Covariation and repeatability of male mating effort and mating preferences in a promiscuous fish

Although mate choice by males does occur in nature, our understanding of its importance in driving evolutionary change remains limited compared with that for female mate choice. Recent theoretical models have shown that the evolution of male mate choice is more likely when individual variation in male mating effort and mating preferences exist and positively covary within populations. However, relatively little is known about the nature of such variation and its maintenance within natural populations. Here, using the Trinidadian guppy (Poecilia reticulata) as a model study system, we report that mating effort and mating preferences in males, based on female body length (a strong correlate of fecundity), positively covary and are significantly variable among subjects. Individual males are thus consistent, but not unanimous, in their mate choice. Both individual mating effort (including courtship effort) and mating preference were significantly repeatable. These novel findings support the assumptions and predictions of recent evolutionary models of male mate choice, and are consistent with the presence of additive genetic variation for male mate choice based on female size in our study population and thus with the opportunity for selection and further evolution of large female body size through male mate choice.     

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.     

Repeatability of Male Mate Choice in the Mosquitofish, Gambusia holbrooki

Male mate choice has evolved in many species in which female fecundity increases with body size. In these species, males are thought to have been selected to favour mating with large females over smaller ones, thereby potentially increasing their reproductive success. While male mate choice is known to occur, it is less well studied than female mate choice and little is known about variation in mating preference among individual males. Here, we presented individual male eastern mosquitofish ( Gambusia holbrooki ) with paired females that differed in body size, and we quantified their mate preference on two consecutive days, allowing us to assess repeatability of preferences expressed. When males were allowed to view paired stimulus females, but not to acquire chemical or tactile cues from them, they exhibited a strong preference for large females over smaller ones. However, individual males were not consistent in the strength of their preference and repeatability was not significant. When individual males were allowed to fully interact with pairs of females, the males again exhibited a preference for large females over smaller ones, as revealed by a greater number of attempted copulations with large females than with smaller ones. In the latter social context, individual male preference was significantly repeatable. These results indicate that male eastern mosquitofish from our Florida study population possess, on average, a mating preference for larger females and that this preference is repeatable when males socially interact freely with females. The significant repeatability for mating preference, based on female body size, obtained for male mosquitofish in the current study is consistent with the presence of additive genetic variation for such preferences in our study population and thus with the opportunity for the further evolution of large body size in female mosquitofish through male mate choice.     

Disruptive sexual selection on male nuptial coloration in an experimental hybrid population of cichlid fish

Theory suggests that genetic polymorphisms in female mating preferences may cause disruptive selection on male traits, facilitating phenotypic differentiation despite gene flow, as in reinforcement or other models of speciation with gene flow. Very little experimental data have been published to test the assumptions regarding the genetics of mate choice that such theory relies on. We generated a population segregating for female mating preferences and male colour dissociated from other species differences by breeding hybrids between species of the cichlid fish genus Pundamilia. We measured male mating success as a function of male colour. First, we demonstrate that non-hybrid females of both species use male nuptial coloration for choosing mates, but with inversed preferences. Second, we show that variation in female mating preferences in an F2 hybrid population generates a quadratic fitness function for male coloration suggestive of disruptive selection: intermediate males obtained fewer matings than males at either extreme of the colour range. If the genetics of female mate choice in Pundamilia are representative for those in other species of Lake Victoria cichlid fish, it may help explain the origin and maintenance of phenotypic diversity despite some gene flow.     

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.     

