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.     

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.     

Sexual selection in the gift-giving dance fly, Rhamphomyia sulcata, favors small males carrying small gifts

In some species of insects males transfer a gift to females during courtship or copulation. In the dance flies these nuptial gifts vary from nutritious prey items to inedible tokens such as a leaf, stone, or silk balloon. Nuptial gifts in dance flies are presumed to increase male mating success. We examined the strength and form of sexual selection on male Rhamphomyia sulcata, an empidid in which males provide females with a nutritious prey item as a nuptial gift. We found that whereas large males carried large gifts, neither large males nor gifts were targets of sexual selection. Indeed, correlational selection analysis and nonparametric examination of the fitness surfaces revealed that small males carrying small gifts were the most successful. Males may be more maneuverable or flight efficient with small gifts, or small males with large gifts may be unable to carry both a large gift and a female in the paired descent flight. These results suggest carrying constraints may be an important factor in determining selection on nuptial gift size. The largest target of sexual selection was old males. Old males were also paired with the largest and most fecund females, highlighting the role mate quality can further contribute to selection on males. Correlational selection analysis also revealed selection for an increase in covariance between male wing length and body size, and for an increase in slope between these traits. Males who deviate away from the optimal phenotypic relationship for two tightly related morphological traits, such as tibia and wing length, may have overall reduced performance. These findings highlight the role correlational sexual selection can play in optimizing nonsexual male morphology and scaling relationships. This study questions the role of the nuptial gift in dance flies as a resource for females.     

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.     

Trade-off between pre and post-copulatory traits depends on locomotor activity in male Tribolium castaneum beetles

Locomotor performance is an indicator of dynamic exercise; thus, it is a central trait in many animal behaviours. Although higher locomotor endurance may increase male reproductive success (e.g., in mate searching and male–male contests), investment in other male reproductive traits (e.g., male attractiveness and sperm competition) may be decreased through energy consumption due to higher activity levels. Here, I investigated male attractiveness, mating success, and paternity success using males of the red flour beetle Tribolium castaneum selected for higher (H) and lower (L) locomotor endurance. Although there was no difference in male attractiveness between the selection regimes, H males had significantly higher mating success than L males. Conversely, L males had significantly higher paternity success than H males. Therefore, there was a trade-off between mating success and paternity success among the selection regimes, suggesting that locomotor endurance affects male reproduction in T. castaneum, and individual variation of locomotor endurance may be maintained within a population.     

An integrative view of sexual selection in Tribolium flour beetles

Sexual selection is a major force driving the evolution of diverse reproductive traits. This evolutionary process is based on individual reproductive advantages that arise either through intrasexual competition or through intersexual choice and conflict. While classical studies of sexual selection focused mainly on differences in male mating success, more recent work has focused on the differences in paternity share that may arise through sperm competition or cryptic female choice whenever females mate with multiple males. Thus, an integrative view of sexual selection needs to encompass processes that occur not only before copulation (pre-mating), but also during copulation (peri-mating), as well as after copulation (post-mating), all of which can generate differences in reproductive success. By encompassing mechanisms of sexual selection across all of these sequential reproductive stages this review takes an integrative approach to sexual selection in Tribolium flour beetles (Coleoptera: Tenebrionidae), a particularly well-studied and economically important model organism. Tribolium flour beetles colonize patchily distributed grain stores, and juvenile and adult stages share the same food resources. Adults are highly promiscuous and female reproduction is distributed across an adult lifespan lasting approximately 1 year. While Tribolium males produce an aggregation pheromone that attracts both sexes, there appears to be little pre-mating discrimination among potential mates by either sex. However, recent work has revealed several peri-mating and post-mating mechanisms that determine how offspring paternity is apportioned among a female's mates. During mating, Tribolium females reject spermatophore transfer and limit sperm numbers transferred by males with low phenotypic quality. Although there is some conflicting evidence, male copulatory leg-rubbing appears to be associated with overcoming female resistance to insemination and does not influence a male's subsequent paternity share. Evidence suggests that Tribolium beetles have several possible post-mating mechanisms that they may use to bias paternity. Male sperm precedence has been extensively studied in Tribolium spp. and the related Tenebrio molitor, and several factors influencing male paternity share among a female's progeny have been identified. These include oviposition time, inter-mating interval, male strain/genotype, the mating regimen of a male's mother, male starvation, and tapeworm infection. Females exert muscular control over sperm storage, although there is no evidence to date that females use this to differentiate among mates. Females could also influence offspring paternity by re-mating with additional males, and T. castaneum females more readily accept spermatophores when they are re-mating with more attractive males. Additional work is needed to examine the possible roles played by both male and female accessory gland products in determining male paternity share. Sexual selection during pre-mating episodes may be reinforced or counteracted by peri- and post-copulatory selection, and antagonistic coevolution between the sexes may be played out across reproductive stages. In Tribolium, males' olfactory attractiveness is positively correlated with both insemination success and paternity share, suggesting consistent selection across different reproductive stages. Similar studies across sequential reproductive stages are needed in other taxa to provide a more integrative view of sexual selection.     

