Past and present resource availability affect mating rate but not mate choice in Drosophila melanogaster.

The choices of when, where, and with whom to mate represent some of the most important decisions an individual can make to increase their fitness. Several studies have shown that the resources available to an individual during development can dramatically alter their mating rate later in life, and even the choice of mate. However, an individual's surroundings and available resources can change rapidly, and it is not clear how quickly the redistribution of resources towards reproduction can change. To address this important question, we measured mating rate and mate choice among Drosophila melanogaster males that were manipulated in terms of both past resources (control vs. starvation) and the resources available during mate choice (food vs. no food). We found that males given access to ample resources prior to mate choice showed higher mating rates than those that were starved, in agreement with previous studies. However, we also found that this effect can be reversed quickly, as starved males given the opportunity to mate in a high-quality environment mated at frequencies equivalent to their fed counterparts. Although past and present resources affected mating rate, they did not affect mate choice, as males mated with high-quality females at high frequencies regardless of their condition and environment. Our results show that both current condition as well as the promise of future resources can dramatically influence individuals' investment into reproduction and that such mating decisions are extremely plastic and reliant on environmental cues.

Female Life-History Trade-Offs and the Maintenance of Genetic Variation in Drosophila melanogaster.

Why do we observe substantial variation in fitness-related traits under strong natural or sexual selection? While there is support for several selective and neutral mechanisms acting in select systems, we lack a comprehensive analysis of the relative importance of various mechanisms within a single system. Furthermore, while sexually selected male traits have been a central focus of this paradox, female sexual traits have rarely been considered. In this study, I evaluate the contribution of various selective mechanisms to the maintenance of substantial variation in female attractiveness and offspring production observed among Drosophila melanogaster genotypes. I tested for contributions from antagonistic pleiotropy, frequency-dependent selection, changing environments, and sexual conflict. I found negative genetic correlations between some traits (male attractiveness vs. female resistance to male harm, early-life offspring production vs. reproductive senescence) and genotype-specific changes in fitness between environments. However, no measurement found strong trade-offs among the fitness components of these genotypes. Overall, I find little evidence that any one mechanism is strong enough to maintain genetic variation on its own. Instead, I suggest that many mechanisms may weaken the selection among genotypes, which would collectively allow neutral processes such as mutation-selection balance to maintain genetic variation within populations.

Environmental stress does not increase the mean strength of selection.

A common intuition among evolutionary biologists and ecologists is that environmental stress will increase the strength of selection against deleterious alleles and among alternate genotypes. However, the strength of selection is determined by the relative fitness differences among genotypes, and there is no theoretical reason why these differences should be exaggerated as mean fitness decreases. We update a recent review of the empirical results pertaining to environmental stress and the strength of selection and find that there is no overall trend towards increased selection under stress, in agreement with other recent analyses of existing data. The majority of past studies measure the strength of selection by quantifying the decrease in fitness imposed by single or multiple mutations in different environments. However, selection rarely acts on one locus independently, and the strength of selection will be determined by variation across the whole genome. We used 20 inbred lines of Drosophila melanogaster to make repeated fitness measurements of the same genotypes in four different environments. This framework allowed us to determine the variation in fitness attributable to genotype across stressful environments and to calculate the opportunity for selection among these genotypes in each stress. Although we found significant decreases in mean fitness in our stressful environments, we did not find any significant differences in the strength of selection among any of the four measured environments. Therefore, in agreement with our updated review, we find no evidence for the oft-cited verbal model that stress increases the strength of selection.

Tissue-specific insulin signaling mediates female sexual attractiveness.

