Sexual selection: harem size and the variance in male reproductive success

Sexual selection is potentially stronger than natural selection when the variance in male reproductive fitness exceeds all other components of fitness variance combined. However, measuring the variance in male reproductive fitness is difficult when nonmating males are absent, inconspicuous, or otherwise difficult to find. Omitting the nonmating males inflates estimates of average male reproductive success and diminishes the variance, leading to underestimates of the potential strength of sexual selection. We show that, in theory, the proportion of the total variance in male fitness owing to sexual selection is approximately equal to H, the mean harem size, as long as H is large and females are randomly distributed across mating males (i.e., Vharem=H). In this case, mean harem size not only provides an easy way to estimate the potential strength of sexual selection but also equals the opportunity for sexual selection, I(mates). In nature, however, females may be overdispersed with VharemH. We show that H+(k-1) is a good measure of the opportunity for sexual selection, where k is the ratio Vharem/H. A review of mating system data reveals that in nature the median ratio for Vharem/H is 1.04, but as H increases, females tend to become more aggregated across mating males with V(harem) two to three times larger than H.     

EXPERIMENTAL MANIPULATION OF SEXUAL SELECTION PROMOTES GREATER MALE MATING CAPACITY BUT DOES NOT ALTER SPERM INVESTMENT

Sexual selection theory makes clear predictions regarding male spermatogenic investment. To test these predictions we used experimental sexual selection in Drosophila pseudoobscura , a sperm heteromorphic species in which males produce both fertile and sterile sperm, the latter of which may function in postmating competition. Specifically, we determined whether the number and size of both sperm types, as well as relative testis mass and accessory gland size, increased with increased sperm competition risk and whether any fitness benefits could accrue from such changes. We found no effect of sexual selection history on either the number or size of either sperm morph, or on relative testis mass. However, males experiencing a greater opportunity for sexual selection evolved the largest accessory glands, had the greatest mating capacity, and sired the most progeny. These findings suggest that sterile sperm are not direct targets of sexual selection and that accessory gland size, rather than testis mass, appears to be an important determinant of male reproductive success. We briefly review the data from experimental sexual selection studies and find that testis mass may not be a frequent target of postcopulatory sexual selection and, even when it is, the resulting changes do not always improve fitness.     

The fitness advantage of a high-performance weapon

Weapons used in combat between males are usually attributed to sexual selection, which operates via a fitness advantage for males with weapons of better 'quality'. Because the performance capacity of morphological traits is typically considered the direct target of selection, Darwin's intrasexual selection hypothesis can be modified to predict that variation in reproductive success should be explained by variation in performance traits relevant to combat. Despite such a straightforward prediction, tests of this hypothesis are conspicuously lacking. We show that territorial male collared lizards with greater bite-force capacity sire more offspring than weaker biting rivals but exhibit no survival advantage. We did not detect stabilizing or disruptive selection on bite-force capacity. Taken together, these results support the hypothesis that superior weapon performance provides a fitness advantage through increased success in male contests. Sexual selection on weapon performance therefore appears to be a force driving the evolution and maintenance of sexual dimorphism in head shape.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 840–845.     

Natural and sexual selection against hybrid flycatchers

While sexual selection is generally assumed to quickly cause or strengthen prezygotic barriers between sister species, its role in causing postzygotic isolation, through the unattractiveness of intermediate hybrids, is less often examined. Combining 24 years of pedigree data and recently developed species-specific molecular markers from collared (Ficedula albicollis) and pied (Ficedula hypoleuca) flycatchers and their hybrids, we were able to quantify all key components of fitness. To disentangle the relative role of natural and sexual selection acting on F1 hybrid flycatchers, we estimated various fitness components, which when combined represent the total lifetime reproductive success of F1 hybrids, and then compared the different fitness components of F1 hybrids to that of collared flycatchers. Female hybrid flycatchers are sterile, with natural selection being the selective force involved, but male hybrids mainly experienced a reduction in fitness through sexual selection (decreased pairing success and increased rate of being cuckolded). To disentangle the role of sexual selection against male hybrids from a possible effect of genetic incompatibility (on the rate of being cuckolded), we compared male hybrids with pure-bred males expressing intermediate plumage characters. Given that sexual selection against male hybrids is a result of their intermediate plumage, we expect these two groups of males to have a similar fitness reduction. Alternatively, hybrids have reduced fitness owing to genetic incompatibility, in which case their fitness should be lower than that of the intermediate pure-bred males. We conclude that sexual selection against male hybrids accounts for approximately 75% of the reduction in their fitness. We discuss how natural and sexual selection against hybrids may have different implications for speciation and conclude that reinforcement of reproductive barriers may be more likely when there is sexual selection against hybrids.     

