Chance, time allocation, and the evolution of adaptively flexible sex role behavior

An alternative to classic sexual selection hypotheses for sex differentiated pre-mating behavior is that time available for mating-as individuals experience it-along with fitness differences among alternative potential mates, induces choosy versus indiscriminate mating behavior. This alternative hypothesis says that selection has acted so that all individuals flexibly express fitness-enhancing choosy, indiscriminate, and competitive mating behavior, induced by time-varying life histories, environmental and social cues. Key predictions of DYNAMATE, the formal model of adaptively flexible sex role behavior of individuals of both sexes within dynamically changing populations, include: (1) All individuals regardless of sex assess likely fitness outcomes from mating with alternative potential mates before expressing choosy or indiscriminate behavior. (2) Males and females express adaptively flexible, choosy and indiscriminate behavior so that individuals may change their behavior-from moment to moment-to fit dynamically changing circumstances. (3) Indiscriminate behavior of males and (4) choosy behavior of females would often be maladaptive even in species with greater female than male parental investment, when females have longer latencies to receptivity to re-mating than males, and when the relative reproductive rate of males is greater than in females. (5) Whether or not females show choosy behavior will not affect whether or not males exhibit choosy or indiscriminate behavior, and vice versa. (6) When other model parameters are equal, the proportion of individuals of a given sex expressing choosy or indiscriminate mating behavior is a function of the distribution of fitness ratios (a distribution of all fitness differences that would be conferred on an individual by mating with any two sequentially or simultaneously encountered alternative potential mates). (7) Whether same-sex individuals behaviorally compete is a function of the fitness that would be conferred if the strategist won access to a potential mate, but not a function of relative reproductive rate or its proxy, the operational sex ratio. We call for re-evaluation of sex differences in choosy, indiscriminate, and competitive behavior under strong experimental controls that level the ecological playing fields of males and females, i.e., under experimental conditions informing the mechanisms of phenotypic expression. We end with comments on the classic question of questions: why are the sexes as they are?     

On Richerson and Boyd's model of cultural evolution by sexual selection

Richerson and Boyd proposed a model of sexual selection in which both the male trait and the female preference are culturally transmitted. We generalize their model by introducing sex-dependent oblique transmission rates and a fairly comprehensive female preference rule. The model differs markedly from the standard genetic models in that the male trait and the female preference are uncorrelated. Hence, there can be no "sexy son" effect to offset the assumed fertility cost to choosy females. Nevertheless, the cultural processes can support a stable polymorphic equilibrium at which the choosy females are present. Also of interest are the cyclical dynamics observed in the neighborhood of the internal equilibrium.     

Parasites make male pipefish careless

Parasite-mediated sexual selection is expected to favour the avoidance of matings with infected individuals. However, the extent to which the costs and benefits of discriminating against parasitized mates trade off may depend upon numerous factors. I investigated the effects of sex and infection status on choosiness in sex-role reversed deep-snouted pipefish (Syngnathus typhle L.) that were either artificially infected with the trematode parasite Cryptocotyle sp. or sham-infected. Sham-infected males were significantly more likely to associate with a sham-infected female rather than with a Cryptocotyle-infected female. Infected males failed to discriminate against infected potential partners. Males were choosier the larger they were relative to the females available for choice. Females were not discriminatory, regardless of their infection status. Given an inverse relation between female fecundity and parasite load, choosy unparasitized males may gain enhanced reproductive success from their choice decisions. In contrast, more heavily infected wild-caught males gave birth to slightly fewer, but not smaller offspring than did uninfected or lightly infected males, suggesting only a low direct premium on choosy females. The detrimental effects of parasitism on male choosiness, and the lack of female discrimination against infected males likely have profound repercussions on the strength of sexual selection acting on the two sexes and on the dynamics of host-parasite interactions in this system.     

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.     

