Sexual conflict is not counterbalanced by good genes in the laboratory Drosophila melanogaster model system

Sexual conflict theory is based on the observation that females of many species are harmed through their interactions with males. Direct harm to females, however, can potentially be counterbalanced by indirect genetic benefits, where females make up for a reduction in offspring quantity by an increase in offspring quality through a generic increase in offspring fitness (good genes) and/or one restricted to the context of sexual selection (sexy sons). Here, we quantify the magnitude of the good genes mechanism of indirect benefits in a laboratory-adapted population of Drosophila melanogaster. We find that despite high-standing genetic variance for fitness, females gain at most only a modest benefit through the good genes form of indirect benefits--far too little to counterbalance the direct cost of male-induced harm.     

Sexy sons from re-mating do not recoup the direct costs of harmful male interactions in the Drosophila melanogaster laboratory model system

The empirical foundation for sexual conflict theory is the data from many different taxa demonstrating that females are harmed while interacting with males. However, the interpretation of this keystone evidence has been challenged because females may more than counterbalance the direct costs of interacting with males by the indirect benefits of obtaining higher quality genes for their offspring. A quantification of this trade-off is critical to resolve the controversy and is presented here. A multi-generation fitness assay in the Drosophila melanogaster laboratory model system was used to quantify both the direct costs to females due to interactions with males and indirect benefits via sexy sons. We specifically focus on the interactions that occur between males and nonvirgin females. In the laboratory environment of our base population, females mate soon after eclosion and store sufficient sperm for their entire lifetime, yet males persistently court these nonvirgin females and frequently succeed in re-mating them. Females may benefit from these interactions despite direct costs to their lifetime fecundity if re-mating allows them to trade-up to mates of higher genetic quality and thereby secure indirect benefits for their offspring. We found that direct costs of interactions between males and nonvirgin females substantially exceeded indirect benefits through sexy sons. These data, in combination with past studies of the good genes route of indirect benefits, demonstrate that inter-sexual interactions drive sexually antagonistic co-evolution in this model system.     

The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions

The diversity of social interactions between sexual partners has long captivated biologists, and its evolution has been interpreted largely in terms of 'direct fitness' pay-offs to partners and their descendants. Inter-sexual interactions also have 'indirect effects' by affecting the fitness of relatives, with important consequences for inclusive fitness. However, inclusive fitness arguments have received limited consideration in this context, and definitions of 'direct' and 'indirect' fitness effects in this field are often inconsistent with those of inclusive fitness theory. Here, we use a sociobiology approach based on inclusive fitness theory to distinguish between direct and indirect fitness effects. We first consider direct effects: we review how competition leads to sexual conflict, and discuss the conditions under which repression of competition fosters sexual mutualism. We then clarify indirect effects, and show that greenbeard effects, kin recognition and population viscosity can all lead to episodes of indirect selection on sexual interactions creating potential for sexual altruism and spite. We argue that the integration of direct and indirect fitness effects within a sociobiology approach enables us to consider a more diverse spectrum of evolutionary outcomes of sexual interactions, and may help resolving current debates over sexual selection and sexual conflict.     

Direct benefits of choosing a high‐fitness mate can offset the indirect costs associated with intralocus sexual conflict

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.     

Good genes and sexual selection in dung beetles (Onthophagus taurus): genetic variance in egg-to-adult and adult viability

Whether species exhibit significant heritable variation in fitness is central for sexual selection. According to good genes models there must be genetic variation in males leading to variation in offspring fitness if females are to obtain genetic benefits from exercising mate preferences, or by mating multiply. However, sexual selection based on genetic benefits is controversial, and there is limited unambiguous support for the notion that choosy or polyandrous females can increase the chances of producing offspring with high viability. Here we examine the levels of additive genetic variance in two fitness components in the dung beetle Onthophagus taurus. We found significant sire effects on egg-to-adult viability and on son, but not daughter, survival to sexual maturity, as well as moderate coefficients of additive variance in these traits. Moreover, we do not find evidence for sexual antagonism influencing genetic variation for fitness. Our results are consistent with good genes sexual selection, and suggest that both pre- and postcopulatory mate choice, and male competition could provide indirect benefits to females.     

