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.     

Male mate choice in the chameleon grasshopper (Kosciuscola tristis)

In many species, males can increase their fitness by mating with the highest quality females. Female quality can be indicated by cues, such as body size, age and mating status. In the alpine grasshopper Kosciuscola tristis, males can be found riding on subadult females early in the season, and as the season progresses, males engage in fights over ovipositing females. These observations suggest that males may be competing for females that are either unmated (early season) or sperm‐depleted (late season). We thus hypothesised that male K. tristis may be choosy in relation to female mating status, and specifically, we predicted that males prefer females that are unmated. We conducted behavioural experiments in which males were given the choice of two females, one mated and one unmated. Contrary to our prediction, males did not mate preferentially with unmated females. However, copulation duration with unmated females was, on average, 24 times the length of copulation with mated females. While female K. tristis can reject mates, we did not observe any evidence of overt female choice during our trials. Females may gain additional benefits from mating multiply and may therefore not readily reject males. While our experiment cannot definitively disentangle female from male control over copulation duration, we suggest that males choose to invest more time in copula with unmated females, perhaps for paternity assurance, and that male mate assessment occurs during copulation rather than beforehand.     

The evolution of male mate choice in insects: a synthesis of ideas and evidence

Mate choice by males has been recognized at least since Darwin's time, but its phylogenetic distribution and effect on the evolution of female phenotypes remain poorly known. Moreover, the relative importance of factors thought to underlie the evolution of male mate choice (especially parental investment and mate quality variance) is still unresolved. Here I synthesize the empirical evidence and theory pertaining to the evolution of male mate choice and sex role reversal in insects, and examine the potential for male mating preferences to generate sexual selection on female phenotypes. Although male mate choice has received relatively little empirical study, the available evidence suggests that it is widespread among insects (and other animals). In addition to 'precopulatory' male mate choice, some insects exhibit 'cryptic' male mate choice, varying the amount of resources allocated to mating on the basis of female mate quality. As predicted by theory, the most commonly observed male mating preferences are those that tend to maximize a male's expected fertilization success from each mating. Such preferences tend to favour female phenotypes associated with high fecundity or reduced sperm competition intensity. Among insect species there is wide variation in mechanisms used by males to assess female mate quality, some of which (e.g. probing, antennating or repeatedly mounting the female) may be difficult to distinguish from copulatory courtship. According to theory, selection for male choosiness is an increasing function of mate quality variance and those reproductive costs that reduce, with each mating, the number of subsequent matings that a male can perform ('mating investment') Conversely, choosiness is constrained by the costs of mate search and assessment, in combination with the accuracy of assessment of potential mates and of the distribution of mate qualities. Stronger selection for male choosiness may also be expected in systems where female fitness increases with each copulation than in systems where female fitness peaks at a small number of matings. This theoretical framework is consistent with most of the empirical evidence. Furthermore, a variety of observed male mating preferences have the potential to exert sexual selection on female phenotypes. However, because male insects typically choose females based on phenotypic indicators of fecundity such as body size, and these are usually amenable to direct visual or tactile assessment, male mate choice often tends to reinforce stronger vectors of fecundity or viability selection, and seldom results in the evolution of female display traits. Research on orthopterans has shown that complete sex role reversal (i.e. males choosy, females competitive) can occur when male parental investment limits female fecundity and reduces the potential rate of reproduction of males sufficiently to produce a female-biased operational sex ratio. By contrast, many systems exhibiting partial sex role reversal (i.e. males choosy and competitive) are not associated with elevated levels of male parental investment, reduced male reproductive rates, or reduced male bias in the operational sex ratio. Instead, large female mate quality variance resulting from factors such as strong last-male sperm precedence or large variance in female fecundity may select for both male choosiness and competitiveness in such systems. Thus, partial and complete sex role reversal do not merely represent different points along a continuum of increasing male parental investment, but may evolve via different evolutionary pathways.     

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.     