A conceptual review of mate choice: stochastic demography,within‐sex phenotypic plasticity,and individual flexibility

Mate choice hypotheses usually focus on trait variation of chosen individuals. Recently, mate choice studies have increasingly attended to the environmental circumstances affecting variation in choosers' behavior and choosers' traits. We reviewed the literature on phenotypic plasticity in mate choice with the goal of exploring whether phenotypic plasticity can be interpreted as individual flexibility in the context of the switch point theorem, SPT (Gowaty and Hubbell 2009 ). We found >3000 studies; 198 were empirical studies of within‐sex phenotypic plasticity, and sixteen showed no evidence of mate choice plasticity. Most studies reported changes from choosy to indiscriminate behavior of subjects. Investigators attributed changes to one or more causes including operational sex ratio, adult sex ratio, potential reproductive rate, predation risk, disease risk, chooser's mating experience, chooser's age, chooser's condition, or chooser's resources. The studies together indicate that “choosiness” of potential mates is environmentally and socially labile, that is, induced – not fixed – in “the choosy sex” with results consistent with choosers' intrinsic characteristics or their ecological circumstances mattering more to mate choice than the traits of potential mates. We show that plasticity‐associated variables factor into the simpler SPT variables. We propose that it is time to complete the move from questions about within‐sex plasticity in the choosy sex to between‐ and within‐individual flexibility in reproductive decision‐making of both sexes simultaneously. Currently, unanswered empirical questions are about the force of alternative constraints and opportunities as inducers of individual flexibility in reproductive decision‐making, and the ecological, social, and developmental sources of similarities and differences between individuals. To make progress, we need studies (1) of simultaneous and symmetric attention to individual mate preferences and subsequent behavior in both sexes, (2) controlled for within‐individual variation in choice behavior as demography changes, and which (3) report effects on fitness from movement of individual's switch points.     

The Role of Courtship Behavior and Size in Mate Preference in the Sex‐Role‐Reversed Gulf Pipefish,Syngnathus scovelli

In sex‐role‐reversed species, sexual selection acts more strongly on females than on males, a situation that can result in the evolution of secondary sexual traits in females and strong mating preferences in males. While some research exploring mating preferences in sex‐role‐reversed species has been conducted, overall, this topic remains relatively unexplored. The Gulf pipefish, Syngnathus scovelli, is a highly polyandrous pipefish species. Sexual selection is significantly stronger in females than in males, which has led to the evolution of both morphological and behavioral female secondary sexual traits. However, because males gestate the offspring in specialized pouches and make a substantial investment in embryos during development, females may also benefit from being choosy. The goal of this study was to examine both male and female mating preferences in this species. We found that male mating preference was significantly associated with female courtship behavior. Larger females were also able to maintain these behaviors for longer intervals than smaller females. No evidence of female mating preference in regard to male size was observed but the data suggest that male behaviors may be providing positive reinforcement to courting females. This research provides further insight into how mate preferences vary among sex‐role‐reversed species.     

Operational sex ratio in newts: field responses and characterization of a constituent chemical cue

Operational sex ratio (OSR) has been traditionally thought ofas a force imposing competition for mates rather than also acue used to regulate the intrasexual competition individualsencounter. To assess whether eastern red-spotted newts, Notophthalmusviridescens, could appropriately compare OSRs, we quantifiedfield responses to traps containing four males, a sexually receptivefemale, four males plus a female, or nothing as a control. Earlyin the breeding season, males from two populations chose competitivemating opportunities over no mating opportunity at all, butgenerally preferred less competitive mating prospects. Laterin the breeding season, as the OSR of newt populations becomesmore male biased, males accordingly increased their acceptanceof intrasexual competition. Females avoided groups of four males,and for both sexes, avoidance of male-biased courting groupsincreased their probability of amplexus courtship. We then isolatedan approximately 33-kD protein from male cloacal glands thatwas used by males to compare OSRs. To our knowledge, this proteinrepresents the first isolated and characterized component ofan olfactory cue used to evaluate OSR. These results supporttwo important principles regarding mating systems: (1) OSR cansomewhat paradoxically be both the source imposing competitionfor mates and the source used to reduce it, and (2) analogousto the sex in short supply often being "choosy" selecting mates,the sex in excess (here, males) appears to be choosy about itsacceptance of intrasexual competition.     

