Alison Pischedda

Intralocus Sexual Conflict Diminishes the Benefits of Sexual Selection

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.

Partitioning sexual selection into its mating success and fertilization success components

Postcopulatory sexual selection due to sperm competition and/or cryptic female choice has been documented in a diversity of taxonomic groups and is considered a pivotal component of sexual selection. Despite this apparent importance, the relative contribution of postcopulatory fertilization success to overall sexual selection has not yet been measured in any species. Here, we used a laboratory-adapted population of the promiscuous fruit fly Drosophila melanogaster to partition the variance in male reproductive success into mating success (a major component of precopulatory sexual selection) and fertilization success (a major component of postcopulatory sexual selection). We found that fertilization success contributed nearly as strongly as mating success to a males net performance in sexual selection, but that most of this postcopulatory component was attributable to variation in male mating order (the tendency to be the last male to mate a female). After adjusting for mating order, only ≈2% of the residual variation in male reproductive success was attributable to differential fertilization success. We found no correlation between male mating success and fertilization success in this system. Unlike natural populations of Drosophila, our laboratory population is adapted to a semelparous lifecycle, so our findings will be most applicable to other promiscuous species with strong sperm precedence and one short breeding period per year or lifetime. In these species, fertilization success may have as much influence on male reproductive success as mating success, but the timing of mating (mating order) may be the predominant factor contributing to variation in fertilization success.

Resolving Intralocus Sexual Conflict: Genetic Mechanisms and Time Frame

Intralocus sexual conflict occurs due to the expression of sexually antagonistic alleles: those that increase fitness when expressed in one sex but decrease fitness when expressed in the other sex. This genetic conflict is expected whenever the sexes are selected toward differing phenotypic optima for a trait that has a positive genetic correlation between the sexes. Here we synthesize recent developments in the areas of genomics, microarray analysis, and developmental and molecular genetics to establish feasible mechanisms by which the intersexual genetic correlation can be reduced, as well as the time course over which conflict resolution is expected to evolve.

The timing of mating influences reproductive success in Drosophila melanogaster: implications for sexual conflict

Despite its potential importance, the role of the timing of mating(s) as a source of variation in female lifetime reproductive success has been largely overlooked. Here, using a laboratory‐adapted population of the model species Drosophila melanogaster, we explore how temporal variation in the patterns of single and multiple matings influences female fecundity. We find that the boost to fecundity known to occur after a virgin female’s initial mating also extends to subsequent matings as nonvirgins, but only for a short duration. This fecundity boost at least partially offsets the direct costs of multiple matings to females in this population of D. melanogaster. The implications of these results for our understanding of the evolution and maintenance of polyandry in this species are discussed in the context of sexual conflict.

Do female Drosophila melanogaster adaptively bias offspring sex ratios in relation to the age of their mate

Modification of offspring sex ratios in response to parental quality is predicted when the long-term fitness returns of sons and daughters differ. One factor that may influence a mothers sex allocation decision is the quality (or attractiveness) of her mate. We investigated whether the sex ratios of offspring produced by female Drosophila melanogaster are biased with respect to the age of the males to which they are mated, and whether there is an adaptive basis for this phenomenon. We found that females mated to old males (13 d post-eclosion) initially produced a greater proportion of daughters than did females mated to young males (1 d post-eclosion). This pattern does not appear to be due to a systematic difference in the numbers or mortality of the X- and Y-bearing sperm originating from old and young fathers, as the overall sex ratios of all offspring produced from a single copulation did not differ between broods fathered by the two types of males. The sons of older males fared worse in competitive mating assays than did the sons of younger males, while daughters of old and young males were of comparable fitness. These results suggest that there is an adaptive basis for the observed sex ratio modification.

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the males population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.

Remating in Drosophila melanogaster: are indirect benefits condition dependent?