Sex-role reversal revisited: choosy females and ornamented, competitive males in a pipefish

In the pipefish Syngnathus typhle sex roles are reversed, thatis, females compete more intensely than males over mates. However,competition over mates among individuals of one sex does notnecessarily prevent members of that same sex from being choosy,and choosiness in the other sex does not prevent competitionwithin it. In an experiment we allowed a female pipefish tochoose freely between two males, after which we released themales and let the three interact. Comparisons with earlier resultsshow that both sexes courted partners and competed with consexuals.However, females courted more often than did males, and courtshipwas more frequent in treatments involving large individualsthan in treatments with small individuals. Males competed amongthemselves for access to mates but for a shorter duration thanfemales in the same situation. Males displayed an ornament towardsfemales but not to males during mating competition. Females,however, used their ornament in both contexts. Females did notalways mate with the male of their previously made choice, whichwe interpret as females being constrained by male-male competition,male motivation to mate, or both. Thus, in this sex-role reversedspecies, mate choice in the more competitive sex may be circumventedand even overruled by mate competition and mating willingnessin the least competitive sex. Hence, sex roles should not beconsidered as sexes being either choosy or competitive but ratherthat males and females may exhibit different combinations ofchoice and competition.     

Complex Courtship Behavior in the Striped Ground Cricket, Allonemobius socius (Orthoptera: Gryllidae): Does Social Environment Affect Male and Female Behavior?

Complex courtship in the striped ground cricket, Allonemobius socius, involves a series of behaviors alternating between the sexes. We examined if complex courtship allows either or both genders to evaluate their mate and how mating behavior changes in different social environments. While complex courtship may allow discrimination by both sexes, here only females exhibited a preference. Males did not alter their courtship behavior or change spermatophore size for different size females. In contrast, females initiated copulation more quickly with bigger males possessing bigger spermatophores. In a different social environment (additional male, female, or both), males were less likely to omit courtship songs and female discrimination of mates changed. The distinct differences in male and female behavior suggest that subtle changes in social environment can have important consequences in structuring courtship and mating behavior.     

Detection of female mating status using chemical signals and cues

Males of many species choose their mate according to the female's reproductive status, and there is now increasing evidence that male fitness can depend on this discrimination. However, females will also aim to regulate their mating activity so as to maximize their own fitness. As such, both sexes may attempt to dictate the frequency and timing of female mating, reflecting the potentially different costs of female signaling to both sexes. Here, I review evidence that chemical cues and signals are used widely by males to discriminate between mated and unmated females, and explore the mechanisms by which female odour changes post‐mating. There is substantial empirical evidence that mated and unmated females differ in their chemical profile, and that this variation provides males with information on a female's mating status. Although there appears to be large variation among species regarding the mechanisms by which female odour is altered post‐mating, the transfer of male substances to females during or subsequent to copulation appear to play a major role. This transfer of substances by males may be part of their strategy to suppress reproduction by competing males, particularly in species where females mate more than once.     

Mate sampling and choosiness in the sand goby

To date, mate choice studies have mostly focused on establishing which mates are chosen or how the choices are performed. Here, we combined these two approaches by empirically testing how latency to mate is affected by various search costs, variation in mate quality and female quality in the sand goby (Pomatoschistus minutus). Our results show that females adjust their mating behaviour according to the costs and benefits of the choice situation. Specifically, they mated sooner when access to males was delayed and when the presence of other females presented a mate sampling cost. We also found a positive link between size variation among potential mating partners and spawning delay in some (but not all) experimental conditions. By contrast, we did not find the number of available males or the females'' own body size (‘quality’) to affect mating latency. Finally, female mating behaviour varied significantly between years. These findings are notable for demonstrating that (i) mate sampling time is particularly sensitive to costs and, to a lesser degree, to variation among mate candidates, (ii) females'' mating behaviour is sensitive to qualitative rather than to quantitative variation in their environment, and (iii) a snapshot view may describe mate sampling behaviour unreliably.     

Do males choose their mates in the lekking moth Achroia grisella? Influence of female body mass and male reproductive status on male mate choice

Lekking males aggregate to attract females and contribute solely to egg fertilization, without any further parental care. Evolutionary theory therefore predicts them to be nonchoosy toward their mates, because any lost mating opportunities would outweigh the benefits associated with such preferences. Nevertheless, due to time costs, the production of energetically costly sexual displays, and potential sperm limitation, the mating effort of lekking males is often considerable. These factors, combined with the fact that many females of varying quality are likely to visit leks, could favor the evolution of male mate preferences. Here, we show that males of the lekking lesser wax moth, Achroia grisella, were indeed more likely to mate with heavier females in choice experiments, even at their virgin mating (i.e., when their reproductive resources have not yet been depleted by previous matings). This differential female mating success could not be attributed to female behavior as heavy and light females showed similar motivation to mate (i.e., latency to approach the males) and time to copulate. Males seem to benefit from mating with heavier females, as fecundity positively correlated with female mass. This new empirical evidence shows that male mate choice may have been underestimated in lekking species.     

