Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

Females prefer males producing a high-rate song with shorter timbal–stridulatory sound intervals in a cicada species

Uncovering mate choice and factors that lead to the choice are very important to understanding sexual selection in evolutionary change. Cicadas are known for their loud sounds produced by males using the timbals. However, males in certain cicada species emit 2 kinds of sounds using respectively timbals and stridulatory organs, and females may produce their own sounds to respond to males. What has never been considered is the mate choice in such cicada species. Here, we investigate the sexual selection and potential impact of predation pressure on mate choice in the cicada Subpsaltria yangi Chen. It possesses stridulatory sound-producing organs in both sexes in addition to the timbals in males. Results show that males producing calling songs with shorter timbal–stridulatory sound intervals and a higher call rate achieved greater mating success. No morphological traits were found to be correlated with mating success in both sexes, suggesting neither males nor females display mate preference for the opposite sex based on morphological traits. Males do not discriminate among responding females during mate searching, which may be due to the high energy costs associated with their unusual mate-seeking activity and the male-biased predation pressure. Females generally mate once but a minority of them re-mated after oviposition which, combined with the desirable acoustic traits of males, suggest females may maximize their reproductive success by choosing a high-quality male in the first place. This study contributes to our understanding mechanisms of sexual selection in cicadas and other insects suffering selective pressure from predators.     

Competitive PCR reveals the complexity of postcopulatory sexual selection in Teleogryllus commodus

The outcome of mate choice depends on complex interactions between males and females both before and after copulation. Although the competition between males for access to mates and premating choice by females are relatively well understood, the nature of interactions between cryptic female choice and male sperm competition within the female reproductive tract is less clear. Understanding the complexity of postcopulatory sexual selection requires an understanding of how anatomy, physiology and behaviour mediate sperm transfer and storage within multiply mated females. Here we use a newly developed molecular technique to directly quantify mixed sperm stores in multiple mating females of the black field cricket, Teleogryllus commodus. In this species, female postcopulatory choice is easily observed and manipulated as females delay the removal of the spermatophore in favour of preferred males. Using twice‐mated females, we find that the proportion of sperm in the spermatheca attributed to the second male to mate with a female (S₂) increases linearly with the time of spermatophore attachment. Moreover, we show that the insemination success of a male increases with its attractiveness and decreases with the size of the female. The effect of male attractiveness in this context suggests a previously unknown episode of mate choice in this species that reinforces the sexual selection imposed by premating choice and conflicts with the outcome of postmating male harassment. Our results provide some of the clearest evidence yet for how sperm transfer and displacement in multiply mated females can lead directly to cryptic female choice, and that three distinct periods of sexual selection operate in black field crickets.     

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.     

The relative importance of intra- and intersexual selection on human male sexually dimorphic traits

Recent evidence suggests that in sexual selection on human males, intrasexual competition plays a larger role than female choice. In a sample of men (N?=?164), we sought to provide further evidence on the effects of men's physical dominance and sexual attractiveness on mating success and hence in sexual selection. Objective measures and subjective ratings of male sexually dimorphic traits purportedly under sexual selection (height, vocal and facial masculinity, upper body size from 3D scans, physical strength, and baseline testosterone) and observer perceptions of physical dominance and sexual attractiveness based on self-presentation video recordings were assessed and associated with mating success (sociosexual behaviour and number of potential conceptions) in a partly longitudinal design. Results from structural equation models and selection analyses revealed that physical dominance, but not sexual attractiveness, predicted mating success. Physical dominance mediated associations of upper body size, physical strength, as well as vocal and facial physical dominance and attractiveness with mating success. These findings thus suggest a greater importance of intrasexual competition than female choice in human male sexual selection.     

Operational sex ratio and resource defence as predictors of the mating system in European bitterling

Operational sex ratio (OSR), the ratio of sexually active males to fertilizable females in a population, plays a central role in the theory of mating systems by predicting that the intensity of male–male competition and the degree of sexual selection increases as the OSR becomes increasingly male biased. At high values of OSR, however, resource defence theory predicts the breakdown of territoriality and a shift towards scramble competition with a decrease in sexual selection. The direction that correlations between OSR and resource competition and variance in mating success will take depends on the biology of the species of interest. We investigated the effects of male population density and male‐biased operational sex ratio on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus . This species spawns inside living unioneid mussels. Large males defended territories, were aggressive towards conspecifics under equal sex ratios and monopolized pair spawnings with females. The mating tactic, however, changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. This change in male behaviour from pair to group spawning has two ramifications for sexual selection. The intensity of sexual selection and variance in male mating success decrease, and the form of sexual competition changes from resource‐ to sperm competition. Thus, the use of alternative mating tactics renders the OSR unable to predict the direction of resource competition and variance in male mating success at high densities.     