Bill Color Preferences of Zebra Finches

Bill color varies with age and sex in zebra finches. Among birds of similar age and condition, males' bills tend to be redder and darker than those of females, but there is overlap in the phenotypic expression of the sexes. The bills of young birds are paler and less red than those of older birds. There is also interindividual variation within age and sex class. Experiments were performed to measure heterosexual and isosexual (= same sex) preferences of finches. Females preferred to associate with males with the reddest, brightest bills; they even preferred males whose bills were exaggerated through color applications of non-toxic marking pen. Males preferred to associate with females with bill colors in the middle of the phenotypic range. Females thus have “directional” preferences for male bill color, whereas male preference is “stabilizing” with regard to female bill color. In isosexual tests, neither sex showed a consistent preference for particular bill colors. Both sexes, however, displayed a tendency toward individual variability in preference. Bill color appears to be more important in heterosexual than in isosexual interactions. Several authors have recently suggested that organisms prefer brightly colored mates because bright coloration indicates superior physical condition. Results reported here do not support this hypothesis. Alternative functional explanations for the observed preferences are that bill color signals mating status, age or reproductive value. None of these appears to be a cogent explanation for the trends. Preferences do not appear to result from sexual imprinting. The possibility that the preferences are aesthetic and non-functional is discussed.     

Low-quality females prefer low-quality males when choosing a mate

Mate choice studies routinely assume female preferences for indicators of high quality in males but rarely consider developmental causes of within-population variation in mating preferences. By contrast, recent mate choice models assume that costs and benefits of searching or competing for high-quality males depend on females'' phenotypic quality. A prediction following from these models is that manipulation of female quality should alter her choosiness or even the direction of her mating preferences. We here provide (to our knowledge) the first example where an experimental manipulation of female quality induced a mating preference for low-quality males. Zebra finches (Taeniopygia guttata) reared in small or large experimental broods became high- or low-quality adults, respectively. Only high-quality females preferred high-quality males'' mate-advertising songs, while all low-quality females preferred low-quality males'' song. Subsequent breeding trials confirmed this pattern: latency until egg laying was shortest in quality-matched pairs, indicating that quality-matched birds were accepted faster as partners. Females produced larger eggs when mated with high-quality males, regardless of their own quality, indicating consensus regarding male quality despite the expression of different choices. Our results demonstrate the importance of considering the development of mating preferences to understand their within-population variation and environmentally induced change.     

Audience Effect Alters Male Mating Preferences in Zebra Finches (Taeniopygia guttata)

The social environment of animals strongly influences the mating preferences of both the choosing and the observing individuals. Notably, there is recent evidence that polygamous males decrease their selectivity when being observed by competitors in order to direct their rivals' attention away from their true interest and, consequently, reduce sperm competition risk. Yet, other mechanisms, whose importance remains unexplored, could induce similar effects. In monogamous species with mutual choice, particularly, if males adjust their selectivity according to the risk of being rejected by their preferred mate, they should as well become less selective when potential rivals are present. Here, we investigated whether the presence of bystanders modifies male mating preferences when the risk of sperm competition is low, by carrying out mate-choice experiments with male zebra finches (Taeniopygia guttata) whose preferences for two females were measured twice: with and without an audience. We found that the presence of potential rivals had no effect on the males' choosiness. However, with an audience, they spent more time with the female that was considered as the less attractive one in the control condition. These findings support the hypothesis that monogamous males alter their mate choice decisions in the presence of a male audience to reduce the risk of remaining unpaired. Thus, our results indicate that several explanations can account for the changes in male preferences due to the presence of competitors and highlight the importance of assessing the relative role of each mechanism potentially involved, to be able to make conclusions about the effect of an audience on signal evolution.     

Does individual personality predict male mating preference for female body size in the Trinidadian guppy?

Within populations, individual animals vary considerably in their behaviour, including mate choice and personality. There is mounting interest in the potential covariation between these two behaviours within individuals, such that personality would influence mate choice. We experimentally tested this proposition under controlled laboratory conditions using male Trinidadian guppies (Poecilia reticulata) as a model study system. We assayed repeatedly the mating preference of individual males for females based on their body size. Additionally, we assayed repeatedly two ecologically relevant personality traits in males, namely exploration of a novel environment and boldness under a simulated predation threat. Finally, we analysed whether male mating preference and personality traits were repeatable, and tested whether the personality of individual males was correlated (covaried) with their mating preference scores. Although all but one of the measures of exploration and boldness behaviour were repeatable over time, male mating preference scores were not repeatable. Measures of male exploration and boldness were not inter-correlated among individuals, suggesting the absence of a behavioural syndrome between exploration and boldness. Unexpectedly, males did not exhibit on average a significant mating preference for larger females over smaller ones; they chose randomly between the paired stimulus females. Overall, we found no compelling evidence for a relationship between individual personality traits and mating preference in male guppies, suggesting that personality does not predict mate choice, at least in our study population and under our experimental conditions. We discuss potential factors, other than male personality and body length, that might maintain inter-individual variation in male mating preferences in the guppy in the wild.     

