Different sexual traits show covariation among genotypes: implications for sexual selection

An unresolved question in sexual selection research is whetherdifferent secondary sexual traits are developmentally independentor instead whether their degree of expression is a manifestationof a general resource pool (i.e., condition) within the organism.If degree of expression of different sexual traits reflectsability to accumulate condition, then covariation should existacross genotypes in the expression of these traits, even ifthey are very different in kind. Here we present evidence forpredicted covariation between morphological (sex comb size)and behavioral (courtship song) sexual traits among geneticlines of Drosophila bipectinata Duda extracted from a naturalpopulation. There is evidence that both these traits in Drosophilaare condition dependent and subject to sexual selection. Wedetected significant body size–independent differencesin comb size among 32 lines. Replicate lines exhibiting relativelyhigh and low values of comb size were then subjected to analysesof courtship song. High sex comb lines exhibited shorter meanburst period and shorter mean burst duration than low sex comblines. These song differences occurred only during the distantpursuit phase of male courtship and existed despite factoringout individual variations in sex comb size, the trait on thebasis of which test lines were originally chosen. The resultsverify the prediction of an association between condition-dependentsecondary sexual traits across genotypes and, therefore, supportthe existence of an overall genetic quality related to conditionacquisition.     

Broad Selectivity for Courtship Song in the Cricket Gryllus bimaculatus

Various characteristics of a long‐distance acoustic signal have been shown to vary to different degrees. It has been suggested that female preferences based on stable song parameters are stabilising or weakly directional, and preferences based on variable parameters are strongly directional. We tested this hypothesis based on a short‐distance signal (courtship song) produced by the field cricket, Gryllus bimaculatus. We studied the degree of variability of different courtship song parameters and the behavioural importance of several parameters using synthesised song models in playback experiments. We found that most of the courtship song elements of G. bimaculatus were quite variable (coefficient of variation, CV, in the range of 20–53%). The most variable parameter of the courtship song was the relative amplitude of two elements: high‐amplitude ticks and low‐amplitude pulses. Because songs containing only ticks (of rare occurrence) appeared to be more effective than songs with both ticks and pulses (of frequent occurrence), we consider female preferences to be directional. Alteration of less variable traits, such as the carrier frequency and duration of ticks (CV = 20–25%), had a different effect on female responsiveness. The synthesised songs with different carrier frequencies of ticks were as attractive to females as the positive control (courtship of muted males accompanied by playback of the recorded song). Altering the duration of ticks had a crucial effect on the female response rate, decreasing female responsiveness to the level observed in the negative control (courtship of muted males). Thus, we did not find a strong relationship between the variability of individual song parameters and their potential importance in song recognition and the evaluation of male quality. The partial inconsistency of our results with the data of other authors may be due to different patterns of past and current selection on long‐distance and short‐distance acoustic signals.     

Male Courtship Behavior and Weapon Trait as Indicators of Indirect Benefit in the Bean Bug,Riptortus pedestris

Females prefer male traits that are associated with direct and/or indirect benefits to themselves. Male–male competition also drives evolution of male traits that represent competitive ability. Because female choice and male–male competition rarely act independently, exploring how these two mechanisms interact is necessary for integrative understanding of the evolution of sexually selected traits. Here, we focused on direct and indirect benefits to females from male attractiveness, courtship, and weapon characters in the armed bug Riptortus pedestris. The males use their hind legs to fight other males over territory and perform courtship displays for successful copulation. Females of R. pedestris receive no direct benefit from mating with attractive males. On the other hand, we found that male attractiveness, courtship rate, and weapon size were significantly heritable and that male attractiveness had positive genetic covariances with both courtship rate and weapon traits. Thus, females obtain indirect benefits from mating with attractive males by producing sons with high courtship success rates and high competitive ability. Moreover, it is evident that courtship rate and hind leg length act as evaluative cues of female choice. Therefore, female mate choice and male–male competition may facilitate each other in R. pedestris. This is consistent with current basic concepts of sexual selection.     

Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds

Sexually selected male courtship displays often involve multiple behavioural and physical traits, but little is known about the function of different traits in mate choice. Here, we examine female courtship behaviours to learn how male traits interact to influence female mating decisions. In satin bowerbirds (Ptilonorhynchus violaceus), successful males give highly aggressive, intense behavioural displays without startling females. Males do this by modulating their displays in response to female crouching, which signals the display intensity that females will tolerate without being startled. Females typically visit multiple males for multiple courtships before choosing a mate, and females show differing tolerance for intense displays during their first courtship with each male. We test three hypotheses that may explain this: (i) familiarity with the courting male; (ii) the order of the courtship in mate-searching; and (iii) the attractiveness of the courting male. We found that females are more tolerant of intense displays during first courtships with attractive males; this increased female tolerance may allow attractive males to give higher intensity courtship displays that further enhance their attractiveness. We then examined why this is so, finding evidence that females are less likely to be startled by males with better physical displays (bower decorations), and this reduced startling then contributes to male courtship success. This role of physical displays in facilitating behavioural displays suggests a novel mechanism by which multiple physical and behavioural traits may influence female choice.     

Firefly Courtship: Behavioral and Morphological Predictors of Male Mating Success in Photinus greeni

Differences in male mating success can generate selection on male morphological traits and courtship behaviors involved in male–male competition or female mate choice. In Photinus fireflies (Coleoptera: Lampyridae), courtship is based on bioluminescent flash signals produced by both sexes. We conducted field observations of Photinus greeni fireflies engaged in competitive courtships, in which females are able to simultaneously assess several males, to identify male morphological traits and courtship behaviors that might predict male mating success. Male morphological traits did not differ between males that successfully mated compared with unsuccessful males (dialoging males that did not mate). However, courtship behavioral interactions differed: successful males tended to have higher flash pattern rates (number of flash patterns per minute), and their courtship flashes were more likely to be answered by females. We also examined how the risk of predation by Photuris fireflies altered courtship behavior of their Photinus prey. When predatory Photuris fireflies were present, P. greeni females were less likely to mate, and showed decreased flash responses to most males. However, P. greeni males that did successfully mate in spite of Photuris presence were males that maintained high flash pattern rates that elicited female responses. These results suggest that both female mate choice and Photuris predation exert strong selective pressures on the evolution of courtship signals in Photinus fireflies.     

Relationships among male sexually selected traits in the bean bug,Riptortus pedestris (Heteroptera: Alydidae)

Current concepts of sexual selection suggest that male reproductive success is determined by multiple sexual traits. As expression and production of multiple sexual traits are frequently associated with each other, positive or negative correlations among multiple sexual traits ensue. These relationships among traits associated with male reproductive success may be crucial in the evolution of male reproductive strategies. Here, we investigate phenotypic relationships among sexually selected traits in the armed bean bug Riptortus pedestris. In this insect, males with a larger body and weapon are more likely to win male–male competitions, and males with a larger weapon or higher courtship rate are more attractive to females. There was a significant positive correlation between body size and weapon size, whereas the courtship rate had significant negative correlations with body size and weapon size. Our results suggested that there was a phenotypic trade‐off between courtship rate and male morphology. In this insect, smaller males may make more effort in courtship behavior as an alternative mating tactic.     

Testosterone control of male courtship in birds

A sequence of behaviours which we call courtship initiates reproduction in a large number of species. In vertebrates, as a component of male sexual behaviour courtship is strongly influenced by testicular androgen. Here I will review some salient issues about the regulation of courtship by testosterone in birds. The first section will briefly summarize the first 100 years of research on this topic. The specific role of testosterone or its oestrogenic metabolites in the control of different components of courtship will be the subject of the second section. Then, I will discuss how behavioural patterns can be recruited into courtship and modified in their structure by testosterone action. In the following section, the role of sexual selection and female choice in shaping the link between testosterone and courtship will be addressed. The problematic nature of the quantitative relationships between testosterone and behaviour will be topic of the fifth section. Finally, I will discuss how courtship traits that are activated by testosterone can be apparently independent of hormone blood concentrations. These issues will be examined in an evolutionary perspective, in an attempt to understand how natural and sexual selection have shaped the links between the hormone and the behaviour.     