Sex, mutation and fitness: asymmetric costs and routes to recovery through compensatory evolution

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.     

Spatial environmental complexity mediates sexual conflict and sexual selection in Drosophila melanogaster

Sexual selection is an important agent of evolutionary change, but the strength and direction of selection often vary over space and time. One potential source of heterogeneity may lie in the opportunity for male–male and/or male–female interactions imposed by the spatial environment. It has been suggested that increased spatial complexity permits sexual selection to act in a complementary fashion with natural selection (hastening the loss of deleterious alleles and/or promoting the spread of beneficial alleles) via two (not mutually exclusive) pathways. In the first scenario, sexual selection potentially acts more strongly on males in complex environments, allowing males of greater genetic “quality” a greater chance of outcompeting rivals, with benefits manifested indirectly in offspring. In the second scenario, increased spatial complexity reduces opportunities for males to antagonistically harm females, allowing females (especially those of greater potential fecundities) to achieve greater reproductive success (direct fitness benefits). Here, using Drosophila melanogaster, we explore the importance of these mechanisms by measuring direct and indirect fitness of females housed in simple vial environments or in vials in which spatial complexity has been increased. We find strong evidence in favor of the female conflict‐mediated pathway as individuals in complex environments remated less frequently and produced more offspring than those housed in a simpler spatial environment, but no difference in the fitness of sons or daughters. We discuss these results in the context of other recent studies and what they mean for our understanding of how sexual selection operates.     

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.     

Don'T throw bateman out with the bathwater!

Bateman identified two aspects of sexual selection. The first,called Bateman's principle, is that sexual selection favorsincreased promiscuity of males but not of females as a resultof differences in parental investment in gametes. The secondis that the variance in mate number of males is the fundamentalcause of a sex difference in fitness variance. We argue thatBateman's insight about the source of sexual selection is morefundamental than his speculation about patterns of parentalinvestment. We show that, when the sex ratio is 1:1, the averagefemale must be as promiscuous as the average male, because eachcopulation involves one male and one female. Because mean maleand female promiscuity are tied together in the same manneras mean male and female fitness, a sex difference in matingpropensity must be the result of either (1) a sex differencein the covariance between matings and number offspring, or (2)Fisherian run-away sexual selection, wherein female reluctanceto mate is a weak form of female choice. We show how femalepromiscuity can limit the evolution of male promiscuity, turningthe central argument of parental investment theory on its head.     

Determinants of male fitness: disentangling intra- and inter-sexual selection

Both intra- and inter-sexual selection may crucially determine a male's fitness. Their interplay, which has rarely been experimentally investigated, determines a male's optimal reproductive strategy and thus is of fundamental importance to the understanding of a male's behaviour. Here we investigated the relative importance of intra- and inter-sexual selection for male fitness in the common lizard. We investigated which male traits predict a male's access to reproduction allowing for both selective pressures and comparing it with a staged mating experiment excluding all types of intra-sexual selection. We found that qualitatively better males were more likely to reproduce and that sexual selection was two times stronger when allowing for both selective pressures, suggesting that inter- and intra-sexual selection determines male fitness and confirming the existence of multi-factorial sexual selection. Consequently, to optimize fitness, males should trade their investment between the traits, which are important for inter- and intra-sexual selection.     

Reproductive competition promotes the evolution of female weaponry

Secondary sexual traits in females are a relatively rare phenomenon. Empirical studies have focused on the role of male mate choice in their evolution; however, recently it has been suggested that secondary sexual traits in females are more likely to be under selection via reproductive competition. We investigated female competition and the influence of female phenotype on fitness in Onthophagus sagittarius, a species of dung beetle that exhibits female-specific horns. We compared reproductive fitness when females were breeding in competition versus breeding alone and found that competition for breeding resources reduced fitness for all females, but that smaller individuals suffered a greater fitness reduction than larger individuals. When females were matched for body size, those with the longest horns gained higher reproductive fitness. The fitness function was positive and linear, favouring increased horn expression. Thus, we present evidence that female body size and horn size in O. sagittarius are under directional selection via competition for reproductive resources. Our study is a rare example of female contest competition selecting for female weaponry.     