Song and Sperm in Crickets: A Trade‐off between Pre‐ and Post‐copulatory Traits or Phenotype‐Linked Fertility?

When females mate multiply (polyandry) both pre‐ and post‐copulatory sexual selection can occur. Sperm competition theory predicts there should be a trade‐off between investment in attracting mates and investment in ejaculate quality. In contrast, the phenotype‐linked fertility hypothesis predicts a positive relationship should exist between investment in attracting mates and investment in ejaculate quality. Given the need to understand how pre‐ and post‐copulatory sexual selection interacts, we investigated the relationship between secondary sexual traits and ejaculate quality using the European house cricket, Acheta domesticus. Although we found no direct relationship between cricket secondary sexual signals and ejaculate quality, variation in ejaculate quality was dependent on male body weight and mating latency: the lightest males produced twice as many sperm as the heaviest males but took longer to mate with females. Our findings are consistent with current theoretical models of sperm competition. Given light males may have lower mating success than heavy males because females take longer to mate with them in no‐choice tests, light males may be exhibiting an alternative reproductive tactic by providing females with more living sperm. Together, our findings suggest that the fitness of heavy males may depend on pre‐copulatory sexual selection, while the fitness of light males may depend on post‐copulatory fertilization success.     

Evolutionary reduction in testes size and competitive fertilization success in response to the experimental removal of sexual selection in dung beetles

Sexual selection is thought to favor the evolution of secondary sexual traits in males that contribute to mating success. In species where females mate with more than one male, sexual selection also continues after copulation in the form of sperm competition and cryptic female choice. Theory suggests that sperm competition should favor traits such as testes size and sperm production that increase a male's competitive fertilization success. Studies of experimental evolution offer a powerful approach for assessing evolutionary responses to variation in sexual selection pressures. Here we removed sexual selection by enforcing monogamy on replicate lines of a naturally polygamous horned beetle, Onthophagus taurus, and monitoring male investment in their testes for 21 generations. Testes size decreased in monogamous lines relative to lines in which sexual selection was allowed to continue. Differences in testes size were dependent on selection history and not breeding regime. Males from polygamous lines also had a competitive fertilization advantage when in sperm competition with males from monogamous lines. Females from polygamous lines produced sons in better condition, and those from monogamous lines increased their sons condition by mating polygamously. Rather than being costly for females, multiple mating appears to provide females with direct and/or indirect benefits. Neither body size nor horn size diverged between our monogamous and polygamous lines. Our data show that sperm competition does drive the evolution of testes size in onthophagine beetles, and provide general support for sperm competition theory.     

Resource availability,mating opportunity and sexual selection intensity influence the expression of male alternative reproductive tactics

The expression of alternative reproductive tactics can be plastic and occur simultaneously depending on cues that vary spatially or temporally. For example, variation in resources and sexual selection intensity is expected to influence the pay‐off of each tactic and shape the decision of which tactic to employ. Males of the nuptial gift‐giving spider Pisaura mirabilis can adopt three tactics: offering a genuine prey gift, a ‘worthless’ non‐nutritious gift or no gift. We hypothesized that resources and/or male body condition, and mating opportunity and sexual selection intensity, vary over the course of the mating season to shape the co‐existence of alternative traits. We measured these variables in the field over two seasons, to investigate the predictions that as the mating season progresses, (i) males become more likely to employ a gift‐giving tactic, and (ii) the likelihood of switching from worthless to genuine gifts increases. Prey availability increased over the season and co‐varied with the propensity of males to employ the gift‐giving tactic, but we found no support for condition‐dependent gift giving. Males responded to an increase in female availability by increasing their mating effort (gift production). Furthermore, the frequency of genuine gift use increased with sexual selection intensity, consistent with the assumption that sperm competition intensity increases with time. Our results suggest that the frequency of alternative tactics is shaped by seasonal changes in ecological factors and sexual selection. This leads to relaxed selection for the gift‐giving tactic early in the season when females are less choosy and resources more scarce, and increased selection for genuine gifts later in the season driven by mating opportunity and risk of sperm competition.     