Female resistance to sexual coercion can evolve to preserve the indirect benefits of mate choice

Sexual conflict over the indirect benefits of mate choice may arise when traits in one sex limit the ability of the other sex to freely choose mates but when these coercive traits are not necessarily directly harmful (i.e. forced fertilization per se). Although we might hypothesize that females can evolve resistance in order to retain the indirect, genetic benefits (reflected in offspring attractiveness) of mating with attractive males, up to now it has been difficult to evaluate potential underlying mechanisms. Traditional theoretical approaches do not usually conceptually distinguish between female preference for male mating display and female resistance to forced fertilization, yet sexual conflict over indirect benefits implies the simultaneous action of all of these traits. Here, we present an integrative theoretical framework that draws together concepts from both sexual selection and sexual conflict traditions, allowing for the simultaneous coevolution of displays and preferences, and of coercion and resistance. We demonstrate that it is possible for resistance to coercion to evolve in the absence of direct costs of mating to preserve the indirect benefits of mate choice. We find that resistance traits that improve the efficacy of female mating preference can evolve as long as females are able to attain some indirect benefits of mating with attractive males, even when both attractive and unattractive males can coerce. These results reveal new evolutionary outcomes that were not predicted by prior theories of indirect benefits or sexual conflict.     

Reinvestigating good genes benefits of mate choice in Drosophila simulans

Studies investigating the genetic benefits of female mate choice frequently find Fisherian benefits to choice, at the same time as detecting small or no good genes (viability) effects. This could be because sons trade‐off viability for increased mating success and, accordingly, it has been suggested that good genes benefits should be investigated in daughters. However, good genes benefits via daughters could also be disrupted by intralocus sexual conflict. As a result, it is not clear when and if good genes benefits should accrue. We investigated potential good genes effects in Drosophila simulans using an isofemale line approach. We assessed the attractiveness of males in two different ways and then measured the longevity, as well as lifetime reproductive success, of their daughters. We also assessed potential direct benefits of female mate choice and good genes effects through the longevity of sons. We found no evidence of direct or good genes benefits to females mating with attractive males, and the failure to find good genes effects via daughters was apparently not a result of masking through intralocus sexual conflict. The results obtained in the present study are consistent with previous findings in this species, and suggest that good genes benefits are at best very small in our study population. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 295–306.     

The coevolution of sexual imprinting by males and females

Sexual imprinting is the learning of a mate preference by direct observation of the phenotype of another member of the population. Sexual imprinting can be paternal, maternal, or oblique if individuals learn to prefer the phenotypes of their fathers, mothers, or other members of the population, respectively. Which phenotypes are learned can affect trait evolution and speciation rates. “Good genes” models of polygynous systems predict that females should evolve to imprint on their fathers, because paternal imprinting helps females to choose mates that will produce offspring that are both viable and sexy. Sexual imprinting by males has been observed in nature, but a theory for the evolution of sexual imprinting by males does not exist. We developed a good genes model to study the conditions under which sexual imprinting by males or by both sexes can evolve and to ask which sexual imprinting strategies maximize the fitness of the choosy sex. We found that when only males imprint, maternal imprinting is the most advantageous strategy. When both sexes imprint, it is most advantageous for both sexes to use paternal imprinting. Previous theory suggests that, in a given population, either males or females but not both will evolve choosiness in mating. We show how environmental change can lead to the evolution of sexual imprinting behavior by both sexes in the same population.     

Good genes go fisherian

It has been a common perception of the ‘good genes’ mechanism of sexual selection that mating with males affording the most extreme sexual ornaments should benefit females by increasing the survival of their progeny. The ‘sexy son’ mechanism, however, stressed the enhanced reproduction of highly ornamented male progeny. A new model developed by Kokko et al. now shows that both mechanisms belong to the same continuum of indirect selection, but their relative weights can vary depending on the costs of mate choice.     