VARIATION IN MATE CHOICE AND MATING PREFERENCES: A REVIEW OF CAUSES AND CONSEQUENCES

The aim of this review is to consider variation in mating p among females. We define mating p as the sensory and behavioural properties that influence the propensity of individuals to mate with certain phenotypes. Two properties of mating p can be distinguished: (i) ‘preference functions’–the order with which an individual ranks prospective mates and (2)‘choosiness’ -the effort an individual is prepared to invest in mate assessment. Patterns of mate choices can be altered by changing the costs of choosiness without altering the preference function. We discuss why it is important to study variation in female mating behaviour and identify five main areas of interest: Variation in mating p and costs of choosiness could (i) influence the rate and direction of evolution by sexual selection, (2) provide information about the evolutionary history of female p, (3) help explain inter-specific differences in the evolution of secondary sexual characteristics, (4) provide information about the level of benefits gained from mate choice, (5) provide information about the underlying mechanisms of mate choice. Variation in mate choice could be due to variability in preference functions, degree of choosiness, or both, and may arise due to genetic differences, developmental trajectories or proximate environmental factors. We review the evidence for genetic variation from genetic studies of heritability and also from data on the repeatability of mate-choice decisions (which can provide information about the upper limits to heritability). There can be problems in interpreting patterns of mate choice in terms of variation in mating p and we illustrate two main points. First, some factors can lead to mate choice patterns that mimic heritable variation in p and secondly other factors may obscure heritable p. These factors are divided into three overlapping classes, environmental, social and the effect of the female phenotype. The environmental factors discussed include predation risk and the costs of sampling; the social factors discussed include the effect of male–male interactions as well as female competition. We review the literature which presents data on how females sample males and discuss the number of cues females use. We conclude that sexual-selection studies have paid far less attention to variation among females than to variation among males, and that there is still much to learn about how females choose males and why different females make different choices. We suggest a number of possible lines for future research.     

SEX DIFFERENCES IN MATE RECOGNITION AND CONSPECIFIC PREFERENCE IN SPECIES WITH MUTUAL MATE CHOICE

Sexual isolation is often assumed to arise because choosy females recognize and reject heterospecific males as mates. Yet in taxa in which both males and females are choosy, males might also recognize and reject heterospecific females. Here, we asked about the relative contribution of the sexes to the strong sexual isolation found in limnetic–benthic species pairs of threespine sticklebacks, which show mutual mate choice. We asked whether males and females of the two species recognize conspecifics and also prefer to mate with them. We found evidence for mate recognition by both sexes but only females prefer conspecifics. The nature of male courtship depended on which species of female they were courting, indicating that males recognized conspecific females and differentiated them from heterospecifics. However, males courted both species of females with equal vigor and changed courtship in a manner that would increase the chance of mating with heterospecifics. Females both recognized conspecifics and strongly preferred them. They responded very little to heterospecific male courtship and almost never mated with them. Therefore, males are likely to undermine sexual isolation, but females uphold it. Despite mutual mate choice and mate recognition in both sexes, females are primarily responsible for sexual isolation in these taxa.     

Effects of parasitic infection on mate sampling by female wild turkeys (Meleagris gallopavo): should infected females be more or less choosy?

Investigations of parasite-mediated sexual selection have concentratedon the effects of parasites on males. Differences in femalesusceptibility to parasitic infection may also cause variationin reproductive behavior. I propose two alternative hypothesesto explain how infected females may alter their mate samplingbehavior. In the first hypothesis, infected females sample fewerprospective mates because chronic parasitic infection imposesenergetic costs that limit the time and calories that a femalecan expend in mate searching. A novel alternative hypothesisis that females recognize their own susceptibility to infectionand thus invest more time searching for a male phenotype thatindicates he offers genes complementary to her genome. In recombination,these good genes would allow her offspring to better resistparasites despite their mother's susceptibility. I examinedthe mate sampling behavior of experimentally infected wild turkeyhens when presented with an array of males, and compared themto control hens. Infected females did not invest more time assessingindividuals, did not wait longer to choose a male, nor werethey less likely to solicit during the trial. They did differfrom control females in that they visited more males beforesoliciting copulation and exhibited different preference functionsfor snood length. These results suggest that females are notso energetically restricted by latent coccidia infection thatthey must hurry to find a mate. Instead, it appears that infectedfemales assess a larger set of males as prospective mates, perhapsto increase the opportunity to obtain complementary genes forparasite resistance.     