Maternal inheritance,epigenetics and the evolution of polyandry

Growing evidence indicates that females actively engage in polyandry either to avoid genetic incompatibility or to bias paternity in favor of genetically superior males. Despite empirical support for the intrinsic male quality hypothesis, the maintenance of variation in male fitness remains a conundrum for traditional "good genes" models of sexual selection. Here, we discuss two mechanisms of non-Mendelian inheritance, maternal inheritance of mitochondria and epigenetic regulation of gene expression, which may explain the persistence of variation in male fitness traits important in post-copulatory sexual selection. The inability of males to transmit mitochondria precludes any direct evolutionary response to selection on mitochondrial mutations that reduce or enhance male fitness. Consequently, mitochondrial-based variation in sperm traits is likely to persist, even in the face of intense sperm competition. Indeed, mitochondrial nucleotide substitutions, deletions and insertions are now known to be a primary cause of low sperm count and poor sperm motility in humans. Paradoxically, in the field of sexual selection, female-limited response to selection has been largely overlooked. Similarly, the contribution of epigenetics (e.g., DNA methylation, histone modifications and non-coding RNAs) to heritable variation in male fitness has received little attention from evolutionary theorists. Unlike DNA sequence based variation, epigenetic variation can be strongly influenced by environmental and stochastic effects experienced during the lifetime of an individual. Remarkably, in some cases, acquired epigenetic changes can be stably transmitted to offspring. A recent study indicates that sperm exhibit particularly high levels of epigenetic variation both within and between individuals. We suggest that such epigenetic variation may have important implications for post-copulatory sexual selection and may account for recent findings linking sperm competitive ability to offspring fitness.     

Female alternative reproductive behaviors: the effect of female group size on mate assessment and copying

Extensive theoretical and empirical research has focused on male alternative reproductive tactics. In comparison, female alternative tactics have attracted little attention, and further theoretical and empirical research are needed. Using a game theoretical model, we examine female choice alternatives (1) by considering assessment errors in a novel and more realistic manner than done previously, and (2) for the first time, by highlighting the formation of groups of females as an important consequence of copying behavior. We consider two alternatives: direct assessment of male quality by females and female copying of the choice of other females. Assessment and copying are predicted to coexist under a wide variety of circumstances and copying is favored when females make assessment errors, when high-quality males are either common or very rare, and when female fitness declines with the number of other females choosing the same male. We also find that the frequency of copying at equilibrium is predicted to decrease when the presence of other females mating with the same male has a positive effect on female fitness (e.g. through increased male parental effort, decreased predation risk or cooperation among females). Female alternative choice tactics also influence the potential for sexual selection. In our model, when the frequency of copying females is low, the potential for sexual selection can be higher than in the absence of female copying. However, contrary to previous theory, we find that as copying females become more common than assessing females, the potential for sexual selection will be low as more females copy the mate choice of other copiers without assessment.     

Male competition fitness landscapes predict both forward and reverse speciation

Speciation is facilitated when selection generates a rugged fitness landscape such that populations occupy different peaks separated by valleys. Competition for food resources is a strong ecological force that can generate such divergent selection. However, it is unclear whether intrasexual competition over resources that provide mating opportunities can generate rugged fitness landscapes that foster speciation. Here we use highly variable male F2 hybrids of benthic and limnetic threespine sticklebacks, Gasterosteus aculeatus Linnaeus, 1758, to quantify the male competition fitness landscape. We find that disruptive sexual selection generates two fitness peaks corresponding closely to the male phenotypes of the two parental species, favouring divergence. Most surprisingly, an additional region of high fitness favours novel hybrid phenotypes that correspond to those observed in a recent case of reverse speciation after anthropogenic disturbance. Our results reveal that sexual selection through male competition plays an integral role in both forward and reverse speciation.     

Males' evolutionary responses to experimental removal of sexual selection

We evaluated the influence of pre- and post-copulatory sexual selection upon male reproductive traits in a naturally promiscuous species, Drosophila melanogaster. Sexual selection was removed in two replicate populations through enforced monogamous mating with random mate assignment or retained in polyandrous controls. Monogamous mating eliminates all opportunities for mate competition, mate discrimination, sperm competition, cryptic female choice and, hence, sexual conflict. Levels of divergence between lines in sperm production and male fitness traits were quantified after 38-81 generations of selection. Three a priori predictions were tested: (i) male investment in spermatogenesis will be lower in monogamy-line males due to the absence of sperm competition selection, (ii) due to the evolution of increased male benevolence, the fitness of females paired with monogamy-line males will be higher than that of females paired with control-line males, and (iii) monogamy-line males will exhibit decreased competitive reproductive success relative to control-line males. The first two predictions were supported, whereas the third prediction was not. Monogamy males evolved a smaller body size and the size of their testes and the number of sperm within the testes were disproportionately further reduced. In contrast, the fitness of monogamous males (and their mates) was greater when reproducing in a non-competitive context: females mated once with monogamous males produced offspring at a faster rate and produced a greater total number of surviving progeny than did females mated to control males. The results indicate that sexual selection favours the production of increased numbers of sperm in D. melanogaster and that sexual selection favours some male traits conferring a direct cost to the fecundity of females.     