Alternative reproductive tactics in male freshwater fish influence the accuracy of species recognition

Sexual conflict can result in coercive mating. Because males bear low costs of heterospecific mating, coercive males may engage in misdirected mating attempts toward heterospecific females. In contrast, sexual selection through consensual mate choice can cause mate recognition cues among species to diverge, leading to more accurate species recognition. Some species show both coercive mating and mate choice‐associated courtship behaviors as male alternative reproductive tactics. We hypothesized that if the selection pressures on each tactic differ, then the accuracy of species recognition would also change depending on the mating tactic adopted. We tested this hypothesis in the guppy (Poecilia reticulata) and mosquitofish (Gambusia affinis) by a series of choice experiments. Poecilia reticulata and G. affinis males both showed imperfect species recognition and directed all components of mating behavior toward heterospecific females. They tended to direct courtship displays more frequently toward conspecific than heterospecific females. With male P. reticulata, however, accurate species recognition disappeared when they attempted coercive copulation: they directed coercions more frequently toward heterospecific females. We also found that heterospecific sexual interaction had little effect on the fecundity of gravid females, which suggests that prepregnancy interactions likely underpin the exclusion of G. affinis by P. reticulata in our region.     

Female Remating Behavior in a Lekking Moth

In polyandrous species, male reproductive success will at least partly be determined by males' success in sperm competition. To understand the potential for post‐mating sexual selection, it is therefore important to assess the extent of female remating. In the lekking moth Achroia grisella, male mating success is strongly determined by female choice based on the attractiveness of male ultrasonic songs. Although observations have indicated that some females will remate, only little is known about the level of sperm competition. In many species, females are more likely to remate if their first mating involved an already mated male than if the first male was virgin. Potentially, this is because mated males are less well able to provide an adequate sperm supply, nutrients, or substances inhibiting female remating. This phenomenon will effectively reduce the strength of pre‐copulatory sexual selection because attractive males with high mating success will be more susceptible to sperm competition. We therefore performed an experiment designed both to provide a more precise estimate of female remating probability and simultaneously to test the hypothesis that female remating is influenced by male mating history. Overall, approximately one of five females remated with a second male. Yet, although females mated to non‐virgin males were somewhat more prone to remate, the effect of male mating history was not significant. The results revealed, however, that heavier females were more likely to remate. Furthermore, we found that females' second copulations were longer, suggesting that, in accordance with theory, males may invest more sperm in situations with an elevated risk of sperm competition.     

Sexual dimorphism in epicuticular compounds despite similar sexual selection in sex role‐reversed seed beetles

Sexual selection imposed by mating preferences is often implicated in the evolution of both sexual dimorphism and divergence between species in signalling traits. Epicuticular compounds (ECs) are important signalling traits in insects and show extensive variability among and within taxa. Here, we investigate whether variation in the multivariate EC profiles of two sex role‐reversed beetle species, Megabruchidius dorsalis and Megabruchidius tonkineus, predicts mate attractiveness and mating success in males and females. The two species had highly distinct EC profiles and both showed significant sexual dimorphism in ECs. Age and mating status in both species were also distinguishable by EC profile. Males and females of both species showed significant association between their EC profile and attractiveness, measured both as latency to mating and as success in mate‐choice trials. Remarkably, the major multivariate vector describing attractiveness was correlated in both species, both sexes, and in both choice and no‐choice experiments such that increased attractiveness was in all cases associated with a similar multivariate modification of EC composition. Furthermore, in both sexes this vector of attractiveness was associated with more male‐like EC profiles, as well as those characterizing younger and nonvirgin individuals, which might reflect a general preference for individuals of high condition in both sexes. Despite significant sexual selection on EC composition, however, we found no support for the proposition that sexual selection is responsible for divergence in ECs between these species.     

