Dominic A. Edward

The evolution and significance of male mate choice

The distinct reproductive roles of males and females, which for many years were characterised in terms of competitive males and choosy females, have remained a central focus of sexual selection since Darwins time. Increasing evidence now shows that males can be choosy too, even in apparently unexpected situations, such as under polygyny or in the absence of male parental care. Here, we provide a synthesis of the theory on male mate choice and examine the factors that promote or constrain its evolution. We also discuss the evolutionary significance of male mate choice and the contrasts in male versus female mate choice. We conclude that mate choice by males is potentially widespread and has a distinct role in how mating systems evolve.

Adaptations to sexual selection and sexual conflict: insights from experimental evolution and artificial selection

Artificial selection and experimental evolution document natural selection under controlled conditions. Collectively, these techniques are continuing to provide fresh and important insights into the genetic basis of evolutionary change, and are now being employed to investigate mating behaviour. Here, we focus on how selection techniques can reveal the genetic basis of post-mating adaptations to sexual selection and sexual conflict. Alteration of the operational sex ratio of adult Drosophila over just a few tens of generations can lead to altered ejaculate allocation patterns and the evolution of resistance in females to the costly effects of elevated mating rates. We provide new data to show how male responses to the presence of rivals can evolve. For several traits, the way in which males responded to rivals was opposite in lines selected for male-biased, as opposed to female-biased, adult sex ratio. This shows that the manipulation of the relative intensity of intra- and inter-sexual selection can lead to replicable and repeatable effects on mating systems, and reveals the potential for significant contemporary evolutionary change. Such studies, with important safeguards, have potential utility for understanding sexual selection and sexual conflict across many taxa. We discuss how artificial selection studies combined with genomics will continue to deepen our knowledge of the evolutionary principles first laid down by Darwin 150 years ago.

Quantifying the life-history response to increased male exposure in female Drosophila Melanogaster

Precise estimates of costs and benefits, the fitness economics, of mating are of key importance in understanding how selection shapes the coevolution of male and female mating traits. However, fitness is difficult to define and quantify. Here, we used a novel application of an established analytical technique to calculate individual‐ and population‐based estimates of fitness—including those sensitive to the timing of reproduction—to measure the effects on females of increased exposure to males. Drosophila melanogaster females were exposed to high and low frequencies of contact with males, and life‐history traits for each individual female were recorded. We then compared different fitness estimates to determine which of them best described the changes in life histories. We predicted that rate‐sensitive estimates would be more accurate, as mating influences the rate of offspring production in this species. The results supported this prediction. Increased exposure to males led to significantly decreased fitness within declining but not stable or increasing populations. There was a net benefit of increased male exposure in expanding populations, despite a significant decrease in lifespan. The study shows how a more accurate description of fitness, and new insights can be achieved by considering individual life‐history strategies within the context of population growth.

Measuring the Fitness Benefits of Male Mate Choice in Drosophila Melanogaster.

It is increasingly realized that the potential for male mate choice is widespread across many taxa. However, measurements of the relative magnitude of the fitness benefits that such choice can confer are lacking. Here, we directly measured, in a comprehensive set of tests that manipulated key variables, the fitness benefits of male mate choice in Drosophila melanogaster by measuring egg production in females that were chosen or rejected by males. The results provided significant evidence for male mate choice. In absolute terms, the observed degree of choice increased male fitness by an average of only 1.59 eggs. However, using a novel technique we show that this benefit of choice represented 14.5% of the maximum potential fitness benefit of choice. The magnitude of mate choice was not significantly altered by variation in (1) mate compatibility, (2) phenotypic plasticity in male mate choice, or (3) whether choosing males were preferred or nonpreferred by females. Overall, we show that male mate choice represents a subtle but significant opportunity for sexual selection, and we offer a novel and widely applicable method for quantifying mate choice.

Sperm competition risk drives plasticity in seminal fluid composition

BackgroundEjaculates contain a diverse mixture of sperm and seminal fluid proteins, the combination of which is crucial to male reproductive success under competitive conditions. Males should therefore tailor the production of different ejaculate components according to their social environment, with particular sensitivity to cues of sperm competition risk (i.e. how likely it is that females will mate promiscuously). Here we test this hypothesis using an established vertebrate model system, the house mouse (Mus musculus domesticus), combining experimental data with a quantitative proteomics analysis of seminal fluid composition. Our study tests for the first time how both sperm and seminal fluid components of the ejaculate are tailored to the social environment.ResultsOur quantitative proteomics analysis reveals that the relative production of different proteins found in seminal fluid – i.e. seminal fluid proteome composition – differs significantly according to cues of sperm competition risk. Using a conservative analytical approach to identify differential expression of individual seminal fluid components, at least seven of 31 secreted seminal fluid proteins examined showed consistent differences in relative abundance under high versus low sperm competition conditions. Notably three important proteins with potential roles in sperm competition – SVS 6, SVS 5 and CEACAM 10 – were more abundant in the high competition treatment groups. Total investment in both sperm and seminal fluid production also increased with cues of heightened sperm competition risk in the social environment. By contrast, relative investment in different ejaculate components was unaffected by cues of mating opportunities.ConclusionsOur study reveals significant plasticity in different ejaculate components, with the production of both sperm and non-sperm fractions of the ejaculate strongly influenced by the social environment. Sperm competition risk is thus shown to be a key factor in male ejaculate production decisions, including driving plasticity in seminal fluid composition.