Female mate choice tactics in a resource-based mating system: field tests of alternative models

Abstract In this study we test theoretical models of female mate choice tactics in natural populations of pine engravers, Ips pini (Say) (Coleoptera: Scolytidae), a species with a resource-based mating system and high search costs. We first develop distinguishing predictions for each of four models of mate choice: random, comparison tactics, and fixed and adjustable thresholds. These predictions relate to commonly collected field data that include the visiting behavior of females and the quality of accepted and rejected mates. Using these types of data, we conclude that pine engravers use an adjustable threshold mate choice tactic because females often accepted the first male encountered, rarely revisited males, visited similar numbers of males in patches of different quality, accepted higher-quality males than those they rejected even on their first encounter with a male in a patch, and had higher acceptance thresholds in high-quality patches than in low-quality patches. This adjustable threshold tactic is consistent with a one-step decision rule and is predicted to occur in species such as pine engravers in which search costs are high and females have information about patch quality before beginning a search in a patch.     

Dynamic mate-searching tactic allows female satin bowerbirds Ptilonorhynchus violaceus to reduce searching

Females can maximize the benefits of mate choice by finding high-quality mates while using search tactics that limit the costs of searching for mates. Mate-searching models indicate that specific search tactics would best optimize this trade-off under different conditions. These models do not, however, consider that females may use information from previous years to improve mate searching and reduce search costs in subsequent years. We followed female satin bowerbirds Ptilonorhynchus violaceus during mate searching and reconstructed their search patterns. We found that females who chose very attractive males typically mated with the same male in the following year, resulting in these females sampling fewer males than those who switched mates. In contrast, females who mated with less attractive males typically rejected their previous mates and searched longer for more attractive mates in the following mating season. A potential cost to mate searching is suggested by the observed increase in the likelihood of force-copulation attempts from marauding males with increased searching. Our results suggest that by using past experiences to adjust their search tactics, females may obtain high-quality mates while limiting search costs. These results emphasize the need to consider historical effects in studies of sexual selection, especially for long-lived species with stable display sites.     

SIZE,SYMMETRY, AND SEXUAL SELECTION IN THE HOUSEFLY,MUSCA DOMESTICA

Relationships between measures of body size, asymmetry, courtship effort, and mating success were investigated in the housefly, Musca domestica (Diptera: Muscidae). A previous study indicated that both male and female flies with low fluctuating asymmetry enjoyed enhanced mating success. The aim of our investigations was to determine whether the greater success of symmetrical males is due to variation in male mating effort or to female choice and whether males exhibited mate choice. However, our study found directional rather than fluctuating asymmetry with both male and female flies having, on average, longer left wings than right. Also, asymmetry was not related to mating success in either sex. Rather, both males and females appeared to exhibit choice on the basis of the size of potential mates, with males preferring females with long bodies and females preferring heavy males. Possible benefits from choice of large mates are discussed. The initial mating strikes (in which the male leaps onto the back of the female) did not appear to be targeted according to female morphology, and their frequency did not vary according to male morphology. This indicates that mate choice by both sexes according to size probably occurs during the later stages of courtship, when the flies are in intimate contact. Possible reasons for the absence of choice according to asymmetry are discussed.     

Alternative Female Choice Tactics in the Scorpionfly Hylobittacus apicalis(Mecoptera) and Their Implications

Females of the scorpionfly Hylobittacus apicalis choose mateson the basis of material benefits (nuptial arthropod prey size)and probably on the basis of genetic benefits males deliverat mating. Females feed on the male's prey throughout copulation.They prefer males with large prey as mates and often refusemales who present small prey. That females may value male geneticquality is suggested by differences in ability of males to obtainlarge prey, which if inherited would influence offspring fitness,and by females often terminating mating with males with smallprey before they transfer any sperm or a complete ejaculate.Females hunt only when males with prey are not available becausehunting exposes individuals to predators. Female Hylobittacusapicalis exhibit alternative mate choice tactics, which arecondition-dependent in expression and probably comprise a conditionalstrategy. Body size, recent feeding history, and male availabilitydetermine how discriminating an individual female actually is,and these conditions may determine the value of material andgenetic benefits in mate choice decisions. The results suggestthat female choice controls male behavior. When females becomechoosy, males are forced to obtain rare large prey despite theincreased risks to males associated with this behavior. The implications of the findings on H. apicalis are discussedin relation to condition dependent female choice patterns inother species and the evolutionary maintenance of female choice.     