Fluctuating asymmetry and sexual selection in the Mediterranean fruitfly (Diptera, Tephritidae)

Sexual selection is known to operate at medfly leks with a few males gaining a high proportion of matings. However, specific male characteristics subject to sexual selection have not been identified. Here we report laboratory studies indicating that directional sexual selection operates on the level of fluctuating asymmetry (FA) in the superior frontal orbital setae (sex setae), with symmetrical males gaining more matings. Studies relating mating success with FA in a male trait have generally been taken as evidence of the operation of indirect sexual selection. For a male trait to acts as a reliable indicator of fitness, FA in the male trait should be negatively associated with trait size and females should mate with the males with the most exaggerated form of the trait. However no association was found between seta FA and mean seta length. In addition sexual selection did not appear to operate on mean trait size, although males with an intermediate sex seta to wing length ratio did achieve higher mating success, indicating that stabilizing sexual selection operates on this relative dimension. It is suggested that differences in male competitive ability may provide an alternative explanation of how such associations between mating success and FA in male characteristics can arise.     

Proximity‐dependent Response to Variably Complex Mating Signals in Túngara Frogs (Physalaemus pustulosus)

The plasticity of animal behavior allows individuals to maximize fitness in a wide range of contexts. Both production of and preference for mating signals are context‐dependent according to internal factors such as hormonal state, and external factors such as predation risk. In many species, male‐to‐female proximity also defines an important context for mating communication. Males often possess short‐distance courtship signals, and females often exhibit distance‐related variation in signal response. Such variation in response may occur when a signal’s relevance changes with male‐to‐female distance, but it may also result from perceptual constraints that are unrelated to fitness. Túngara frogs produce variably complex advertisement calls, and sexual selection theory predicts that females should prefer calls of greater complexity. Preference tests, however, have not demonstrated consistent trends for preference between calls of variable complexity. We tested whether proximity to males influences female response to variable signal complexity and found that both preference and memory for signal complexity are proximity‐dependent.     

Positive genetic correlation between female preference and offspring fitness

In many species, females display preferences for extreme male signal traits, but it has not been determined if such preferences evolve as a consequence of females gaining genetic benefits from exercising choice. If females prefer extreme male traits because they indicate male genetic quality that will enhance the fitness of offspring, a genetic correlation will evolve between female preference genes and genes that confer offspring fitness. We show that females of Drosophila serrata prefer extreme male cuticular hydrocarbon (CHC) blends, and that this preference affects offspring fitness. Female preference is positively genetically correlated with offspring fitness, indicating that females have gained genetic benefits from their choice of males. Despite male CHCs experiencing strong sexual selection, the genes underlying attractive CHCs also conferred lower offspring fitness, suggesting a balance between sexual selection and natural selection may have been reached in this population.     

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.     

Perspective: sexual conflict and sexual selection: chasing away paradigm shifts

Abstract.— Traditional models of sexual selection propose that partner choice increases both average male and average female fitness in a population. Recent theoretical and empirical work, however, has stressed that sexual conflict may be a potent broker of sexual selection. When the fitness interests of males and females diverge, a reproductive strategy that increases the fitness of one sex may decrease the fitness of the other sex. The chase-away hypothesis proposes that sexual conflict promotes sexually antagonistic, rather than mutualistic, coevolution, whereby manipulative reproductive strategies in one sex are counteracted by the evolution of resistance to such strategies in the other sex. In this paper, we consider the criteria necessary to demonstrate the chase-away hypothesis. Specifically, we review sexual conflict with particular emphasis on the chase-away hypothesis; discuss the problems associated with testing the predictions of the chase-away hypothesis and the extent to which these predictions and the predictions of traditional models of sexual selection are mutually exclusive; discuss misconceptions and mismeasures of sexual conflict; and suggest an alternative approach to demonstrate sexual conflict, measure the intensity of sexually antagonistic selection in a population, and elucidate the coevolutionary trajectories of the sexes.