False promises: females spurn cheating males in a field cricket

Females commonly prefer to mate with males that provide greater material benefits, which they often select using correlated male signals. When females select higher-benefit males based on correlated signals, however, males can potentially deceive females by producing exaggerated signals of benefit quality. The handicap mechanism can prevent lower-quality males from producing exaggerated signals, but cannot prevent cheating by higher-quality males that choose to withhold the benefit, and this poses a major problem for the evolution of female choice based on direct benefits. In a field cricket, Gryllus lineaticeps, females receive seminal fluid products from males with preferred songs that increase their fecundity and lifespan. We tested the hypothesis that female behaviour penalizes males that provide lower-quality benefits. When females were paired with males that varied in benefit quality but had experimentally imposed average songs, they were less likely to re-mate with males that provided lower-quality benefits in the initial mating. This type of conditional female re-mating may be a widespread mechanism that penalizes males that cheat on direct benefits.     

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.     

Male mating constraints affect mutual mate choice: prudent male courting and sperm-limited females

Costs of sperm production may lead to prudence in male sperm allocation and also to male mate choice. Here, we develop a life history-based mutual mate choice model that takes into account the lost-opportunity costs for males from time out in sperm recovery and lets mate competition be determined by the prevailing mate choice strategies. We assume that high mating rate may potentially lead to sperm depletion in males, and that as a result, female reproduction may be limited by the availability of sperm. Increasing variation in male quality leads, in general, to increased selective mate choice by females, and vice versa. Lower-quality males may, however, gain access to more fecund higher-quality females by lowering their courting rate, thus increasing their sperm reserves. When faced with strong male competition for mates, low-quality males become less choosy, which leads to assortative mating for quality and an increased mating rate across all males. With assortative mating, the frequency of antagonistic interactions (sexual conflict) is reduced, allowing males to lower the time spent replenishing sperm reserves in order to increase mating rate. This in turn leads to lower sperm levels at mating and therefore could lead to negative effects on female fitness via sperm limitation.     

Superior sperm competitors sire higher-quality young

The evolution of polyandry remains controversial. This is because, unlike males, in many cases multiple mating by females does not increase fecundity and inevitably involves some costs. As a result, a large number of indirect benefit models have been proposed to explain polyandry. One of these, the good sperm hypothesis, posits that high-quality males are better sperm competitors and sire higher-quality offspring. Hence, by mating multiply, females produce offspring of superior quality. Despite being potentially widely applicable across species, this idea has received little attention. In a laboratory experiment with yellow dung flies ( Scathophaga stercoraria ) we found that males that were more successful in sperm competition also had offspring that developed faster. There was no relationship between paternal success in sperm competition and the ability of offspring to survive post-emergence starvation. Since faster development times are likely to be advantageous in this species, our data provide some support for polyandry evolving as a means of producing higher-quality offspring via sperm competition.     

Sex roles and mutual mate choice matter during mate sampling

The roles of females and males in mating competition and mate choice have lately proven more variable, between and within species, than previously thought. In nature, mating competition occurs during mate search and is expected to be regulated by the numbers of potential mates and same-sex competitors. Here, we present the first study to test how a temporal change in sex roles affects mating competition and mate choice during mate sampling. Our model system (the marine fish Gobiusculus flavescens) is uniquely suitable because of its change in sex roles, from conventional to reversed, over the breeding season. As predicted from sex role theory, courtship was typically initiated by males and terminated by females early in the breeding season. The opposite pattern was observed late in the season, at which time several females often simultaneously courted the same male. Mate-searching females visited more males early than late in the breeding season. Our study shows that mutual mate choice and mating competition can have profound effects on female and male behavior. Future work needs to consider the dynamic nature of mating competition and mate choice if we aim to fully understand sexual selection in the wild.     

The cost of dishonesty

The handicap principle states that stable biological signals must be honest and costly to produce. The cost of the signal should reflect the true quality of the signaller. Here, it is argued that honest signalling may be maintained although the used signals are not handicaps. A game theoretic model in the form of a game of signalling is presented: all the existing evolutionarily stable strategies (ESSs) are found. Honest and cheap signalling of male quality is shown to be evolutionarily stable if females divorce the mate if it turns out that he has cheated about his quality. However, for this ESS to apply, the cost of lost time must not be too great. The stability of the honest signalling is based on deceivers being prevented from spreading in the population because they suffer from a cost of divorce. Under some fairly strict conditions, a mixed polymorphism of dishonesty and honesty represents another possible ESS.     