Beauty and the beast: mechanisms of sexual selection in humans

Literature in evolutionary psychology suggests that mate choice has been the primary mechanism of sexual selection in humans, but this conclusion conforms neither to theoretical predictions nor available evidence. Contests override other mechanisms of sexual selection; that is, when individuals can exclude their competitors by force or threat of force, mate choice, sperm competition, and other mechanisms are impossible. Mates are easier to monopolize in two dimensional mating environments, such as land, than in three-dimensional environments, such as air, water, and trees. Thus, two-dimensional mating environments may tend to favor the evolution of contests. The two-dimensionality of the human mating environment, along with phylogeny, the spatial and temporal clustering of mates and competitors, and anatomical considerations, predict that contest competition should have been the primary mechanism of sexual selection in men. A functional analysis supports this prediction. Men's traits are better designed for contest competition than for other sexual selection mechanisms; size, muscularity, strength, aggression, and the manufacture and use of weapons probably helped ancestral males win contests directly, and deep voices and facial hair signal dominance more effectively than they increase attractiveness. However, male monopolization of females was imperfect, and female mate choice, sperm competition, and sexual coercion also likely shaped men's traits. In contrast, male mate choice was probably central in women's mating competition because ancestral females could not constrain the choices of larger and more aggressive males through force, and attractive women could obtain greater male investment. Neotenous female features and body fat deposition on the breasts and hips appear to have been shaped by male mate choice.     

Precopulatory but not postcopulatory male reproductive traits diverge in response to mating system manipulation in Drosophila melanogaster

Competition between males creates potential for pre‐ and postcopulatory sexual selection and conflict. Theory predicts that males facing risk of sperm competition should evolve traits to secure their reproductive success. If those traits are costly to females, the evolution of such traits may also increase conflict between the sexes. Conversely, under the absence of sperm competition, one expectation is for selection on male competitive traits to relax thereby also relaxing sexual conflict. Experimental evolution studies are a powerful tool to test this expectation. Studies in multiple insect species have yielded mixed and partially conflicting results. In this study, we evaluated male competitive traits and male effects on female costs of mating in Drosophila melanogaster after replicate lines evolved for more than 50 generations either under enforced monogamy or sustained polygamy, thus manipulating the extent of intrasexual competition between males. We found that in a setting where males competed directly with a rival male for access to a female and fertilization of her ova polygamous males had superior reproductive success compared to monogamous males. When comparing reproductive success solely in double mating standard sperm competition assays, however, we found no difference in male sperm defense competitiveness between the different selection regimes. Instead, we found monogamous males to be inferior in precopulatory competition, which indicates that in our system, enforced monogamy relaxed selection on traits important in precopulatory rather than postcopulatory competition. We discuss our findings in the context of findings from previous experimental evolution studies in Drosophila ssp. and other invertebrate species.     

A novel method of comparing mating success and survival reveals similar sexual and viability selection for mobility traits in female tree crickets

The relationship between sexual and viability selection in females is necessarily different than that in males, as investment in sexual traits potentially comes at the expense of both fecundity and survival. Accordingly, females do not usually invest in sexually selected traits. However, direct benefits obtained from mating, such as nuptial gifts, may encourage competition among females and subsidize investment into sexually selected traits. We compared sexual and viability selection on female tree crickets Oecanthus nigricornis, a species where females mate frequently to obtain nuptial gifts and sexual selection on females is likely. If male choice determines female mating success in this species, we expect sexual selection for fecundity traits, as males of many species prefer more fecund females. Alternatively, intrasexual scramble or combat competition on females may select for larger jumping legs or wider heads (respectively). We estimated mating success in wild caught crickets using microsatellite analysis of stored sperm and estimated relative viability by comparing surviving female O. nigricornis to those captured by a common wasp predator. In support of the scramble competition hypothesis, we found sexual selection for females with larger hind legs and narrower heads. We also found stabilizing viability selection for intermediate head width and hind leg size. As predicted, traits under viability and sexual selection were very similar, and the direction of that selection was not opposing. However, because the shape of sexual and viability selection differs, these episodes of selection may favour slightly different trait sizes.     

Male morphology,performance and female mate choice of a swarming insect

1. Females of many species select mates based on important morphological and performance traits. This behaviour likely facilitates reproductive success thus exhibiting sexual selection. Most such studies have evaluated a single morphological variable, and only a minority of them studies the effects of behaviour and performance (functional capacity: Irschick et al., Evolutionary Ecology Research, 10 , 177–196, 2008) at all.
2. This study compares male morphological and performance traits differing in three variables that may correlate with fitness: condition index, flight ascent speed and resistance to torpor in relation to male mating success in the parasitoid wasp species Alabagrus texanus (Braconidae), a species where males swarm about emerging virgin females that display both choosy and non-choosy behavioural phenotypes.
3. Males that successfully mated with choosy females exhibited higher condition indices and somewhat stronger resistance to torpor than other males. Conversely, males that mated with non-choosy females did not differ in any trait from other males we measured. Early-arriving males did not have higher condition indices or greater mating success than other males.
4. Thus, both morphological and performance traits contributed to male success, which acted through female choice, indicating a role for sexual selection. Patterns of choice further differed among females, independent of male traits.