Individuals choose their mates so as to maximize reproductive success, and one important component of this choice is assessment of traits reflecting mate quality. Little is known about why specific traits are used for mate quality assessment nor about how they reflect it. We have previously shown that global manipulation of insulin signaling, a nutrient-sensing pathway governing investment in survival versus reproduction, affects female sexual attractiveness in the fruit fly, Drosophila melanogaster. Here we demonstrate that these effects on attractiveness derive from insulin signaling in the fat body and ovarian follicle cells, whose signals are integrated by pheromone-producing cells called oenocytes. Functional ovaries were required for global insulin signaling effects on attractiveness, and manipulations of insulin signaling specifically in late follicle cells recapitulated effects of global manipulations. Interestingly, modulation of insulin signaling in the fat body produced opposite effects on attractiveness, suggesting a competitive relationship with the ovary. Furthermore, all investigated tissue-specific insulin signaling manipulations that changed attractiveness also changed fecundity in the corresponding direction, pointing to insulin pathway activity as a reliable link between fecundity and attractiveness cues. The cues themselves, cuticular hydrocarbons, responded distinctly to fat body and follicle cell manipulations, indicating independent readouts of the pathway activity from these two tissues. Thus, here we describe a system in which female attractiveness results from an apparent connection between attractiveness cues and an organismal state of high fecundity, both of which are created by lowered insulin signaling in the fat body and increased insulin signaling in late follicle cells.

Mate choice in fruit flies is rational and adaptive.

According to rational choice theory, beneficial preferences should lead individuals to sort available options into linear, transitive hierarchies, although the extent to which non-human animals behave rationally is unclear. Here we demonstrate that mate choice in the fruit fly Drosophila melanogaster results in the linear sorting of a set of diverse isogenic female lines, unambiguously demonstrating the hallmark of rational behaviour, transitivity. These rational choices are associated with direct benefits, enabling males to maximize offspring production. Furthermore, we demonstrate that female behaviours and cues act redundantly in mate detection and assessment, as rational mate choice largely persists when visual or chemical sensory modalities are impaired, but not when both are impaired. Transitivity in mate choice demonstrates that the quality of potential mates varies significantly among genotypes, and that males and females behave in such a way as to facilitate adaptive mate choice.

Female Stick Insects Mate Multiply to Find Compatible Mates.

Why females of many species mate multiply in the absence of direct benefits remains an open question in evolutionary ecology. Interacting and mating with multiple males can be costly to females in terms of time, resources, predation risk, and disease transmission. A number of indirect genetic benefits have been proposed to explain such behaviors, but the relative importance of these mechanisms in natural systems remains unclear. We tested for several direct and indirect benefits of polyandry in the walking stick Timema cristinae. We found no evidence of direct benefits with respect to longevity or fecundity. However, male × female genotypic interactions affected egg-hatching success and offspring production independent of relatedness, suggesting that mating with certain males benefits females and that the best male may differ for each female. Furthermore, multiply mated females biased paternity toward one or few males, and the extent of this bias was positively correlated to egg-hatching success. Our data, therefore, provide evidence for indirect benefits through compatibility effects in this species. By mating multiply, females may improve their chances of mating with a compatible male if compatibility cannot be assessed before mating. Such compatibility effects can explain the evolution and maintenance of polyandry in Timema and many other species.

Differential effects of genetic vs. environmental quality in Drosophila melanogaster suggest multiple forms of condition dependence.

Condition is a central concept in evolutionary ecology, but the roles of genetic and environmental quality in condition-dependent trait expression remain poorly understood. Theory suggests that condition integrates genetic, epigenetic and somatic factors, and therefore predicts alignment between the phenotypic effects of genetic and environmental quality. To test this key prediction, we manipulated both genetic (mutational) and environmental (dietary) quality in Drosophila melanogaster and examined responses in morphological and chemical (cuticular hydrocarbon, CHC) traits in both sexes. While the phenotypic effects of diet were consistent among genotypes, effects of mutation load varied in magnitude and direction. Average effects of diet and mutation were aligned for most morphological traits, but non-aligned for the male sexcombs and CHCs in both sexes. Our results suggest the existence of distinct forms of condition dependence, one integrating both genetic and environmental effects and the other purely environmental. We propose a model to account for these observations.