Strategic choice handicaps when females seek high male net viability

We examine a strategic-choice handicap model in which males send costly signals to advertise their quality to females. Females are concerned with the net viability of the male with whom they mate, where net viability is a function of the male's quality and signal. We identify circumstances in which a signaling equilibrium would require high-quality males to send signals so much larger than those of lower-quality males (to deter mimicry by the latter) as to yield lower net viabilities for the former. This causes females to shun males who send large signals, ensuring that there is no signaling equilibrium.     

SEXUAL SELECTION, HONEST ADVERTISEMENT AND THE HANDICAP PRINCIPLE: REVIETWING THE EVIDENCE

• (i) To find out whether a mating preference could have initially evolved for adaptive reasons, one must determine whether the preferred trait could have provided useful information about mate quality at the time when the preference first arose.
• (ii) One way to do so is to determine whether the preference evolved before or after the preferred trait. If the preference evolved first, then it cannot initially have served an adaptive function in mate choice, rather it must have arisen by random drift, or as a pleiotropic consequence of selection acting on other aspects of individual perceptual abilities.
• (iii) A number of studies have shown that females exhibit a mating preference (e.g. for movement) in non-sexual contexts also, which suggests that it may have evolved for reasons unconnected to mate choice. In addition, phylogenetic analyses have revealed that in several cases, females of a certain taxon exhibit a preference for a male trait that is absent in a sister taxon and in outgroup taxa, and that this preference is shared by females of the sister taxon tacking the male trait. The principle of parsimony suggests that such a preference has been inherited from a common ancestor, while the preferred trait arose only once in the lineage exhibiting the trait, i.e. that the preference predates the attractive trait.
• (iii) While the above evidence indicates that females may possess ‘hidden’ preferences for male traits that are not exhibited by members of their own species, and that in at least some cases males have later evolved display traits that exploit preexisting preferences of this kind, there have been too few historical studies of preference evolution to allow one to assess the frequency of such exploitation. Moreover historical studies cannot provide strong support for the adaptive origin hypothesis, because coevolution of trait and preference (as opposed to exploitation of a pre-existing bias) is compatible with Fisherian models of preference evolution as well as with honest advertisement and the handicap principle. One can conclude only that while some mating preferences did not originally evolve for adaptive reasons, others may or may not have done so.
• (iv) To find out whether a mating preference is currently maintained by natural selection because the preferred trait provides useful information about mate quality, one must investigate the phenotypic and genotypic correlates of display, and the fitness consequences of mate choice.
• (v) A review of the published data reveals some support for the ideas of adaptive choice and honest advertisement. In a number of species, preferred display traits are correlated with putative measures of quality, and in a small proportion of these, there is evidence that reproductive success and/or offspring performance are higher for individuals mated to attractive partners. Very few studies report a failure to find any such correlates of display or any such benefits.
• (vi) While the above result suggests that honest advertisement does sometimes occur in extant populations (which does not necessarily imply that preferred traits originally evolved as reliable indicators of mate quality), the possibility of publication bias means that one cannot assess how widespread it is. More data is needed to remedy this problem, particularly regarding the fitness consequences of mate choice for females. Experimental rather than observational methods are the best means to gather such data. Studies that look for correlates of display, for instance, should rely on experimentally induced rather than natural variation in ‘quality’.
• (vii) The most common correlates of male display are age and dominance. The latter observation suggests that there may often be interactions between the processes of intersexual and intrasexual selection.
• (viii) There is considerably more evidence to support the idea of female choice for direct than for indirect benefits. At the same time, however, it is apparent that mating decisions are commonly influenced by more than one measure of quality, so that these two kinds of choice need not be independent. To assess this possibility will require more studies of the relationship between male attractiveness and offspring performance.
• (ix) Mate choice is frequently based on more than one display trait, and each trait is frequently influenced by more than one aspect of quality. ‘One quality, one trait’ views of honest advertisement are simplistic, and must be abandoned.
• (x) Honesty in sexual displays is sometimes maintained by cost (as in strategic handicap models) and sometimes, with approximately equal frequency, by physical necessity (as in revealing handicap models). In some cases, both mechanisms are involved in a single signalling system. To further distinguish between these possibilities will require experimental investigation of display cost, based on manipulation of display traits.