By measuring the direct and indirect fitness costs and benefits of sexual interactions, the feasibility of alternate explanations for polyandry can be experimentally assessed. This approach becomes more complicated when the relative magnitude of the costs and/or benefits associated with multiple mating (i.e., remating with different males) vary with female condition, as this may influence the strength and direction of sexual selection. Here, using the model organism Drosophila melanogaster, we test whether the indirect benefits that a nonvirgin female gains by remating (“trading‐up”) are influenced by her condition (body size). We found that remating by small‐bodied, low‐fecundity females resulted in the production of daughters of relatively higher fecundity, whereas the opposite pattern was observed for large‐bodied females. In contrast, remating had no measurable effect on the relative reproductive success of sons from dams of either body size. These results are consistent with a hypothesis based on sexually antagonistic genetic variation. The implications of these results to our understanding of the evolution and consequences of polyandry are discussed.

Natural Variation in the Strength and Direction of Male Mating Preferences for Female Pheromones in Drosophila melanogaster

Many animal species communicate using chemical signals. In Drosophila, cuticular hydrocarbons (CHCs) are involved in species and sexual identification, and have long been thought to act as stimulatory pheromones as well. However, a previous study reported that D. melanogaster males were more attracted to females that were lacking CHCs. This surprising result is consistent with several evolutionary hypotheses but is at odds with other work demonstrating that female CHCs are attractive to males. Here, we investigated natural variation in male preferences for female pheromones using transgenic flies that cannot produce CHCs. By perfuming females with CHCs and performing mate choice tests, we found that some male genotypes prefer females with pheromones, some have no apparent preference, and at least one male genotype prefers females without pheromones. This variation provides an excellent opportunity to further investigate the mechanistic causes and evolutionary implications of divergent pheromone preferences in D. melanogaster males.

Male × Female Interaction for a Pre-Copulatory Trait, but Not a Post-Copulatory Trait, among Cosmopolitan Populations of Drosophila melanogaster

Sexual coevolution occurs when changes in the phenotype of one sex select for changes in the other sex. We can identify the “footprint” of this coevolution by mating males and females from different populations and testing for a male-female genotype interaction for a trait associated with male (or female) performance. Here we mated male Drosophila melanogaster from five different continents with females from their own and different continents to test for a male-female interaction for mating speed, a pre-copulatory trait, and female reproductive investment, a post-copulatory trait. We found a strong male-female interaction for mating speed, consistent with previous studies using different populations, suggesting that the potential for sexual coevolution for this trait is present in this species. In contrast, we did not detect a male-female interaction for female reproductive investment. Although a male-female interaction for mating speed is compatible with the hypothesis of ongoing sexual coevolution, the nature of our experimental design is unable to exclude alternate explanations. Thus, the evolutionary mechanisms promoting male-female genotype interactions for pre-copulatory mating traits in D. melanogaster warrant further investigation.

Sexual selection has minimal impact on effective population sizes in species with high rates of random offspring mortality: An empirical demonstration using fitness distributions.

The effective population size (Ne) is a fundamental parameter in population genetics that influences the rate of loss of genetic diversity. Sexual selection has the potential to reduce Ne by causing the sex‐specific distributions of individuals that successfully reproduce to diverge. To empirically estimate the effect of sexual selection on Ne, we obtained fitness distributions for males and females from an outbred, laboratory‐adapted population of Drosophila melanogaster. We observed strong sexual selection in this population (the variance in male reproductive success was ∼14 times higher than that for females), but found that sexual selection had only a modest effect on Ne, which was 75% of the census size. This occurs because the substantial random offspring mortality in this population diminishes the effects of sexual selection on Ne, a result that necessarily applies to other high fecundity species. The inclusion of this random offspring mortality creates a scaling effect that reduces the variance/mean ratios for male and female reproductive success and causes them to converge. Our results demonstrate that measuring reproductive success without considering offspring mortality can underestimate Ne and overestimate the genetic consequences of sexual selection. Similarly, comparing genetic diversity among different genomic components may fail to detect strong sexual selection.