Testing the correlated response hypothesis for the evolution and maintenance of male mating preferences in Drosophila serrata

Mate preferences are abundant throughout the animal kingdom with female preferences receiving the most empirical and theoretical attention. Although recent work has acknowledged the existence of male mate preferences, whether they have evolved and are maintained as a direct result of selection on males or indirectly as a genetically correlated response to selection for female choice remains an open question. Using the native Australian species Drosophila serrata in which mutual mate choice occurs for a suite of contact pheromones (cuticular hydrocarbons or CHCs), we empirically test key predictions of the correlated response hypothesis. First, within the context of a quantitative genetic breeding design, we estimated the degree to which the trait values favoured by male and female choice are similar both phenotypically and genetically. The direction of sexual selection on male and female CHCs differed statistically, and the trait combinations that maximized male and female mating success were not genetically correlated, suggesting that male and female preferences target genetically different signals. Second, despite detecting significant genetic variance in female preferences, we found no evidence for genetic variance in male preferences and, as a consequence, no detectable correlation between male and female mating preferences. Combined, these findings are inconsistent with the idea that male mate choice in D. serrata is simply a correlated response to female choice. Our results suggest that male and female preferences are genetically distinct traits in this species and may therefore have arisen via different evolutionary processes.     

Male versus female mate choice: sexual selection and the evolution of species recognition via reinforcement

Male mate choice, expressed through courtship preferences, sometime occurs even under the mating system of polygyny, when the operational sex ratio is skewed toward males. The conditions under which male mate choice may be expected during polygyny are not well established. Servedio and Lande (2006, Evolution 60:674-685), assuming strict polygyny where all females have equal mating success, show that when having a preference does not increase the amount of energy that a male can put into courtship, male preferences for "arbitrary" female ornaments should not be expected to evolve; direct selection acts against them because they place males that carry them into situations in which there is high competition for mates. Here I explore in detail two situations under which logic dictates that this effect may be overcome or reversed. First I determine the contributions that direct and indirect selection place on male versus female preferences for traits that increase viability, using notation that allows the exact expression of these measures of selection. I find that direct selection against male preferences still predominates in the male mate choice model, causing less evolution by male than female preferences under these conditions. Second I address whether male mate choice is likely to evolve as a mechanism of premating isolation leading to species recognition, driven by the process of reinforcement. Reinforcement is compared under male and female mate choice, using a variety of models analyzed by both analytical techniques assuming weak selection and numerical techniques under broader selective conditions. I demonstrate that although under many conditions stronger premating isolation evolves under female mate choice, reinforcement may indeed occur via male mate choice alone.     

Does sexual experience affect the strength of male mate choice for high‐quality females in Drosophila melanogaster?

Although females are traditionally thought of as the choosy sex, there is increasing evidence in many species that males will preferentially court or mate with certain females over others when given a choice. In the fruit fly, Drosophila melanogaster, males discriminate between potential mating partners based on a number of female traits, including species, mating history, age, and condition. Interestingly, many of these male preferences are affected by the male''s previous sexual experiences, such that males increase courtship toward types of females that they have previously mated with and decrease courtship toward types of females that have previously rejected them. D. melanogaster males also show courtship and mating preferences for larger females over smaller females, likely because larger females have higher fecundity. It is unknown, however, whether this preference shows behavioral plasticity based on the male''s sexual history as we see for other male preferences. Here, we manipulate the sexual experience of D. melanogaster males and test whether this manipulation has any effect on the strength of male mate choice for large females. We find that sexually inexperienced males have a robust courtship preference for large females that is unaffected by previous experience mating with, or being rejected by, females of differing sizes. Given that female body size is one of the most common targets of male mate choice across insect species, our experiments with D. melanogaster may provide insight into how these preferences develop and evolve.     