     

Incidental Sanctions and the Evolution of Direct Benefits

Recent research has shown that a variety of traits that increase male success in mating and sperm competition can impose costs on females, resulting in antagonistic coevolution between the sexes. Yet, in many animals, females are known to receive direct benefit from their mates, including many in which female multiple mating results in intense sperm competition among males. The most common explanation for the evolution of male‐provided direct benefits is pre‐mating female choice based on benefit quality. This explanation is insufficient, however, for those direct benefits that females cannot directly assess prior to mating. Given that intrasexual selection will often favor male traits that increase female mating costs, many types of direct benefits can thus be difficult to explain. In this paper, we review four additional hypotheses for the evolution of male‐provided direct benefits, and present a fifth hypothesis that has received little attention. This latter hypothesis proposes that selection often favors female reproductive tactics that are conditional upon the past costs and benefits of mating. These conditional female reproductive tactics should evolve because the quality of the benefit provided by a previous mate can change the costs and benefits of alternative reproductive decisions. Furthermore, many of the conditional reproductive tactics we might expect females to express should incidentally penalize males which provide lower quality direct benefits. These conditional reproductive tactics may thus play an important role in determining whether females incur costs or receive benefits from their mates. In addition to favoring the evolution of direct benefits, we argue that conditional female reproductive tactics may also favor reliable signaling of benefit quality. The most common explanation for reliable signaling is the handicap mechanism, which proposes that differential costs of signaling prevent low quality males from deceptively producing attractive signals. For direct benefits, however, there is a second type of deception: males which produce attractive signals and can afford to provide high quality direct benefits may choose to cheat on the advertised benefit. The handicap mechanism does nothing to prevent cheating on direct benefits by males which can afford to produce attractive signals, and is thus insufficient for ensuring reliable signaling of benefit quality. In contrast, conditional female reproductive tactics that incidentally penalize low benefit males should also penalize males which cheat on the benefits advertised by their signals.     

黄腹山鹪莺稳定的配偶关系限制雄性欺骗者

多数鸟类通过性特征限制在同性竞争和配偶选择中的“欺骗者”存在,与此相反,雀形目扇尾莺科部分物种表现出繁殖季节性特征消退的身体特征变化模式.在广州市南沙区通过“目字笼”对黄腹山鹪莺配偶关系稳定性的限制机制进行研究,发现虽然雌性个体到访原配个体和对照个体的次数几乎相同,但是雌性个体对原配雄性的单次选择时间明显长于对照雄性个体,总计选择时间也明显长于对照雄性个体.选择实验过程中,原配雄性的跳动次数明显高于对照个体雄性,以竖尾扑哧和鸣声恐吓等为代表的威慑行为次数也明显高于对照雄性个体.结果说明,雌性更青睐于原配个体,配对时间越长,忠诚度越高,而且原配雄性比入侵雄性个体表现出更高的活跃度和威慑行为.繁殖季节性特征消退的物种可以通过保持稳定的配偶关系以限制“欺骗者”存在.可以推测繁殖的巨大投入和雌性之间的同性竞争可能是产生这种配偶稳定性的主要原因.     

Can non‐directional male mating preferences facilitate honest female ornamentation?

Recent studies have demonstrated male mate choice for female ornaments in species without sex-role reversal. Despite these empirical findings, little is known about the adaptive dynamics of female signalling, in particular the evolution of male mating preferences. The evolution of traits that signal mate quality is more complex in females than in males because females usually provide the bulk of resources for the developing offspring. Here, we investigate the evolution of male mating preferences using a mathematical model which: (i) specifically accounts for the fact that females must trade-off resources invested in ornaments with reproduction; and (ii) allows male mating preferences to evolve a non-directional shape. The optimal adaptive strategy for males is to develop stabilizing mating preferences for female display traits to avoid females that either invests too many or too few resources in ornamentation. However, the evolutionary stability of this prediction is dependent upon the level of error made by females when allocating resources to either signal or fecundity.     