Sexual selection and conflict in the bulb mite, <Emphasis Type="Italic">Rhizoglyphus robini</Emphasis> (Astigmata: Acaridae)

Whether benefits of mate choice accrued by females outweigh costs associated with sexual selection remains largely unresolved. The ‘good genes’ perspective, posing that mate choice benefits females genetically has been challenged by the arguments that sexual selection is driven mostly by direct costs and inter-sexual conflict. Here, I present an overview of experimental tests of predictions of good genes and sexual conflict mechanisms in the bulb mite Rhizoglyphus robini.     

The limits of sexual conflict in the narrow sense: new insights from waterfowl biology

Sexual conflict occurs when the evolutionary interests of the sexes differ and it broadly applies to decisions over mating, fertilization and parental investment. Recently, a narrower view of sexual conflict has emerged in which direct selection on females to avoid male-imposed costs during mating is considered the distinguishing feature of conflict, while indirect selection is considered negligible. In this view, intersexual selection via sensory bias is seen as the most relevant mechanism by which male traits that harm females evolve, with antagonistic coevolution between female preferences and male manipulation following. Under this narrower framework, female preference and resistance have been synonymized because both result in a mating bias, and similarly male display and coercion are not distinguished. Our recent work on genital evolution in waterfowl has highlighted problems with this approach. In waterfowl, preference and resistance are distinct components of female phenotype, and display and coercion are independent male strategies. Female preference for male displays result in mate choice, while forced copulations by unpreferred males result in resistance to prevent these males from achieving matings and fertilizations. Genital elaborations in female waterfowl appear to function in reinforcing female preference to maintain the indirect benefits of choice rather than to reduce the direct costs of coercive mating. We propose a return to a broader view of conflict where indirect selection and intrasexual selection are considered important in the evolution of conflict.     

Indirect effects of phytochemicals on offspring performance of Queensland fruit fly,Bactrocera tryoni (Diptera: Tephritidae)

Phytochemical lures such as methyl eugenol (ME) and cue‐lure are used in the management of Bactrocera fruit flies for monitoring and control. These lures are not just attractants, but also trigger physiological changes in males that lead to enhanced mating success. Additionally, in the cue‐lure‐responsive Bactrocera tryoni, females mated with lure‐fed males exhibit changes in fecundity, remating receptivity and longevity. While the lures show current generation effects, no research has been carried out on possible multigenerational effects, although such effects have been hypothesized within a ‘sexy‐son’ sexual selection model. In this study, we test for indirect, cross‐generational effects of lure exposure in F1offspring of B. tryoni females mated with cue‐lure‐fed, zingerone‐fed and lure‐unfed (=control) males. The F1 attributes we recorded were immature development time, immature survival, adult survival and adult male lure foraging. No significant differences were found between treatments for any of the three life‐history measurements, except that the offspring sired by zingerone‐fed males had a longer egg development time than cue‐lure and control offspring. However, indirect exposure to lures significantly enhanced the lure‐foraging ability of F1 adult males. More offspring of cue‐lure‐fed males arrived at a lure source in both large flight cages and small laboratory cages over a 2‐h period than did control males. The offspring of zingerone‐fed males were generally intermediate between cue‐lure and control offspring. This study provides the first evidence of a next generation effect of fruit fly male lures. While the results of this study support a ‘sexy‐son’ sexual selection mechanism for the evolution of lure response in Bactrocera fruit flies, our discussion urges caution in interpreting our results in this way.     

PURGING THE GENOME WITH SEXUAL SELECTION: REDUCING MUTATION LOAD THROUGH SELECTION ON MALES

Healthy males are likely to have higher mating success than unhealthy males because of differential expression of condition‐dependent traits such as mate searching intensity, fighting ability, display vigor, and some types of exaggerated morphological characters. We therefore expect that most new mutations that are deleterious for overall fitness may also be deleterious for male mating success. From this perspective, sexual selection is not limited to influencing those genes directly involved in exaggerated morphological traits but rather affects most, if not all, genes in the genome. If true, sexual selection can be an important force acting to reduce the frequency of deleterious mutations and, as a result, mutation load. We review the literature and find various forms of indirect evidence that sexual selection helps to eliminate deleterious mutations. However, direct evidence is scant, and there are almost no data available to address a key issue: is selection in males stronger than selection in females? In addition, the total effect of sexual selection on mutation load is complicated by possible increases in mutation rate that may be attributable to sexual selection. Finally, sexual selection affects population fitness not only through mutation load but also through sexual conflict, making it difficult to empirically measure how sexual selection affects load. Several lines of enquiry are suggested to better fill large gaps in our understanding of sexual selection and its effect on genetic load.     