     

Sperm competition and small size advantage for males of the golden orb‐web spider Nephila edulis

Sexual selection, through female choice and/or male–male competition, has influenced the nature and direction of sexual size dimorphism in numerous species. However, few studies have examined the influence of sperm competition on size dimorphism. The orb‐web spider Nephila edulis has a polygamous mating system and extreme size dimorphism. Additionally, the frequency distribution of male body size is extremely skewed with most males being small and few large. The duration of copulation, male size and sexual cannibalism have been identified as the significant factors determining patterns of sperm precedence in spiders. In double mating trials, females were assigned to three treatments: either they mated once with both males or the first or the second male was allowed to mate twice. Paternity was strongly associated with the duration of copulation, independent of mating order. Males that were allowed to mate twice not only doubled the duration of copulation but also their paternity. Small males had a clear mating advantage, they copulated longer than large males and fertilized more eggs. Males of different sizes used different tactics to mate. Large males were more likely to mate through a hole they cut into the web, whereas small males approached the female directly. Furthermore, small males usually mated at their first attempt but large males required several attempts before mating took place. There was no obvious female reaction towards males of different sizes.     

Sexual selection in hermit crabs: a review and outlines of future research

The information currently available on sexual selection in hermit crabs is reviewed to identify the role of males and females before, during and after mating. According to this information, possible mechanisms of male–male competition, female choice and/or sexual conflict are suggested. Important male components that may affect mating success include dragging the female shell, rotations of the female's shell and male cheliped palpations, and male size and/or shell characteristics (species and size). Possible female determinants of male mating/fertilization success include size (as an indicator of egg production capacity), signalling of sexual receptivity to males, delay from mate guarding to copulation and mating duration. Avenues for deeper exploration in males include the role of the number and morphometry of male sexual tubes during sperm transfer, and whether ejaculate size and sperm number can be adjusted with variable situations of sperm competition intensity and risk. In females it would be interesting to investigate the chemical and behavioural mechanisms affecting spermatophore breakage for sperm release and the variable duration from sperm transfer to spawning. Given these possibilities, and that sperm is externally deposited on the female's body but inside her shell (except for those species that do not use shells, e.g. Birgus , or species where shells are rather small and do not cover the body totally, e.g. Parapagurus ), we conclude that hermit crabs are unique subjects for separating male and female effects, particularly with respect to the applicability of current ideas in sexual selection such as female choice and sexual conflict. Some practical ideas are provided to disentangle both hypotheses using these animals.     

Correlates of reproductive success within alternative mating tactics of the common shrew

Male common shrews (Sorex araneus) adopt two discrete matingtactics. The most successful males, in terms of number of offspringfathered, are those that establish large overlapping home rangesin areas of high female density early in the breeding season.An alternative, less successful mating tactic is to travel longdistances in search of mating opportunities. This study is aninvestigation of correlates of reproductive success for malesadopting these different mating tactics. Reproductive successunder natural conditions was assessed using DNA fingerprinting,and survival of offspring was monitored in the field. The numberof offspring fathered by males with overlapping home rangeswas positively correlated with the number of female ranges overlappedduring the breeding season and with testes mass. The numberof offspring fathered by males that made long-distance movementswas positively correlated with their epididymal sperm counts.It is argued that competitively superior (overlapping) malesachieve high reproductive success by competing to maximize thenumber of females inseminated, whereas those adopting an alternativemating tactic instead compete largely via sperm competition,aiming to maximize insemination success with any particularfemale. There was no significant difference in the fluctuatingasymmetry (FA) of males adopting different mating tactics (FAwas measured as the difference in length of the paired lateralscent glands). Fluctuating asymmetry was not related to thenumber of offspring fathered by males adopting either matingtactic, but was significantly correlated with the proportionof male offspring fathered that survived to sexual maturity.Although apparently not correlated with mating success in thisspecies, FA may reflect some aspect of genetic quality thataffects offspring survival. [Behav Ecol 7: 334–340 (1996)]