Acoustic preference functions and song variability in the Hawaiian cricket Laupala cerasina

Female preference functions for different sexual traits can differ significantly, from 'unimodal' to 'open ended'. Through the study of acoustic communication in anurans, several studies have reported an association between static (stereotyped) traits versus dynamic (variable) traits and preference function shape (unimodal versus open ended, respectively). Observing a similar pattern in a phylogenetically independent group would suggest that deterministic forces have caused a relationship between signal variability and preference function shape in acoustic signalling systems. We examined this phenomenon in crickets, another animal characterized by intersexual acoustic communication. We measured the within-male variability for three acoustic features of the male calling song in Laupala cerasina and the corresponding shape of the female preference function for each of these features. We offer support for the generalization that open-ended preference functions correspond to relatively dynamic courtship traits and unimodal preference functions correspond to relatively static courtship traits. We discuss the evolutionary significance of these findings in the context of the natural history of the Laupala species radiation.     

The neural mechanisms of mate choice: a hypothesis

Scientists have described many physical and behavioral traits in avian and mammalian species that evolved to attract mates. But the brain mechanisms by which conspecifics become attracted to these traits is unknown. This paper maintains that two aspects of mate choice evolved in tandem: 1) traits that evolved in the "display producer" to attract mates and, 2) corresponding neural mechanisms in the "display chooser" that enable them to become attracted to these display traits. Then it discusses our (in-progress) fMRI brain scanning project on human romantic attraction, what we believe is a developed form of "courtship attraction" common to avian and mammalian species as well as the primary neural mechanism underlying avian and mammalian mate choice. The paper hypothesizes that courtship attraction is associated with elevated levels of central dopamine and norepinephrine and decreased levels of central serotonin in reward pathways of the brain. It also proposes that courtship attraction is part of a triune brain system for mating, reproduction and parenting. 1)The sex drive evolved to motivate birds and mammals to court any conspecifics. 2) The attraction system evolved to enable individuals to discriminate among potential mating partners and focus courtship activities on particular individuals, thereby conserving mating time and energy. 3) The neural circuitry for attachment evolved to enable individuals to complete species-specific parental duties.     

Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana

Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F(1-3) offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana that represent different phylogeographic clades that have been separate for ca. 0.5 million years (MY), and differ to some extent in both traits. Here, we characterize the nature and identify the targets of sexual selection on song, CHCs, and both traits combined within the populations. Three measures of courtship outcome were used as fitness proxies. They were the probability of mating, mating latency, and the production of rejection song by females, and showed patterns of association with different traits that included both linear and quadratic selection. Courtship song predicted courtship outcome better than CHCs and the signal modalities acted in an additive rather than synergistic manner. Selection was generally consistent in direction and strength between the two populations and favored males that sang more vigorously. Sexual selection differed in the extent, strength, and nature on some of the traits between populations. However, the differences in the directionality of selection detected were not a good predictor of population differences. In addition, a character previously shown to be important for species recognition, interpulse interval, was found to be under sexual selection. Our results highlight the complexity of understanding the relationship between within-population sexual selection and population differences. Sexual selection alone cannot predict differences between populations.     

Co-option of male courtship signals from aggressive display in bowerbirds

The pre-existing trait hypothesis suggests that females evolve a mating preference for an already existing male trait. This hypothesis poses a simple resolution to Darwin's long-standing question of how elaborate, male display traits evolve. The frequently observed convergence of aggressive and courtship displays across a wide array of species provides the only current support for this hypothesis. Here we provide much more detailed supporting evidence from bowerbird skrraa calls used in aggression and courtship. Consistent with the pre-existing trait hypothesis we show that (i) putatively co-opted skrraa calls used in courtship and aggression are homologous, (ii) skrraa calls were used in aggression in bowerbirds before being used in courtship, (iii) historically, intense, aggressive-like courtship calls were present near the time of co-option, and (iv) bower types contemporaneous with co-option emphasize design features that provide females protection from the adverse effects of intense courtship displays. These results, plus evidence for a female preference for males with intense aggressive-like courtship skrraa calls, suggest that aggressive skrraa calls have been co-opted for use in male courtship display     

Changes in courtship behaviour following rejection: The influence of female phenotype in Drosophila melanogaster