Pre‐ and postcopulatory sexual selection act in concert to determine male reproductive success in Tribolium castaneum

To capture how sexual selection shapes male reproductive success across different stages of reproduction in Tribolium castaneum (Coleoptera, Tenebrionidae), we combined sequential sperm defence (P1) and sperm offence (P2) trials with additional trials where both males were added simultaneously to the female. We found a positive correlation between the relative paternity share in simultaneous male–male competition trials and the P2 trial. This suggests that males preferred by females as sires achieve superior fertilization success during sperm competition in the second male position. In simultaneous male–male competition trials, where pre‐, peri‐ and postcopulatory sexual selection were all allowed to act, the relative paternity share of preferred males was more than 20% higher than in P2 sperm competition trials where precopulatory female choice was disabled. Additional behavioural observations revealed that mating with more attractive males resulted significantly more frequently in offspring production than mating with less attractive males. Thus, by comparing male fertilization success in trials where precopulatory choice was turned off with more inclusive estimates of fertilization success where pre‐ and pericopulatory choice could occur, we show that female mate choice may effectively inhibit sperm competition. Female mate choice and sperm competition (P2) are positively correlated, which is consistent with directional sexual selection in this species. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 67–75.     

Acoustic preference functions and sexual selection on the male calling song in the grasshopper Chorthippus biguttulus

Male courtship songs have two functions in species recognition and intraspecific mate choice. Female preference might thus exert different types of selection pressure on male song traits. We used a combination of acoustic mate choice experiments and statistical analyses to examine how traits of the calling songs of male nightingale grasshoppers,Chorthippus biguttulus , are influenced by different sexual selection pressures. We recorded calling songs of males and tested their attractiveness to females in acoustic mate choice experiments. The attractiveness values were a good estimate of the potential male mating success. In experiments with a pair of males, females copulated significantly more often with the male that had the higher attractiveness value. To detect directional, stabilizing, disruptive or correlative selection acting on male song properties we used linear and nonlinear regressions between male song traits and female response behaviour. Three signal traits were revealed to be under directional selection: song loudness, pause to syllable ratio and the mean duration of gaps within syllables. A nonlinear regression testing for correlative selection showed that a fourth song trait, rhythm, in combination with mean gap duration was also important for female mate choice. With these traits and trait combinations we were able to explain 42% of the variance in attractiveness between males. Since we found no evidence for stabilizing selection, but ample evidence for directional selection, we conclude that selection on the traits examined is related to mate choice mainly in the context of intraspecific sexual selection and probably less so in species recognition. Copyright 2003 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.      

Limits to Nuptial Gift Production by Male Fireflies, Photinus ignitus

Males of diverse insect species provide females with nuptial gifts, and limits on males' ability to produce these gifts may influence courtship behavior and mating systems. In the firefly Photinus ignitus, males transfer a complex spermatophore to females during mating. We provided firefly males unlimited access to responsive females to examine whether spermatophore production limits male mating success. Male spermatophore mass decreased significantly across sequential matings, and the percentage of successful matings declined during the second half of each male's life span. Male body mass explained a significant proportion of variation in size of the first spermatophore produced by P. ignitus males, but this relationship disappeared with second spermatophores. This study indicates that males' ability to produce spermatophores declines over their lifetime and that limits on nuptial giftproduction can constrain male mating success in Photinus fireflies.     