Males mate with females even after sperm depletion in the two-spotted spider mite

Generally, males increase their reproductive success by mating with as many females as possible, whereas females increase their reproductive success by choosing males who provide more direct and indirect benefits. The difference in reproductive strategy between the sexes creates intense competition among males for access to females, therefore males spend much energy and time for competition with rival males for their reproduction. However, if they do not need to engage themselves into male competition and females are in no short supply, how many females can a male mate with and fertilize? We address this question in the two-spotted spider mite, Tetranychus urticae Koch. In this study, we investigated how many females a young, virgin male mated in 3 h, and checked whether the mated females were fertilized. We found that on average males mated with 12–13 females (range: 5–25). As latency to next mating did not change with the number of matings, the males are predicted to engage in even more matings if the mating trial were continued beyond 3 h. Copulation durations decreased with the number of matings and typically after 11 copulations with females any further copulations did not lead to fertilization, suggesting that males continued to mate with females even after sperm depletion. We discuss why spider mite males continue to display mating and copulation behaviour even after their sperm is depleted.

     

Sexual selection and assortative mating: an experimental test

Mate choice and mate competition can both influence the evolution of sexual isolation between populations. Assortative mating may arise if traits and preferences diverge in step, and, alternatively, mate competition may counteract mating preferences and decrease assortative mating. Here, we examine potential assortative mating between populations of Drosophila pseudoobscura that have experimentally evolved under either increased (‘polyandry’) or decreased (‘monogamy’) sexual selection intensity for 100 generations. These populations have evolved differences in numerous traits, including a male signal and female preference traits. We use a two males: one female design, allowing both mate choice and competition to influence mating outcomes, to test for assortative mating between our populations. Mating latency shows subtle effects of male and female interactions, with females from the monogamous populations appearing reluctant to mate with males from the polyandrous populations. However, males from the polyandrous populations have a significantly higher probability of mating regardless of the female's population. Our results suggest that if populations differ in the intensity of sexual selection, effects on mate competition may overcome mate choice.     

Intersexual sibling interactions and male benevolence in a fig wasp

We studied interactions between males and females of the Australian pollinating fig wasp, Pleistodontes imperialis (Chalcidoidea, Agaonidae), in Ficus platypoda (Moraceae). As for many other fig wasps, all mating occurs within the confines of a syconium before females depart. We show that initially there is scramble competition between males for access to virgin females. During this time males excavated a small hole into a female's gall to mate through. These holes were just large enough for insemination, but not large enough for females to exit their galls. Males ignored mated females, and as virgin females became scarce males switched strategies and began to enlarge insemination holes until they were large enough for females to escape, showing that males enhance female fitness by means other than just mating. Syconia with experimentally reduced numbers of males had fewer liberated females, suggesting that female fitness is strongly affected by the number of males present. Females may be unable to escape their galls unassisted because of morphological adaptations to syconium founding. We argue that sex allocation should be affected not only by competition among males but also by intersexual interactions between siblings. This could potentially offset the strong female bias predicted by local mate competition. Copyright 2000 The Association for the Study of Animal Behaviour.     

Female discrimination thresholds frequently exceed local male display variation: implications for mate choice dynamics and sexual selection

Among the factors that can influence female mate choice decisions is the degree to which females differentiate among similar displays: as differences decrease, females are expected to eventually stop discriminating. This discrimination threshold, in conjunction with the magnitude of male trait variation females regularly encounter while making mate choice decisions, may have important consequences for sexual selection. If local display variation is above the discrimination threshold, female preferences should translate into higher mating success for the more attractive male. But if display variation is frequently below the threshold, the resulting increased pattern of random mating may obscure the existence of female mate choice. I investigated the interplay between female discrimination and male display variation in green treefrogs (Hyla cinerea) and found that call trait differences between nearest neighbour males were frequently smaller than what females are expected to discriminate. This finding has two important consequences for our understanding of sexual selection in the wild: first, low display variation should weaken the strength of selection on male display traits, but the direction of selection should mirror the one predicted from females choice trials. Second, caution is needed when interpreting data on realized mating success in the wild: a pattern of random mating with respect to male display traits does not always mean that female preferences are weak or that conditions are too challenging for females to express their preferences. Rather, insufficient display variation can generate the same pattern.     

