Unsuccessful Courtship Research Articles

Previous Interspecific Courtship Impairs Female Receptivity to Conspecifics in the Parasitoid Wasp Nasonia longicornis But Not in N. vitripennis.

Interspecific sexual interactions are not uncommon in animals. In sympatry, females often face the risk of accidentally mating with a heterospecific male. Based on the actual risks imposed by the environment at a given time and place, females should be able to adjust their mate acceptance in order to avoid interspecific copulations as well as accidentally refusing to mate with a conspecific. We investigate the ability of females of the two parasitoid wasp species Nasonia vitripennis (Nv) and N. longicornis (Nl) to adjust their mate acceptance in response to previous unsuccessful courtship by heterospecific males. We show that Nl females are more reluctant to mate with a conspecific male when having been courted previously by a heterospecific male, but Nv females are not. We argue that this strategy is reasonable for Nl females but not for Nv females, which follow a different strategy to avoid the fitness costs imposed by heterospecific copulations.

Bactrocera oleae-induced olive VOCs routing mate searching in Psyttalia concolor males: impact of associative learning.

Olfaction is a key sense routing foraging behaviour in parasitoids. Preferences for food, mate and host stimuli can be innate in parasitic wasps. Alternatively, learning-mediated mechanisms play a crucial role. Females of the braconid parasitoid Psyttalia concolor exploit olfactory cues arising from tephritid hosts and related microhabitats. However, little is known on the olfactory stimuli routing males searching for mates. In this study, we focused on the attractiveness of Bactrocera oleae-induced olive volatiles towards P. concolor males. Furthermore, we evaluated learning occurrence in virgin males, when trained for selected unattractive volatile organic compounds (VOCs) associated with mate rewards. (E)-β-Ocimene, α-pinene and limonene attracted virgin males in Y-tube bioassays. Unattractive VOCs evoked positive chemotaxis after associative learning training. P. concolor males exposed to VOCs during a successful or unsuccessful mating, showed short-term preference for these VOCs (<1 h). However, memory consolidation was strictly dependent on reward value. Indeed, males experiencing a successful mating showed a fast consolidation into protein dependent long-term memory, appearing after 24 h. On the other hand, males experiencing a less valuable training experience (i.e. unsuccessful courtship), did not show consolidated memory after 24 h. Overall, our findings suggest that P. concolor virgin males may exploit VOCs from the host microhabitat to boost their mate searching activity, thus their reproductive success. However, since learning is a costly process, P. concolor males retained durable memories just in presence of a valuable reward, thus avoiding maladaptive behaviours.

A Behavioral Index for investigating female preference in Aleuropoda insignis, the flat-horned hissing cockroach

Aleuropoda insignis, the flat-horned hissing cockroach, make whistling noises during courtship. Comer &amp; Conley (2016) showed these animals display variation in the form of different syllables, which have features of whistles. Elliptorhina chopardi also make whistling courtship songs (Sueur &amp; Aubin, 2006) along with several other species of Tribe Gromphadorhini, which are known for hissing sounds used in courtship and agonistic communication (Nelson &amp; Fraser, 1980). Sexual selection may be the foundation for species-specific courtship calls since several other species of hissing cockroaches are present in Madagascar. Females may show more interest in or be more likely to respond to specific syllables or songs, forming the basis for species identification. To begin to examine female preference for species-specific courtship calls, we placed virgin males and females in a behavioral chamber and made audiovisual recordings of behavior. We created a behavioral index based on sampling behaviors observed during successful courtship, which had been previously described by Robinson &amp; Conley (2015). This behavioral index includes proximity of animals to one another, antenna-tapping, antennation, and body orientation &amp; position with certain behaviors scored as 1-3 depending on specific criteria for ‘intensity’. We compared behavioral indices of females for trials categorized as successful courtship (song with copulation), unsuccessful courtship (song with no copulation) and no courtship. Behavioral indices were highest for successful courtship and lowest for no courtship indicating the usefulness of this index for studying female preference for song types and or sexual selection involved in species isolation.