Remating and sperm competition in replicate populations of Drosophila melanogaster adapted to alternative environments.

The prevalence of sexual conflict in nature, as well as the supposedly arbitrary direction of the resulting coevolutionary trajectories, suggests that it may be an important driver of phenotypic divergence even in a constant environment. However, natural selection has long been central to the operation of sexual conflict within populations and may therefore constrain or otherwise direct divergence among populations. Ecological context may therefore matter with respect to the diversification of traits involved in sexual conflict, and if natural selection is sufficiently strong, such traits may evolve in correlation with environment, generating a pattern of ecologically-dependent parallel evolution. In this study we assess among-population divergence both within and between environments for several traits involved in sexual conflict. Using eight replicate populations of Drosophila melanogaster from a long-term evolution experiment, we measured remating rates and subsequent offspring production of females when housed with two separate males in sequence. We found no evidence of any variation in male reproductive traits (offense or defense). However, the propensity of females to remate diverged significantly among the eight populations with no evidence of any environmental effect, consistent with sexual conflict promoting diversification even in the absence of ecological differences. On the other hand, females adapted to one environment (ethanol) tended to produce a higher proportion of offspring sired by their first mate as compared to those adapted to the other (cadmium) environment, suggesting ecologically-based divergence of this conflict phenotype. Because we find evidence for both stochastic population divergence operating outside of an ecological context and environment-dependent divergence of traits under sexual conflict, the interaction of these two processes is an important topic for future work.

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.

Hydrocarbon divergence and reproductive isolation in Timema stick insects.

BACKGROUND: Individuals commonly prefer certain trait values over others when choosing their mates. If such preferences diverge between populations, they can generate behavioral reproductive isolation and thereby contribute to speciation. Reproductive isolation in insects often involves chemical communication, and cuticular hydrocarbons, in particular, serve as mate recognition signals in many species. We combined data on female cuticular hydrocarbons, interspecific mating propensity, and phylogenetics to evaluate the role of cuticular hydrocarbons in diversification of Timema walking-sticks. RESULTS: Hydrocarbon profiles differed substantially among the nine analyzed species, as well as between partially reproductively-isolated T. cristinae populations adapted to different host plants. In no-choice trials, mating was more likely between species with similar than divergent hydrocarbon profiles, even after correcting for genetic divergences. The macroevolution of hydrocarbon profiles, along a Timema species phylogeny, fits best with a punctuated model of phenotypic change concentrated around speciation events, consistent with change driven by selection during the evolution of reproductive isolation. CONCLUSION: Altogether, our data indicate that cuticular hydrocarbon profiles vary among Timema species and populations, and that most evolutionary change in hydrocarbon profiles occurs in association with speciation events. Similarities in hydrocarbon profiles between species are correlated with interspecific mating propensities, suggesting a role for cuticular hydrocarbon profiles in mate choice and speciation in the genus Timema.

Sexual selection is ineffectual or inhibits the purging of deleterious mutations in Drosophila melanogaster.

The effects of sexual selection on population mean fitness are unclear and a subject of debate. Recent models propose that, because reproductive success may be condition dependent, much of the genome may be a target of sexual selection. Under this scenario, mutations that reduce health, and thus nonsexual fitness, may also be deleterious with respect to reproductive success, meaning that sexual selection may contribute to the purging of deleterious alleles. We tested this hypothesis directly by subjecting replicate Drosophila melanogaster populations to two treatments that altered the opportunity for sexual selection and then tracked changes in the frequency of six separate deleterious alleles with recessive and visible phenotypic effects. While natural selection acted to decrease the frequency of all six mutations, the addition of sexual selection did not aid in the purging of any of them, and for three of them appears to have hampered it. Courtship and mating have harmful effects in this species and mate choice assays showed that males directed more courtship and mating behavior toward wild-type over mutant females, providing a likely explanation for sexual selection's cost. Whether this cost extends to other mutations (e.g., those lacking visible phenotypic effects) is an important topic for future research.