A two-sex life history model of handicap signaling

The males of many species (such as peacocks) develop excessively large traits, which appear to interfere with their agility and hence survival probability. Moreover, it is also observed that females seem to prefer mating males with such clumsy traits. Zahavi (1975) proposed a handicap theory to explain this phenomenon, suggesting that this trait/preference interaction is a way in which strong males can signal their viability by yielding a handicap in terms of a clumsy trait size. This paper presents a two-sex model of selfish genes that generates this particular male-female interaction, and characterizes the conditions behind a handicap equilibrium. We first show the female dominance result of Bateman (1948) in this two-sex model, and then specify the relevant equilibrium conditions, including the incentive compatibility condition for females, the individual rationality condition for males, and the stability condition of population composition. Identifying these conditions helps us understand the various features of the searching/signaling of sex selection in evolution.     

Male size does not affect the strength of male mate choice for high-quality females in Drosophila melanogaster

Theory predicts that the strength of male mate choice should vary depending on male quality when higher-quality males receive greater fitness benefits from being choosy. This pattern extends to differences in male body size, with larger males often having stronger pre- and post-copulatory preferences than smaller males. We sought to determine whether large males and small males differ in the strength (or direction) of their preference for large, high-fecundity females using the fruit fly, Drosophila melanogaster. We measured male courtship preferences and mating duration to show that male body size had no impact on the strength of male mate choice; all males, regardless of their size, had equally strong preferences for large females. To understand the selective pressures shaping male mate choice in males of different sizes, we also measured the fitness benefits associated with preferring large females for both large and small males. Male body size did not affect the benefits that males received: large and small males were equally successful at mating with large females, received the same direct fitness benefits from mating with large females, and showed similar competitive fertilization success with large females. These findings provide insight into why the strength of male mate choice was not affected by male body size in this system. Our study highlights the importance of evaluating the benefits and costs of male mate choice across multiple males to predict when differences in male mate choice should occur.     

Male mate choice in fishes

Selection generally favours male competition for females, and female mate choice of males. If, however, females vary in quality, and if males are limited in the maximum number of females with which they can mate, then selection should also favour male mate choice. We report on male mate choice in two species of fishes with different mating systems: the threespine stickleback, which has male parental care, and the coho salmon, which has female parental care. In both species, males allocated their mating effort in direct proportion to female quality.     

Females of the lekking great snipe do not prefer males with whiter tails

A previous experimental study of great snipe, Gallinago media, has reported an effect on male mating success of the amount of white in their tails. That result is one of a very limited set of existing experimental results supporting a female mate preference for a morphological trait in animals. However, a later observational study did not find any correlation between amount of white and male mating success. If females sample a limited number of males, their preferences need not result in strong relationships between mating success and trait values in males, possibly explaining the failure to find the predicted correlation. Yet, females of lekking species are thought to have ample opportunities for mate sampling. To resolve these contrasting results, we present in this paper (1) a larger correlational study (several leks during 10 years) showing no relationship between male mating success and whiteness of tails (measured in several ways), and most importantly (2) evidence that individual females do not mate predominantly with males with very white tails among those males that each female samples. These results show that females do not prefer males with whiter tails as mates, within the contemporary natural variation in the trait. They also show that there is no sexual selection of the trait at present. This does not necessarily imply that white tails are not a sexually selected adaptation in males, but the mechanisms are likely to have been different from direct mate choice of whiter tails per se. Copyright 2000 The Association for the Study of Animal Behaviour.     

Truthful signalling, the heritability paradox, and the Malthusian equi-marginal principle

The article shows that heritable quality differentials are consistent with the Zahavi Handicap Principle (the Truthful Signalling Hypothesis (TSH)). Earlier analyses have assumed non-heritable quality. The crucial innovation is the Malthusian equi-marginal principle: under selection pressures the relative numbers of higher- and lower-quality organisms will change until, in equilibrium, not the average but the marginal levels of quality will be equalized. Assuming kin selection, each male maximizes his own reproductive success and signals until the marginal value of more signalling is zero. We further require evolutionary stability; displacements to higher or lower population sizes must be restored to equilibrium. The article proposes an alternative to Fisher's [1958. The Genetical Theory of Natural Selection. Dover Publications, Inc., New York [Original publication 1929]] and Hamilton and Zuk's [1982. Heritable true fitness and bright birds: a role for parasites? Science 218, 384-387] suggestions. The model is solvable for ranges of parameters that constitute the stable region. We particularly consider the unit signalling costs of the high- and low-quality males, where it has been widely believed that for a TSH equilibrium the former must be lower than the latter. This article confirms our earlier result that this is not a necessary condition for a truthful signalling equilibrium, though the unit signalling costs of the high-quality males cannot be too much larger.