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.     

A review of the potential of surface flow constructed wetlands to enhance macroinvertebrate diversity in agricultural landscapes with particular reference to Integrated Constructed Wetlands (ICWs)

Discriminating female mate preferences enhance the variance in reproductive success among males of a population and create a potential for sexual selection, which can account for trait evolution and diversification. Fish color patterns are among the prime targets of mate choice-driven sexual selection. Populations of the cichlid Tropheus from Lake Tanganyika display remarkable geographic color pattern variation, but the role of female choice in their rapid and rich phenotypic diversification is unclear. Males and females establish a pair bond prior to spawning monogamously, but as brood care is strictly maternal, female investment in reproduction is high and the operational sex ratio is male-biased. Therefore, variance in male reproductive success can accrue if individual males succeed repeatedly in securing a mate. To test this prediction in the red colored Tropheus moorii “Chimba”, four pairs of males were presented to a series of females and female mate preferences were inferred from pairwise interactions. There was a significant difference in mating success between the males of each pair (P < 0.001 over all trials), as—with one exception—females shared preferences for the same males. Male courtship activity was strongly correlated with female choice. Our experiment suggests that female choice contributes to the variance in male reproductive success in the tested population.     

Female mate choice is not affected by mate condition in a fish with male care

Several studies have shown that mate choice based on condition leads to higher reproductive success of the choosing individual. Yet, a growing body of literature has failed to find support for mate choice based on mate condition, even when the choosing individual would clearly benefit from such a choice. This indicates that animals’ mate choice is often more complex than currently appreciated and that even well-founded expected preferences cannot be taken for granted. Using the broad-nosed pipefish, Syngnathus typhle, we manipulated male condition experimentally to explore whether it affects female mate choice. In this sex-role-reversed species, males care for the offspring in a specialised brood pouch. Males are the choosier sex, but given the opportunity, females are selective as well. During brooding, males can both provide embryos with nutrients and take up nutrients that originate from eggs deposited in the pouch, and embryo survival correlates positively with male condition. Together, this suggests that it would be beneficial for females to mate with males in high condition. However, we found no female preference for males in better condition. Thus, this study adds to the literature of mate choice that is unaffected by mate condition. Possible reasons for our result are discussed.     

Assortative Pairings in Diamond Firetails (Stagonopleura guttata) are not the Result of Mutual Mate Choice for an Ornament

Positive assortative mating occurs when individuals with similar phenotypes mate more frequently with each other than is expected by chance. In species in which both the males and females are ornamented, assortative pairings could arise from mutual mate choice on the same trait. We test this mechanism of mate choice and assortative pairing in the Diamond Firetail (Stagonopleura guttata), an Australian estrildid finch in which both sexes are ornamented with red bills, red rumps and white flank spots. We have previously shown sex differences in the degree of ornamentation as females have more flank spots than males. These white flank spots are used during sexual display, being fully displayed by courting males and by females when approaching a displaying male. Here, we experimentally test whether mutual mate preference is based on the number of flank spots. There was no evidence for a direct mutual preference for spot number. Given a choice of potential mates with a natural or experimentally manipulated number of flank spots, males preferred females with more spots, while female preference was not solely based on flank spots. Intriguingly, in both wild and captive Diamond Firetails, we found the number of flank spots in pairs was correlated suggesting a basis for positive assortative pairing. Nevertheless, we conclude that assortative pairing in Diamond Firetails is not due to mutual choice of mates based on the number of flank spots. We discuss different selection pathways for this trait in each sex.     