Flash signals, nuptial gifts and female preference in photinus fireflies

The evolution of male courtship signals such as the bioluminescentflashes of fireflies may be shaped, at least in part, by femalepreference for particular characteristics of the male signal.These female preferences for male courtship signals may ariseas a result of the benefits of choosing males with particulartraits. One possible benefit of mate choice occurs if femalescan use male courtship signals as an honest indicator of malenutritional contributions at mating, nuptial gifts. This paperreviews female preference for male flash characteristics inPhotinus fireflies (Coleoptera: Lampyridae), and the potentialfor females to use male flash characteristics to predict nuptialgift quality. In Photinus firefly species with single pulseflashes females preferentially respond to flashes of greaterintensity and duration. Male Photinus provide a nuptial giftto females at mating in the form of a spermatophore and flashduration serves as a good predictor of spermatophore mass formales collected early in the season. However, Photinus firefliesdo not feed as adults, so spermatophore mass decreases withsubsequent matings. In response, nutrient-limited females maystop preferentially responding to longer duration flashes, increasingtheir overall responsiveness later in the mating season as theyforage for spermatophores. Therefore, the evolution of malecourtship signals in Photinus fireflies is the product not onlyof female preference for male flash characteristics, but alsothe costs and benefits of female choice that shape these preferences.     

A novel method of comparing mating success and survival reveals similar sexual and viability selection for mobility traits in female tree crickets

The relationship between sexual and viability selection in females is necessarily different than that in males, as investment in sexual traits potentially comes at the expense of both fecundity and survival. Accordingly, females do not usually invest in sexually selected traits. However, direct benefits obtained from mating, such as nuptial gifts, may encourage competition among females and subsidize investment into sexually selected traits. We compared sexual and viability selection on female tree crickets Oecanthus nigricornis, a species where females mate frequently to obtain nuptial gifts and sexual selection on females is likely. If male choice determines female mating success in this species, we expect sexual selection for fecundity traits, as males of many species prefer more fecund females. Alternatively, intrasexual scramble or combat competition on females may select for larger jumping legs or wider heads (respectively). We estimated mating success in wild caught crickets using microsatellite analysis of stored sperm and estimated relative viability by comparing surviving female O. nigricornis to those captured by a common wasp predator. In support of the scramble competition hypothesis, we found sexual selection for females with larger hind legs and narrower heads. We also found stabilizing viability selection for intermediate head width and hind leg size. As predicted, traits under viability and sexual selection were very similar, and the direction of that selection was not opposing. However, because the shape of sexual and viability selection differs, these episodes of selection may favour slightly different trait sizes.     

Seasonal Variation in Mate Choice of Photinus ignitus Fireflies

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

Death feigning in the face of sexual cannibalism

Pre-copulatory sexual cannibalism by females affects male and female reproductive success in profoundly different ways, with the females benefiting from a meal and the male facing the risk of not reproducing at all. This sexual conflict predicts evolution of traits to avoid cannibalism and ensure male reproductive success. We show that males of the nuptial gift-giving spider Pisaura mirabilis display a remarkable death feigning behaviour--thanatosis--as part of the courtship prior to mating with potentially cannibalistic females. Thanatosis is a widespread anti-predator strategy; however, it is exceptional in the context of sexual selection. When the female approached a gift-displaying male, she usually showed interest in the gift but would sometimes attack the male, and at this potentially dangerous moment the male could 'drop dead'. When entering thanatosis, the male would collapse and remain completely motionless while retaining hold of the gift so it was held simultaneously by both mates. When the female initiated consumption of the gift, the male cautiously 'came to life' and initiated copulation. Death feigning males were more successful in gaining copulations, but did not have prolonged copulations. We propose that death feigning evolved as an adaptive male mating strategy in conjunction with nuptial gift giving under the risk of being victimized by females.     

Courtship raises male fertilization success through post-mating sexual selection in a spider

Courtship is well known for its positive effects on mating success. However, in polyandrous species, sexual selection continues to operate after copulation. Cryptic female choice is expected under unpredictable mating rates in combination with sequential mate encounters. However, there are very few accounts of the effects of courtship on cryptic female choice, and the available evidence is often correlative.Mature Argiope bruennichi females are always receptive and never attack or reject males before mating, although sexual cannibalism after mating occurs regularly. Still, males usually perform an energetic vibratory display prior to copulation. We tested the hypothesis that beneficial effects of courtship arise cryptically, during or after mating, resulting in increased paternity success under polyandry. Manipulating courtship duration experimentally, we found that males that mated without display had a reduced paternity share even though no differences in post-copulatory cannibalism or copulation duration were detected. This suggests that the paternity advantage associated with courtship arose through female-mediated processes after intromission, meeting the definition of cryptic female choice.     