Sexual Conflict and Sperm Competition

Traits that increase a males fertilization success during sperm competition can be harmful to females and therefore represent a source of sexual conflict. In this review, we consider the variety of male adaptations to sperm competition (MASC) that may give rise to sexual conflict-including mate guarding, prolonged copulations, the transfer of large numbers of sperm, and the manipulation of females through nonsperm components of the ejaculate. We then reflect on the fitness economics influencing the escalation of these sexual conflicts, considering the likelihood of females evolving traits to offset the negative effects of MASC when compared with the strong selection on males that lead to MASC. We conclude by discussing the potential evolutionary outcomes of sexual conflict arising from MASC, including the opportunities for females to mitigate conflict costs and the prospects for conflict resolution.

INTERACTIONS BETWEEN GENOTYPE AND SEXUAL CONFLICT ENVIRONMENT INFLUENCE TRANSGENERATIONAL FITNESS IN DROSOPHILA MELANOGASTER

Theory predicts that sexual conflict can fuel evolutionary change and generate substantial reproductive costs. This was tested here by measuring the fitness of focal individuals across multiple generations using an experimental framework. We manipulated sexual conflict through high versus low exposure of females to males across a four‐generation pedigree of Drosophila melanogaster, and assessed fitness in 1062 females and 639 males. We used the animal model to estimate (1) genotype by sexual conflict environment interactions for female fitness and (2) indirect benefits gained through sons and daughters. Some female genotypes achieved higher fitness under low, in comparison to high, conflict and vice versa. We found a consistent 10% reduction in female fitness under high conflict, regardless of maternal history. Following high exposure, females produced sons with increased, but grandsons with decreased, fitness. This opposing effect suggests no consistent fitness gains through sons for females that mated multiply. We saw no indirect benefits through daughters. Our pedigree was based exclusively on maternal links; however, maternal effects are unlikely to contribute significantly unless expressed across multiple generations. In sum, we quantified a significant sexual conflict load and a female genotype by sexual conflict interaction that could slow the erosion of genetic variation.

Variation in adult sex ratio alters the association between courtship, mating frequency and paternity in the lek‐forming fruitfly Ceratitis capitata

The intensity with which males deliver courtship and the frequency with which they mate are key components of male reproductive success. However, we expect the strength of the relationship between these traits and a male’s overall paternity to be strongly context dependent, for example to be altered significantly by the extent of post‐mating competition. We tested this prediction in a lekking insect, Ceratitis capitata (medfly). We examined the effect of manipulating the sex ratio from male‐ to female‐biased (high and low male competition, respectively) on courtship behaviour, mating frequency and paternity of focal males. Under high male competition, focal males delivered significantly more courtship but gained lower paternity than under lower competition. Paternity was positively associated with mating frequency and small residual testes size. However, the association between mating frequency and paternity was significantly stronger under low competition. We conclude that manipulation of sex ratio significantly altered the predictors of mating success and paternity. The relationship between pre‐ and post‐mating success is therefore plastic and alters according to the prevailing level of competition. The results highlight the importance of post‐copulatory processes in lekking species and illuminate selection pressures placed on insects such as medflies that are mass reared for pest control.

SEXUAL CONFLICT AND INTERACTING PHENOTYPES: A QUANTITATIVE GENETIC ANALYSIS OF FECUNDITY AND COPULA DURATION IN DROSOPHILA MELANOGASTER

Many reproductive traits that have evolved under sexual conflict may be influenced by both sexes. Investigation of the genetic architecture of such traits can yield important insight into their evolution, but this entails that the heritable component of variation is estimated for males and females—as an interacting phenotype. We address the lack of research in this area through an investigation of egg production and copula duration in the fruit fly, Drosophila melanogaster. Despite egg production rate being determined by both sexes, which may cause sexual conflict, an assessment of this trait as an interacting phenotype is lacking. It is currently unclear whether copula duration is determined by males and/or females. We found significant female, but not male, genetic variance for egg production rate that may indicate reduced potential for ongoing sexually antagonistic coevolution. In contrast, copula duration was determined by significant genetic variance in both sexes. We also identified genetic variation in egg retention among virgin females. Although previously identified in wild populations, it is unclear why this should be present in a laboratory stock. This study provides a novel insight into the shared genetic architecture of reproductive traits that are the subject of sexual conflict.

Variation in Male Mate Choice in Drosophila melanogaster

Male mate choice has been reported in the fruit fly, Drosophila melanogaster, even though males of this species were previously thought to maximise their fitness by mating with all available females. To understand the evolution of male mate choice it is important to understand variation in male mating preferences. Two studies, using different stock populations and different methods, have reported contrasting patterns of variation in male mate choice in D. melanogaster. Two possible explanations are that there are evolved differences in each stock population or that the methods used to measure choice could have biased the results. We investigated these hypotheses here by repeating the methods used in one study in which variable male mate choice was found, using the stock population from the other study in which choice was not variable. The results showed a significant resource-independent male preference for less fecund, smaller females, which contrasts with previous observations of male mate choice. This indicates that different selection pressures between populations have resulted in evolved differences in the expression of male mate choice. It also reveals phenotypic plasticity in male mate choice in response to cues encountered in each choice environment. The results highlight the importance of variation in male mate choice, and of identifying mechanisms in order to understand the evolution of mate choice under varying ecological conditions.