Male mate choice in Tibetan macaques Macaca thibetana at Mt. Huangshan, China

Though females are generally more selective in mate choice, males may also benefit from mate choice if male reproductive success is limited by factors other than simply the number of female mates, and if females differ in short-term reproductive potential. We studied male mate choice in a free-ranging troop of Tibetan macaques Macaca thibetana at Mt. Huangshan,China, from August 2007 to April 2008. We employed focal animal sampling and all occurrence sampling to record sexual related behaviors. Eight adult females were divided into three female quality categories according to the females' age, rank and parity.Using male mating effort as a proxy for male mate choice, we found that males do distinguish female quality and show time-variant mating strategies. Specifically, females with dominant rank, high fecundity, and middle age attracted significantly more males. Our results suggest that female short-term reproductive potential appears to be an important variable in determining male mating effort. Male Tibetan macaques do exercise mate choice for higher quality females as well as reduce useless reproductive cost, which is consistent with the direct benefits theory of mate choice.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

Mate choice by either sex may vary with changes in the associated costs and benefits, determined by factors such as the availability of potential mates and variation in mate quality. We examined seasonal variation in operational sex ratio, courtship behavior, spermatophore mass, egg count, and the relationship between morphological traits and mating success in Photinus ignitus fireflies to determine if mate choice in either sex varied with the availability and relative reproductive investment of fertilizable females and sexually active males. Successfully mating males had larger lanterns than unsuccessful males when the operational sex ratio was male‐biased. In addition, female responsiveness to male signals increased as the number of courting males decreased, and male spermatophore mass decreased with body size across the mating season. Successfully mating females had larger body mass than unsuccessful females. Female body mass predicted egg count and female rejection by males increased as the season progressed and female size decreased. These results suggest that both male and female P. ignitus exhibit mate choice, and that such choice is influenced by seasonal variation in the abundance and quality of potential mates.     

Sexual History Affects Mating Behavior and Mate Choice in the Crayfish Orconectes limosus

Because mating entails both costs and potential benefits to both sexes, males and females should be under selection to make optimal choices from among available potential mates. For example, in some cases, individuals may benefit by using information on potential mates' previous sexual histories to make mate choices. In such cases, the form and direction of these benefits may vary both between the sexes and based on the sexual history of the choosing individuals themselves. We investigated the effects of recent previous sexual history on the mate choice and mating behavior of both males and females of the crayfish Orconectes limosus. In one experiment, we found that opposite‐sex dyads comprising crayfish that had both mated 7–8 d previously with other conspecifics were significantly less likely to mate than dyads in which at least one crayfish was unmated. In a second experiment, we found that, when presented with a choice of tethered (but free to move) opposite‐sex conspecifics, only virgin females discriminated between males based on sexual history, showing a preference for virgin males over recently mated males. Mated females, mated males, and virgin males showed no preferences based on the sexual histories of potential mates. We discuss the implications of these inferences in the context of what was previously known about mating behavior and potential sperm limitation in crustaceans and other taxa.     

A Comparative Bayes tactic for mate assessment and choice

Models of mate choice tactics have assumed that females randomlyencounter males when collecting information and the informationis perfect. Empirical observations of four bird species showthat females selectively visit males and repeat visits to malesbefore mating. This suggests that the assumptions of previousmodels have been too restrictive. An alternative model of informationgathering and mate choice, which relaxes the assumptions ofrandom encounters and perfect information, is presented. Inthis Comparative Bayes model, the decision of when and fromwhom to collect information is made using Bayesian estimatesof each male's quality. Predictions from the model are that:(1) the occurrence of mate assessment will increase as initialuncertainty about the quality of males increases, as the costof gathering information decreases, and as the signal perceivedby the female becomes a better representation of males' actualqualities; (2) the occurrence of repeat visits to males willbe highest when signals from males are of medium reliability;and (3) the decision of which male to assess will depend onthe estimated qualities of males, prior certainty about eachmale's quality, the reliability of each male's signal, and thecosts of assessment. Simulations compare the fitness outcomesof the Comparative Bayes tactic to other mate choice tactics.The fitness from the Comparative Bayes tactic is significantlyhigher than from the fixed threshold tactic and than from thebest-of-n tactic when the cost of assessment is low. [BehavEcol 7: 451–460 (1996)]