of paternity share when competing with an unrelated male. If these results are robust and generalizable, fruit flies could be a major new focus for the experimental study of kin selection and social evolution. In our opinion, however, the restrictive conditions required for male cooperation to be adaptive in this species make it unlikely to evolve. We investigated these phenomena in two different populations ofD. melanogasterusing protocols very similar to those in the two previous studies. Our experiments show no evidence for a reduction in mate harm based upon either relatedness or familiarity between males, and no reduction in male reproductive success when two brothers are in the presence of an unfamiliar, unrelated, ‘foreign’ male. Thus, the reduction of sexual conflict owing to male cooperation does not appear to be a general feature of the species, at least under domestication, and these contrasting results call for further investigation: in new populations, in the field and in the laboratory populations in which these phenomena have been reported.

Evolution based on the benefits of acquiring “good genes” in sexual selection is only plausible with the reliable transmission of genetic quality from one generation to the next. Accumulating evidence suggests that sexually antagonistic (SA) genes with opposite effects on Darwinian fitness when expressed in the two different sexes may be common in animals and plants. These SA genes should weaken the potential indirect genetic benefits of sexual selection by reducing the fitness of opposite-sex progeny from high-fitness parents. Here we use hemiclonal analysis in the fruit fly, Drosophila melanogaster, to directly measure the inheritance of fitness across generations, over the entire genome. We show that any potential genetic benefits of sexual selection in this system are not merely weakened, but completely reversed over one generation because high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons. Moreover, male fitness was not inherited by sons, consistent with both theory and recent evidence connecting this form of SA variation with the X chromosome. This inheritance pattern may help to explain how genetic variation for fitness is sustained despite strong sexual selection, and why the ZW sex chromosome system found in birds and butterflies appears to foster the evolution of extreme secondary sexual characters in males., Hemiclonal analysis ofDrosophila melanogaster reveals that high-fitness males produce low-fitness daughters and high-fitness mothers produce low-fitness sons, with implications for models of sexual selection.

A wild-type population of Drosophila melanogaster was used to assess the impact of a known deleterious mutation, nub(1), when it had (1) evolved for up to 180 generations with the mutation or (2) recently had the same mutant allele introgressed into it. Relative to this benchmark, we observed much stronger initial fitness depression in males (-74%) than in females (-38%) and also relatively greater fitness recovery by evolved males (+55%) than females (+17%). Experimental assays revealed amelioration in both juvenile and adult fitness and suggested that the greater relative recovery of male fitness was from gains through sexual selection. These evolutionary changes in male fertility depended on pairing with their coevolved mates for both mate choice and post-copulatory components of sexual selection. Without replication at the population level, these results are used to motivate a general hypothesis rather than definitively test it: Differences in reproductive optima may generally skew mutational effects towards the more strongly sexually-selected sex due to genic capture and condition dependence.

One of the enduring temptations of evolutionary theory is the extrapolation from short-term to long-term, from a few species to all species. Unfortunately, the study of experimental evolution reveals that extrapolation from local to general patterns of evolution is not usually successful. The present article supports this conclusion using evidence from the experimental evolution of life-history in Drosophila. The following factors demonstrably undermine evolutionary correlations between functional characters: inbreeding, genotype-by-environment interaction, novel foci of selection, long-term selection, and alternative genetic backgrounds. The virtual certainty that at least one of these factors will arise during evolution shreds the prospects for global theories of the effects of adaptation. The effects of evolution apparently don't generalize, even though evolution is a global process.

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a 'gender-load' in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.

Sexually antagonistic alleles are selected discordantly between the sexes. Experimental evidence indicates that sexually antagonistic fitness variation is abundant in the genome of Drosophila melanogaster. Theory predicts that the X chromosome will be enriched with this type of variation. To test this prediction in D. melanogaster, we sampled, and cytogenetically cloned, 20 X chromosomes and compared their fitness variation to genome-wide levels. At the juvenile stage, in which gender roles are most similar, the X chromosome made no detectable contribution to genome-wide fitness variation. At the adult stage, in which gender roles diverge, the X chromosome was estimated to harbour 45% of the genome-wide fitness variation and 97% of the genome-wide sexually antagonistic variation. This genomic structure has important implications for the process of sexual selection because X-linked sexually antagonistic variation contributes to negative intersexual heritability for fitness, i.e. high-fitness males (females) produce, on average, low-fitness daughters (sons).

A new hypothesis is proposed for the rapid evolution of postzygotic reproductive isolation via hybrid infertility. The hypothesis is motivated by two lines of experimental research from Drosophila melanogaster that demonstrate that sexually antagonistic fitness variation is abundant and that epistatic fitness variation on the Y chromosome is common. The hypothesis states that the expression of sexually antagonistic genes leads to a ‘gender-load’ in each sex. In response, gender-limited reproductive genes are selected to ameliorate, through pleiotropy, the expression of sexually antagonistic genes. Chronic coevolution between gender-limited genes and gender-unlimited sexually antagonistic genes causes rapid divergence of reproductive proteins among allopatric populations, ultimately leading to hybrid infertility.

Because of their distinctive roles in reproduction, females and males are selected toward different optimal phenotypes. Ontogenetic conflict between the sexes arises when homologous traits are selected in different directions. The evolution of sexual dimorphism by sex-limited gene expression alleviates this problem. However, because the majority of genes are not sex-limited, the potential for substantial conflict may remain. Here we assess the degree of ontogenetic conflict in the fruit-fly, Drosophila melanogaster, by cloning 40 haploid genomes and measuring their Darwinian fitness in both sexes. The intersexual genetic correlations for juvenile viability, adult reproductive success, and total fitness were used to gauge potential conflict during development. First, as juveniles, where the fitness objectives of the two sexes appear to be similar, survival was strongly positively correlated across sexes. Second, after adult maturation, where gender roles diverge, a significant negative correlation for reproductive success was found. Finally, because of counterbalancing correlations in the juvenile and adult components, no intersexual correlation for total fitness was found. Highly significant genotype-by-gender interaction variance was measured for both adult and total fitness. These results demonstrate strong intersexual discord during development because of the expression of sexually antagonistic variation.

We have examined starvation and desiccation resistance in 43 outbred populations of Drosophila melanogaster that have diverged from a common ancestral population as a result of a variety of defined selection protocols. The populations differ up to 8.5-fold in desiccation resistance and up to 10-fold in starvation resistance. We used these populations to search for evolved physiological changes that might explain the differences in stress resistance. We examined two hypotheses for increased stress resistance that had been proposed previously in the literature: (1) that increments in starvation resistance are principally the result of differential lipid accumulation, and (2) that changes in glycogen accumulation play a role in evolved increases in resistance to desiccation stress. By quantifying desiccation resistance, starvation resistance, lipid content, and carbohydrate content in each of our populations of flies, we were able to demonstrate strong correlations between the capacity of the flies to resist starvation and the quantity of lipid or carbohydrate that the flies had stored. The strongest correlation (R2 = 0.99) was observed when the total energy content of both the lipid and carbohydrate stores was regressed against starvation resistance. These results demonstrate that the flies responded to selection for starvation resistance through a genetically determined increase in both lipid and carbohydrate storage. Similar analyses of the correlation between lipid storage or total energy storage and desiccation resistance revealed no significant correlations. Carbohydrate storage was significantly correlated with desiccation resistance in female but not in male flies. These results suggest that different forms of stress are resisted with distinct physiological mechanisms and that the evolutionary response of the flies to stress selection is specific to the stress imposed.