Courtship can be costly and so selection should favour individual males that reduce courtship towards female types that have a low probability of resulting in copulation. One way males can do this is by associating previous courtship failure with the traits of particular rejecting females. We characterised changes in male Drosophila melanogaster courtship behaviour following a failed mating attempt with one of the four female phenotypes that varied in size, age or mating status. To do this, we assessed individual courtship behaviour for each male presented again with a female of the same phenotype that previously rejected him. Males reduced subsequent courtship most strongly for recently mated (sexually non‐receptive) females. More interestingly, males also significantly reduced courtship activity following a failed mating experience from old females but did not do so for control (large, young, virgin) or small females. As such, males significantly reduced courtship towards both female types possessing chemical cues associated with their phenotype (age and mating status), but not towards a female phenotype based on physical characteristics (body size). Our results suggest that males are able to modify their courtship behaviour following experience, but that they are better prepared to associate chemical traits that may be more reliable indicators of the likelihood of courtship failure.     

Direct mate choice for simultaneous acoustic and visual courtship displays in the damselfish, Dascyllus albisella (Pomacentridae)

Acoustic signals are well established as key components of mate selection in terrestrial species, but not in aquatic species. It has long been known that damselfish (Pomacentridae) use a combined visual and acoustic display in their courtship.. This study examined several male qualities including individual size, courtship vigor, territory size and complexity, as well as components of the acoustic call including dominant frequency, pulse characteristics and repetition rate. The objective was to determine which male traits were correlated with mating success. Observations made over ten reproductive cycles revealed that female mate choices were not random and that male mating success was correlated with courtship rate (a simultaneous visual and acoustic cue) and the number of neighboring females, but not with male morphological traits, territory quality, or acoustic call structure. These results suggest that females choose mates based on a condition-dependent trait (courtship rate) that advertises quality of paternal care, which supports good parent models of sexual selection, thereby demonstrating the importance of the combined acoustic/visual display for sexual selection in fishes     

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the “gatekeepers” of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close‐range signals are as important as long‐distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.     

Divergent patterns of diversification in courtship and genitalic characters of Timema walking‐sticks

Understanding the patterns of diversification in sexual traits and the selection underlying such diversification represents a major unresolved question in evolutionary biology. We examined the phylogenetic diversification for courtship and external genitalic characters across ten species of Timema walking‐sticks, to infer the tempos and modes of character change in these sexual traits and to draw inferences regarding the selective pressures underlying speciation and diversification in this clade. Rates of inferred change in male courtship behaviours were proportional to speciation events, but male external genitalic structures showed a pattern of continuous change across evolutionary time, with divergence proportional to branch lengths. These findings suggest that diversification of courtship behaviour is mediated by processes that occur in association with speciation, whereas diversification of genitalia occurs more or less continuously, most likely driven by forces of sexual selection.     

Energy and predation costs of firefly courtship signals

Animal courtship signals include many highly conspicuous traits and behaviors, and it is generally assumed that such signals must balance the benefits of attracting mates against some fitness costs. However, few studies have assessed the multiple costs potentially incurred by any one courtship signal, so we have limited understanding of the relative importance of different costs. This study provides the first comprehensive assessment of signal costs for Photinus fireflies (Coleoptera: Lampyridae), using controlled experiments to measure both the energy and predation costs associated with their bioluminescent courtship signals. We measured energy required to generate bioluminescent flashes, using differential open-flow respirometry, and found that flash signaling results in only a nominal increase in energy expenditure above resting levels. These results suggest that the energy required to generate bioluminescent flashes represents a minor component of the total cost of firefly courtship. However, controlled field experiments revealed that visually oriented predators imposed major costs on firefly courtship signals, with higher signaling rates significantly increasing the likelihood of predation. Together with previous results demonstrating that female fireflies prefer more conspicuous courtship signals, these results support the importance of multiple-receiver communication networks in driving signal evolution.     