Maintenance of genetic variation in sexual ornaments: a review of the mechanisms

Female preferences for elaborate male sexual traits have been documented in a number of species in which males contribute only genes to the next generation. In such systems, mate choice has been hypothesised to benefit females genetically. For the genetic benefits to be possible there must be additive genetic variation (V(A)) for sexual ornaments, such that highly ornamented males can pass fitter genes on to the progeny of choosy females. Here, I review the mechanisms that can contribute to the maintenance of this variation. The variation may be limited to sexual ornaments, resulting in Fisherian benefits in terms of the increased reproductive success of male progeny produced by choosy females. Alternatively, ornaments may capture V(A) in other life-history traits. In the latter case, "good genes" benefits may apply in terms of improved performance of the progeny of either sex. Some mechanisms, however, such as negative pleiotropy, sexually antagonistic variation or overdominance, can maintain V(A )in ornaments and other life-history traits with little variation in total fitness, leaving little room for any genetic benefits of mate choice. Distinguishing between these mechanisms has consequences not only for the theory of sexual selection, but also for evolution of sex and for biological conservation. I discuss how the traditional ways of testing for genetic benefits can usefully be supplemented by tests detecting benefits resulting from specific mechanisms maintaining V(A )in sexual ornaments.     

Sexual competition among females: What causes courtship-role reversal?

In most animals, males are the competitive sex whereas females are typically non-competitive and choosy of mates. In a variety of taxa, certain species (or populations within species) show a reversal in these typical courtship roles. Recent research with these organisms supports a central tenet of sexual selection theory: that it is the relative investment of the sexes in offspring that controls the number of males and females available for mating, and thus is the main determinant of the degree of sexual competition in each sex.     

Predicting the direction of sexual selection

Our current understanding of the operation of sexual selection is predicated on a sex difference in parental investment, which favours one sex becoming limiting and choosy over mates, the other competitive and nonchoosy. This difference is reflected in the operational sex ratio (OSR), the ratio of sexually receptive males to females, considered to be of fundamental importance in predicting the direction of sexual selection. Difficulties in measuring OSR directly have led to the use of the potential reproductive rates (PRR) as a measure of the level of investment in offspring of males and females. Several recent studies have emphasized that other factors, such as variation in mate quality and sex differences in mortality patterns, also influence the direction of sexual selection. However, as yet there has been no attempt to form a comprehensive theory of sex roles. Here we show that neither OSR nor PRR is the most fundamentally important determinant of sex roles, and that they are not interchangeable. Instead, the cost of a single breeding attempt has a strong direct effect on competition and choosiness as well as consistent relationships to both OSR and PRR. Our life history based approach to mate choice also yields simple, testable predictions on lack of choice in either sex and on mutual mate choice.     

MUTUAL MATE CHOICE AND SEX DIFFERENCES IN CHOOSINESS

Sexual competition is associated closely with parental care because the sex providing less care has a higher potential rate of reproduction, and hence more to gain from competing for multiple mates. Sex differences in choosiness are not easily explained, however. The lower-caring sex (often males) has both higher costs of choice, because it is more difficult to find replacement mates, and higher direct benefits, because the sex providing more care (usually females) is likely to exhibit more variation in the quality of contributions to the young. Because both the costs and direct benefits of mate choice increase with increasing parental care by the opposite sex, general predictions about sex difference in choosiness are difficult. Furthermore, the level of choosiness of one sex will be influenced by the choosiness of the other. Here, we present an ESS model of mutual mate choice, which explicitly incorporates differences between males and females in life history traits that determine the costs and benefits of choice, and we illustrate our results with data from species with contrasting forms of parental care. The model demonstrates that sex differences in costs of choice are likely to have a much stronger effect on choosiness than are differences in quality variation, so that the less competitive sex will commonly be more choosy. However, when levels of male and female care are similar, differences in quality variation may lead to higher levels of both choice and competition in the same sex.     