Mate‐sampling costs and sexy sons

Costly female mating preferences for purely Fisherian male traits (i.e. sexual ornaments that are genetically uncorrelated with inherent viability) are not expected to persist at equilibrium. The indirect benefit of producing ‘sexy sons’ (Fisher process) disappears: in some models, the male trait becomes fixed; in others, a range of male trait values persist, but a larger trait confers no net fitness advantage because it lowers survival. Insufficient indirect selection to counter the direct cost of producing fewer offspring means that preferences are lost. The only well‐cited exception assumes biased mutation on male traits. The above findings generally assume constant direct selection against female preferences (i.e. fixed costs). We show that if mate‐sampling costs are instead derived based on an explicit account of how females acquire mates, an initially costly mating preference can coevolve with a male trait so that both persist in the presence or absence of biased mutation. Our models predict that empirically detecting selection at equilibrium will be difficult, even if selection was responsible for the location of the current equilibrium. In general, it appears useful to integrate mate sampling theory with models of genetic consequences of mating preferences: being explicit about the process by which individuals select mates can alter equilibria.     

Assessing sexual conflict in the Drosophila melanogaster laboratory model system

We describe a graphical model of interlocus coevolution used to distinguish between the interlocus sexual conflict that leads to sexually antagonistic coevolution, and the intrinsic conflict over mating rate that is an integral part of traditional models of sexual selection. We next distinguish the 'laboratory island' approach from the study of both inbred lines and laboratory populations that are newly derived from nature, discuss why we consider it to be one of the most fitting forms of laboratory analysis to study interlocus sexual conflict, and then describe four experiments using this approach with Drosophila melanogaster. The first experiment evaluates the efficacy of the laboratory model system to study interlocus sexual conflict by comparing remating rates of females when they are, or are not, provided with a spatial refuge from persistent male courtship. The second experiment tests for a lag-load in males that is due to adaptations that have accumulated in females, which diminish male-induced harm while simultaneously interfering with a male's ability to compete in the context of sexual selection. The third and fourth experiments test for a lag-load in females owing to direct costs from their interactions with males, and for the capacity for indirect benefits to compensate for these direct costs.     

Assessing putative interlocus sexual conflict in Drosophila melanogaster using experimental evolution

The theoretical foundation of sexually antagonistic coevolution is that females suffer a net fitness cost through their interactions with males. The empirical prediction is that direct costs to female lifetime fecundity will exceed indirect benefits despite a possible increase in the genetic quality of offspring. Although direct costs of males have been repeatedly shown, to date no study has comprehensively tested whether females are compensated for this direct harm through indirect benefits. Here we use experimental evolution to show that a mutation giving Drosophila melanogaster females nearly complete resistance to the direct costs of male courtship and remating, but which also excluded almost all indirect benefits, is strongly favoured by selection. We estimated the selection coefficient favouring the resistance allele to be +20%. These results demonstrate that any indirect benefits that females accrued were not sufficient to counter-balance the direct costs of males, and reinforce a large body of past studies by verifying interlocus sexual conflict in this model system.     