The importance of calling song and courtship song in female mate choice in the variable field cricket

Male field crickets produce calling songs, courtship songs, tactile signals and chemical signals. Although calling songs are known to play an important role in female mate choice, the importance of the other signals in mate choice is poorly understood. In the variable field cricket, Gryllus lineaticeps, females select mates, in part, based on variation in male calling song. Females prefer higher chirp rates, a trait which is partially dependent on male nutrient intake, and females prefer longer chirp durations, a trait which appears to be independent of male nutrient intake. We tested whether females also have preferences based on variation in male courtship song, and whether the structure of male courtship song varies with nutrient intake. First, we reexamined female preference for calling song chirp rate. Then, we examined: (1) female preference based on courtship song chirp rate; (2) the relative importance of calling song and courtship song chirp rate; (3) the nutrition dependence of courtship song chirp rate; and (4) the correlation between calling song and courtship song chirp rate. As reported previously, females preferred higher calling song chirp rates, and in addition, preferred higher courtship song chirp rates. Females were more likely to switch from a speaker broadcasting more attractive calling song to a speaker broadcasting less attractive calling song when the attractive calling song was associated with an unattractive courtship song than when it was associated with an attractive courtship song. Preferences based on courtship song may thus cause females to alter the choices that they made based on calling song. Males that received greater nutrients did not produce higher courtship song chirp rates. There was no correlation between calling song and courtship song chirp rate. As a result, the two traits may provide information to females about different aspects of male quality. Copyright 2000 The Association for the Study of Animal Behaviour.     

Multimodal signalling in estrildid finches: song,dance and colour are associated with different ecological and life‐history traits

Sexual traits (e.g. visual ornaments, acoustic signals, courtship behaviour) are often displayed together as multimodal signals. Some hypotheses predict joint evolution of different sexual signals (e.g. to increase the efficiency of communication) or that different signals trade off with each other (e.g. due to limited resources). Alternatively, multiple signals may evolve independently for different functions, or to communicate different information (multiple message hypothesis). We evaluated these hypotheses with a comparative study in the family Estrildidae, one of the largest songbird radiations, and one that includes many model species for research in sexual selection and communication. We found little evidence for either joint evolution or trade‐offs between song and colour ornamentation. Some negative correlations between dance repertoire and song traits may suggest a functional compromise, but generally courtship dance also evolved independently from other signals. Instead of correlated evolution, we found that song, dance and colour are each related to different socio‐ecological traits. Song complexity evolved together with ecological generalism, song performance with investment in reproduction, dance with commonness and habitat type, whereas colour ornamentation was shown previously to correlate mostly with gregariousness. We conclude that multimodal signals evolve in response to various socio‐ecological traits, suggesting the accumulation of distinct signalling functions.     

Physiological factors in the courtship processing of Drosophila melanogaster

The sexual receptivity of young virgin Drosophila melanogaster females develops between 24 and 48 hr from eclosion. Measurement of this process suggests that percentage receptivity (reflecting ‘switch-on’) and courtship duration (reflecting ‘courtship processing’) may not be controlled by entirely different processes. A decline in courtship duration was found to accompany the swtich-on of receptivity, suggesting that the settings in the courtship processing system are under the control of the same developmental process.Once a female has become sexually mature her courtship processing system is set to require certain quantities of courtship before acceptance occurs. This setting is stable, at least while the female is still virgin, and is correlated with a fundamental variable in the reproductive biology of the female, her fecundity.     

Male courtship attractiveness and paternity success in Photinus greeni fireflies

Although female mate choice and male sperm competition have separately attracted much attention, few studies have addressed how precopulatory and postcopulatory episodes of sexual selection might interact to drive the evolution of male traits. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, and females gain direct benefits through male nuptial gifts acquired during multiple matings over several nights. We experimentally manipulated matings of P. greeni fireflies to test the hypothesis that postcopulatory paternity success might be biased toward males that are more attractive during courtship interactions. We first measured male courtship attractiveness to individual females using field behavioral assays. Females were then assigned to two double-mating treatments: (1) least attractive second male-females were first mated with their most attractive male, followed by their least attractive male, or (2) most attractive second male-females mated with males in reverse order. Larval offspring produced by each female following these double matings were genotyped using random amplified polymorphic DNA (RAPD) markers, and male paternity was determined. Contrary to prediction, firefly males that were more attractive to females based on their bioluminescent courtship displays subsequently showed significantly lower paternity, reflecting possible male trade-offs or sexual conflict. Differences in male paternity were not related to male body condition, testes or accessory gland mass, or to variation in female spermathecal size. Additionally, this study suggests that changes in phenotypic selection gradients may occur during different reproductive stages. These results indicate that it is crucial for future studies on sexual selection in polyandrous species to integrate both precopulatory and postcopulatory episodes to fully understand the evolution of male traits.