动物的性选择

有性生殖为个体之间设置了一个冲突和竞争的环境,因为雌雄个体都希望最大限度地把自己的基因传递给后代。性选择保证了动物的繁殖成功。性选择可以分为性别内选择和性别间选择。性别内选择促使动物格斗器官或其他有利于在格斗中获胜的一些特征得到发展;性别间选择促使用来吸引异性的一些特征得到发展。雌性动物的配偶选择或与所选择的特征协同进化,或可以从选择中得到直接的利益。     

Rearing Temperature Influences Adult Response to Changes in Mating Status

Rearing environment can have an impact on adult behavior, but it is less clear how rearing environment influences adult behavior plasticity. Here we explore the effect of rearing temperature on adult mating behavior plasticity in the butterfly Bicyclus anynana, a species that has evolved two seasonal forms in response to seasonal changes in temperature. These seasonal forms differ in both morphology and behavior. Females are the choosy sex in cohorts reared at warm temperatures (WS butterflies), and males are the choosy sex in cohorts reared at cooler temperatures (DS butterflies). Rearing temperature also influences mating benefits and costs. In DS butterflies, mated females live longer than virgin females, and mated males live shorter than virgin males. No such benefits or costs to mating are present in WS butterflies. Given that choosiness and mating costs are rearing temperature dependent in B. anynana, we hypothesized that temperature may also impact male and female incentives to remate in the event that benefits and costs of second matings are similar to those of first matings. We first examined whether lifespan was affected by number of matings. We found that two matings did not significantly increase lifespan for either WS or DS butterflies relative to single matings. However, both sexes of WS but not DS butterflies experienced decreased longevity when mated to a non-virgin relative to a virgin. We next observed pairs of WS and DS butterflies and documented changes in mating behavior in response to changes in the mating status of their partner. WS but not DS butterflies changed their mating behavior in response to the mating status of their partner. These results suggest that rearing temperature influences adult mating behavior plasticity in B. anynana. This developmentally controlled behavioral plasticity may be adaptive, as lifespan depends on the partner’s mating status in one seasonal form, but not in the other.     

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.     

Constrained mate choice in social monogamy and the stress of having an unattractive partner

In socially monogamous animals, mate choice is constrained by the availability of unpaired individuals in the local population. Here, we experimentally investigate the physiological stress endured by a female (the choosy sex) when pairing with a non-preferred social partner. In two experimental contexts, female Gouldian finches (Erythrura gouldiae) socially paired with poor-quality mates had levels of circulating corticosterone that were three to four times higher than those observed in females that were paired with preferred mates. The elevated level of this stress hormone in response to partner quality was observed within 12 h of the experimental introduction and maintained over a period of several weeks. Our findings demonstrate the extent of intra-individual conflict that occurs when individuals are forced to make mate-choice decisions that are not perfectly aligned with mate-choice preferences. The elevated level of corticosterone also suggests a mechanistic route through which females might adaptively manage their responses to intersexual conflict over reproductive investment.     

The operational sex ratio influences choosiness in a pipefish

If more females than males are available for mating in the breedingpopulation (i.e., the operational sex ratio, OSR, is femalebiased), males can afford to be choosy. In the pipefish (Syngnathustyphle) females compete for males, who are choosy. In natureOSRs are typically female biased, but may occasionally be malebiased. In a series of experiments, males were allowed to choosebetween a large and a small female under a perceived excessof either males or females. Under female bias, males preferredthe large female: they spent more time close to her than tothe small female; they courted the large female sooner thanthe small; and they tended to copulate sooner and more oftenwith the large female. Under male bias all these differencesvanished and males mated at random with respect to female size.Males reproduced at a faster rate under male than under femalebias because they received more eggs in their brood pouches.Thus, males switched from maximizing mate quality (i.e., beingchoosy) to minimizing the risk of not reproducing (i.e., beingquick) as the OSR became male biased.     

Does competitive divergence occur if assortative mating is costly?

Most models of sympatric speciation have assumed that assortative mating has no costs. A few studies, however, have shown that the costs for being choosy can prevent such speciation. Here, we investigate the role of the strength of assortment and of the costs for being choosy for a simple genetic model of a single ('magic') trait that mediates both intraspecific competition for a continuum of resources and assortative mating, which is induced by choosy females who preferentially mate with males of similar phenotype. Choosiness may be costly if it is difficult to find a mating partner. Such magic trait models are considered to be most conducive of sympatric speciation. We consider a sexually reproducing population of haploid individuals that is density regulated. The trait is determined by a single locus with multiple alleles. The strength of stabilizing selection (caused by a unimodal resource distribution), the strength of competition, the degree of assortment and the costs for being choosy are independent parameters. We investigate analytically and numerically how these parameters determine the equilibrium and stability structure. In particular, we identify conditions under which no polymorphism at all is maintained as well as conditions under which strong competitive divergence occurs, or the population even splits into two reproductively isolated classes of highly diverse phenotypes. If costs are absent or moderate, genetic variability tends to be minimized at intermediate strengths of assortment, and reproductively isolated classes of phenotypes are a likely result of evolution only for intermediate or strong competition and for very strong assortment. The likelihood of divergence depends relatively weakly on the costs as long as they are not high. With high costs, however, increasingly strong assortment rapidly depletes all genetic variation, and strong competitive divergence is prevented.     