Parental sex discrimination and intralocus sexual conflict

Intralocus sexual conflict occurs when populations segregate for alleles with opposing fitness consequences in the two sexes. This form of selection is known to be capable of maintaining genetic and fitness variation in nature, the extent of which is sensitive to the underlying genetics. We present a one-locus model of a haploid maternal effect that has sexually antagonistic consequences for offspring. The evolutionary dynamics of these maternal effects are distinct from those of haploid direct effects under sexual antagonism because the relevant genes are expressed only in females. Despite this, we find the same opportunity for sexually antagonistic polymorphism at the maternal effect locus as at a direct effect locus. Thus, sexually antagonistic maternal effects may underlie some natural genetic variation. The model we present permits alternative interpretations of how the genes are expressed and how the fitness variation is assigned, which invites a theoretical comparison to models of both imprinted genes and sex allocation.     

Experimental evidence that sexual conflict influences the opportunity, form and intensity of sexual selection

Sexual interactions are often rife with conflict. Conflict between members of the same sex over opportunities to mate has long been understood to effect evolution via sexual selection. Although conflict between males and females is now understood to be widespread, such conflict is seldom considered in the same light as a general agent of sexual selection. Any interaction between males or females that generates variation in fitness, whether due to conflict, competition or mate choice, can potentially influence sexual selection acting on a range of male traits. Here we seek to address a lack of direct experimental evidence for how sexual conflict influences sexual selection more broadly. We manipulate a major source of sexual conflict in the black field cricket, Teleogryllus commodus, and quantify the resulting changes in the nature of sexual selection using formal selection analysis to statistically compare multivariate fitness surfaces. In T. commodus, sexual conflict occurs over the attachment time of an external spermatophore. By experimentally manipulating the ability of males and females to influence spermatophore attachment, we found that sexual conflict significantly influences the opportunity, form, and intensity of sexual selection on male courtship call and body size. When males were able to harass females, the opportunity for selection was smaller, the form of selection changed, and sexual selection was weaker. We discuss the broader evolutionary implications of these findings, including the contributions of sexual conflict to fluctuating sexual selection and the maintenance of additive genetic variation.     

Intralocus sexual conflict for fitness: sexually antagonistic alleles for testosterone

Intralocus sexual conflict occurs when a trait encoded by the same genetic locus in the two sexes has different optima in males and females. Such conflict is widespread across taxa, however, the shared phenotypic traits that mediate the conflict are largely unknown. We examined whether the sex hormone, testosterone (T), that controls sexual differentiation, contributes to sexually antagonistic fitness variation in the bank vole, Myodes glareolus. We compared (opposite-sex) sibling reproductive fitness in the bank vole after creating divergent selection lines for T. This study shows that selection for T was differentially associated with son versus daughter reproductive success, causing a negative correlation in fitness between full siblings. Our results demonstrate the presence of intralocus sexual conflict for fitness in this small mammal and that sexually antagonistic selection is acting on T. We also found a negative correlation in fitness between parents and their opposite-sex progeny (e.g. father-daughter), highlighting a dilemma for females, as the indirect genetic benefits of selecting reproductively successful males (high T) are lost with daughters. We discuss mechanisms that may mitigate this disparity between progeny quality.     

Beyond sex allocation: the role of mating systems in sexual selection in parasitoid wasps

Despite the diverse array of mating systems and life histories which characterise the parasitic Hymenoptera, sexual selection and sexual conflict in this taxon have been somewhat overlooked. For instance, parasitoid mating systems have typically been studied in terms of how mating structure affects sex allocation. In the past decade, however, some studies have sought to address sexual selection in the parasitoid wasps more explicitly and found that, despite the lack of obvious secondary sexual traits, sexual selection has the potential to shape a range of aspects of parasitoid reproductive behaviour and ecology. Moreover, various characteristics fundamental to the parasitoid way of life may provide innovative new ways to investigate different processes of sexual selection. The overall aim of this review therefore is to re‐examine parasitoid biology with sexual selection in mind, for both parasitoid biologists and also researchers interested in sexual selection and the evolution of mating systems more generally. We will consider aspects of particular relevance that have already been well studied including local mating structure, sex allocation and sperm depletion. We go on to review what we already know about sexual selection in the parasitoid wasps and highlight areas which may prove fruitful for further investigation. In particular, sperm depletion and the costs of inbreeding under chromosomal sex determination provide novel opportunities for testing the role of direct and indirect benefits for the evolution of mate choice.