The Strength of Species Recognition in Captive Female Zebra Finches (Taeniopygia guttata): A Comparison Across Estrildid Heterospecifics

Conspecific recognition is essential for sexually reproducing species. Captive zebra finches ( Taeniopygia guttata ) are a model system in which the behavioural, ontogenetic and neurobiological bases of own-species (conspecific) recognition have been studied in detail. To assess the potential role of phylogeographic effects on species recognition, we examined the spatial preferences of unmated captive-bred female zebra finches between unfamiliar captive males of conspecific and estrildid heterospecific male stimuli. In accordance with prior studies using domesticated Bengalese finches ( Lonchura striata vars. domestica ), we found significant spatial and behavioural preference for conspecific males by female zebra finches, irrespective of heterospecific male phylogeographic origin mating status, or individual behaviour. This result has ramifications for the interpretation of social and mate preferences in this model species as it implies a consistency of species discrimination by captive female zebra finches.     

Sex-Specific Audience Effect in the Context of Mate Choice in Zebra Finches

Animals observing conspecifics during mate choice can gain additional information about potential mates. However, the presence of an observer, if detected by the observed individuals, can influence the nature of the behavior of the observed individuals, called audience effect. In zebra finches (Taeniopygia guttata castanotis), domesticated males show an audience effect during mate choice. However, whether male and female descendants of the wild form show an audience effect during mate choice is unknown. Therefore, we conducted an experiment where male and female focal birds could choose between two distinctive phenotypes of the opposite sex, an artificially adorned stimulus bird with a red feather on the forehead and an unadorned stimulus bird, two times consecutively, once without an audience and once with an audience bird (same sex as test bird). Males showed an audience effect when an audience male was present and spent more time with adorned and less time with unadorned females compared to when there was no audience present. The change in time spent with the respective stimulus females was positively correlated with the time that the audience male spent in front of its cage close to the focal male. Females showed no change in mate choice when an audience female was present, but their motivation to associate with both stimulus males decreased. In a control for mate-choice consistency there was no audience in either test. Here, both focal females and focal males chose consistently without a change in choosing motivation. Our results showed that there is an audience effect on mate choice in zebra finches and that the response to a same-sex audience was sex-specific.     

Differences between the sexes in direction and duration of response to seeing a potential sex partner mate with another

We have shown previously that: (1) female Japanese quail, Coturnix japonica, increase and male Japanese quail decrease their tendencies to affiliate with potential sex partners after seeing them mate, and (2) in both sexes of quail, affiliative preferences and choice of a sex partner are highly correlated. Here we predict that because effects of a prior male's sperm on a second male's probability of fertilizing a female are relatively brief, a male's avoidance of whichever member of a pair of females he has seen mating should be transitory. Conversely, because female quail seek high-quality males as mates and quality is a relatively permanent characteristic, females' preferences between males should remain constant over time. We found, as predicted, that the durations of effects on affiliation of seeing a potential sex partner mate differed in male and female quail. Forty-eight hours after male quail saw a female mate, they no longer avoided her, whereas 48 h after female quail saw a male mate, his attractiveness remained enhanced. We conclude by suggesting that both the direction and the duration of responses of male and female Japanese quail to seeing a member of the other sex mating enhance the fitness of members of each sex. Copyright 2000 The Association for the Study of Animal Behaviour.     

Removal of adult males from the rearing environment increases preference for same-sex partners in the zebra finch

The developmental processes producing preferences for opposite-sex mating partners are not well understood. Zebra finches, Taeniopygia guttata, are colonial and socially monogamous with biparental care. To determine whether the early social environment contributes to sexual partner preference, we removed adult males from breeding colonies when the oldest chicks were less than 1 week old (male-removal rearing) or left them in the breeding cage (control rearing). At independence, male-removal and control offspring were moved to unisex cages. As adults they were given two-choice tests with male versus female stimuli followed by group aviary tests. Male-removal subjects, unlike controls, did not prefer opposite-sex stimuli in the two-choice tests. Male-removal subjects were less likely than controls to successfully pair with opposite-sex birds in the group aviary tests; 38% of them paired with a same-sex bird. Thus early social experience may contribute to a critical component of mate choice, choosing the opposite sex, in this pair-bonding species. Copyright 2000 The Association for the Study of Animal Behaviour.