Shaking Youngsters and Shaken Adults: Female Beetles Eavesdrop on Larval Seed Vibrations to Make Egg-Laying Decisions

Egg-laying decisions are critical for insects, and particularly those competing for limited resources. Sensory information used by females to mediate egg-laying decisions has been reported to be primarily chemical, but the role of vibration has received little attention. We tested the hypothesis that vibrational cues produced by feeding larvae occupying a seed influences egg-laying decisions amongst female cowpea beetles. This hypothesis is supported by three lines of evidence using two strains of the cowpea beetle (Callosobruchus maculatus), an Indian strain with choosy females and aggressively competing larvae and a Brazilian strain with less choosy females and larvae exhibiting an “accommodating” type of competition. First, in free-choice bioassays of seed selection, choosy Indian females selected control seeds (free of eggs, larvae, or egg-laying marker) over seeds with live larvae (free of eggs and egg-laying marker), but did not discriminate between control seeds and those with dead larvae. In contrast, less choosy Brazilian females showed no preference for seeds containing live or dead larvae over controls. Second, laser-doppler vibrometer recordings confirmed that larvae feeding inside seeds generate vibrations that are available to the female during egg-laying decisions. Third, during dichotomous choice experiments where artificial vibrations approximating those produced by feeding larvae were played back during seed selection, Indian females preferred immobile control seeds over vibrating seeds, but Brazilian females showed no preference. These results support the hypothesis that females use larval vibrations in their egg-laying decisions; whether these vibrations are passive cues exploited by the female, or active signals that ‘steer’ the behaviour of the female is unknown. We propose that vibration cues and signals could be important for host selection in insects, particularly those laying on substrates where visual or chemical cues may be unreliable. This seems to be the case with females of the cowpea beetle since visual cues are not important and chemical egg-marking does not last more than two weeks, allowing vibration cues to improve discrimination of egg-laying substrate particularly by choosy females.     

The evolution and significance of male mate choice

The distinct reproductive roles of males and females, which for many years were characterised in terms of competitive males and choosy females, have remained a central focus of sexual selection since Darwin's time. Increasing evidence now shows that males can be choosy too, even in apparently unexpected situations, such as under polygyny or in the absence of male parental care. Here, we provide a synthesis of the theory on male mate choice and examine the factors that promote or constrain its evolution. We also discuss the evolutionary significance of male mate choice and the contrasts in male versus female mate choice. We conclude that mate choice by males is potentially widespread and has a distinct role in how mating systems evolve.     

Sex Recognition via Chemical Cues in the Sex-Role-Reversed Gulf Pipefish (Syngnathus scovelli)

Sexual selection theory predicts that members of the choosy sex, usually females, should employ multiple sensory systems to obtain information about potential mates. Such predictions should also apply to systems in which sexual selection acts most strongly on females (i.e. sex-role-reversed species), and males of these taxa should be the individuals employing multiple cues to assess female attractiveness. Very little work has been directed toward mate choice involving multiple sensory systems in sex-role-reversed taxa, but fishes of the family Syngnathidae (pipefishes, seahorses, and sea dragons) provide an excellent opportunity to contribute to this research enterprise. While much is known about visual communication in pipefish, the role of chemical communication has not been investigated. Using dichotomous choice tests, we found that male, but not female, Gulf pipefish attended to chemical cues of opposite sex conspecifics. Given that males distinguished sex on the basis of chemical cues, we also tested whether males could assess female body size, an important trait with respect to mate choice in pipefish, on the basis of chemical cues alone. When given the choice between chemical cues produced by large vs. small females, males exhibited no preference. Our results suggest that male pipefish can use chemical cues to distinguish between males and females but not to differentiate females of different body size.