Predictors of male insemination success in the mosquitofish (Gambusia holbrooki)

Identifying targets of selection is key to understanding the evolution of sexually selected behavioral and morphological traits. Many animals have coercive mating, yet little is known about whether and how mate choice operates when these are the dominant mating tactic. Here, we use multivariate selection analysis to examine the direction and shape of selection on male insemination success in the mosquitofish (Gambusia holbrooki). We found direct selection on only one of five measured traits, but correlational selection involving all five traits. Larger males with longer gonopodia and with intermediate sperm counts were more likely to inseminate females than smaller males with shorter gonopodia and extreme sperm counts. Our results highlight the need to investigate sexual selection using a multivariate framework even in species that lack complex sexual signals. Further, female choice appears to be important in driving the evolution of male sexual traits in this species where sexual coercion is the dominant mating tactic.     

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.     

Polyandry as a mediator of sexual selection before and after mating

The Darwin–Bateman paradigm recognizes competition among males for access to multiple mates as the main driver of sexual selection. Increasingly, however, females are also being found to benefit from multiple mating so that polyandry can generate competition among females for access to multiple males, and impose sexual selection on female traits that influence their mating success. Polyandry can reduce a male''s ability to monopolize females, and thus weaken male focused sexual selection. Perhaps the most important effect of polyandry on males arises because of sperm competition and cryptic female choice. Polyandry favours increased male ejaculate expenditure that can affect sexual selection on males by reducing their potential reproductive rate. Moreover, sexual selection after mating can ameliorate or exaggerate sexual selection before mating. Currently, estimates of sexual selection intensity rely heavily on measures of male mating success, but polyandry now raises serious questions over the validity of such approaches. Future work must take into account both pre- and post-copulatory episodes of selection. A change in focus from the products of sexual selection expected in males, to less obvious traits in females, such as sensory perception, is likely to reveal a greater role of sexual selection in female evolution.     

Influence of male courtship intensity and male–male competition on paternity distribution in Hermann's tortoise,Testudo hermanni hermanni (Chelonia: Testudinidae)

Honest‐advertisement models of sexual selection suggest that condition‐dependent male secondary sexual characters could function as reliable signals of male quality, enabling females to discriminate among potential partners, both in the pre‐ and post‐copulatory phases. In this context, many studies have revealed the importance of promiscuous mating systems and female sperm storage in determining the occurrence of such a model of sexual selection. By contrast, few studies have investigated the presence and extent of post‐copulatory female choice in chelonian species. The present study aimed to investigate the effect of male size, male–male competition, and courtship intensity on paternity distribution in Testudo hermanni hermanni, combining behavioural and genetic data. We created experimental groups composed of two males of different sizes and three or four randomly selected females. Observations conducted during social interactions between males revealed that a hierarchy, unrelated to male size, was soon established: Alpha males were more aggressive towards competitors and courted females more intensively. Alpha males also achieved a higher mounting success than Beta males. Paternity analysis performed on hatchlings produced from experimental females revealed that male reproductive success was not correlated with male–female size ratio. Finally, despite the higher mounting success of Alpha males, paternity analysis revealed that male reproductive success did not differ between Alpha and Beta males. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 656–667.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Pre‐ and postcopulatory sexual selection favor aggressive,young males in polyandrous groups of red junglefowl

A challenge in evolutionary biology is to understand the operation of sexual selection on males in polyandrous groups, where sexual selection occurs before and after mating. Here, we combine fine‐grained behavioral information (>41,000 interactions) with molecular parentage data to study sexual selection in replicated, age‐structured groups of polyandrous red junglefowl, Gallus gallus. Male reproductive success was determined by the number of females mated (precopulatory sexual selection) and his paternity share, which was driven by the polyandry of his female partners (postcopulatory sexual selection). Pre‐ and postcopulatory components of male reproductive success covaried positively; males with high mating success also had high paternity share. Two male phenotypes affected male pre‐ and postcopulatory performance: average aggressiveness toward rival males and age. Aggressive males mated with more females and more often with individual females, resulting in higher sexual exclusivity. Similarly, younger males mated with more females and more often with individual females, suffering less intense sperm competition than older males. Older males had a lower paternity share even allowing for their limited sexual exclusivity, indicating they may produce less competitive ejaculates. These results show that—in these populations—postcopulatory sexual selection reinforces precopulatory sexual selection, consistently promoting younger and more aggressive males.