Diffuse resistance courtship in the scorpion Rhopalurus rochai (Scorpiones: Buthidae)

Male-female courtship signals are frequently subject to arms races, with patterns of behaviour evolving reciprocally to manipulate the reproductive output. Female resistance should be particularly effective when asymmetrical offspring care occurs under low and unpredictable resource distribution, because this would increase maternal costs. Our hypothesis is that under these conditions females will evolve diffuse mating strategies to avoid predictable exploitation by male optimal counter tactics. Mating in scorpions is a complex process, and female resistance occurs through specific behaviours. Here we focus on the scorpion Rhopalurus rochai that inhabits strongly unpredictable arid habitats. We find that courtship success does not rely on typical resistance and stimulatory patterns of behaviours. The screening for prospective partners occurs in the pre-dance phase. Network statistics reveal that unsuccessful courtships are characterised by reduced complexity of interactions, a result typical of non-additive interactions that introduce unpredictability in the network. Unpredictable female resistance reduces male control over female reproduction more effectively than resistance through specific behavioural tactics; it could be selected in cases of extreme parental investment asymmetry, particularly in the context of resource fluctuation, as in the scorpion R. rochai, that inhabits environments with characteristic climatic unpredictability. Female resistance through a diffuse process would function as an extremely efficient screening device. The establishment of diffuse female resistance courtship would preclude the evolution of simple/single male optimal behavioural patterns, and thus the male-female arms races would reach a more complex state, whereby varied and contextually dependent male strategies would be required to settle the reproductive game.

Is bigger better? Male body size affects wing-borne courtship signals and mating success in the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae).

Variations in male body size are known to affect inter- and intrasexual selection outcomes in a wide range of animals. In mating systems involving sexual signaling before mating, body size often acts as a key factor affecting signal strength and mate choice. We evaluated the effect of male size on courtship displays and mating success of the olive fruit fly, Bactrocera oleae (Diptera: Tephritidae). Wing vibrations performed during successful and unsuccessful courtships by large and small males were recorded by high-speed videos and analyzed through frame-by-frame analysis. Mating success of large and small males was investigated. The effect of male-male competition on mating success was evaluated. Male body size affected both male courtship signals and mating outcomes. Successful males showed wing-borne signals with high frequencies and short interpulse intervals. Wing vibrations displayed by successful large males during copulation attempt had higher frequencies over smaller males and unsuccessful large males. In no-competition conditions, large males achieved higher mating success with respect to smaller ones. Allowing large and small males to compete for a female, large males achieve more mating success over smaller ones. Mate choice by females may be based on selection of the larger males, able to produce high-frequency wing vibrations. Such traits may be indicative of "good genes," which under sexual selection could means good social-interaction genes, or a good competitive manipulator of conspecifics.

Pleiotropic actions of the male pheromone cis-vaccenyl acetate in Drosophila melanogaster.

The male-specific lipid, cis-vaccenyl acetate (cVA) has multiple functions in intra-species communication in Drosophila melanogaster. The presence of cVA in a male suppresses courtship motivation of other males and averts male–male courtship. Meanwhile, aggression behaviors between males are promoted by a high amount of cVA caused by increased densities of male flies. cVA also works as a modifier of courtship memory, which is suppressed courtship motivation driven by previous unsuccessful courtship experience. Conversely, cVA in the courting male stimulates female reproductive motivation and increases the probability of copulation success. It also works as an aggregation pheromone, attracting both males and females at the gathering spot. Thus, cVA is a unique example of a single molecule leading to different behaviors in response to the social context. However, despite recent advances in understanding the molecular and neural machinery for cVA sensing, it is still largely unknown how cVA triggers a specific behavior as the situation demands. In this review article, I discuss two potential machineries that might determine cVA actions for behavior selection at the sensory level.

Singing on the wings! Male wing fanning performances affect female willingness to copulate in the aphid parasitoid Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae).

Lysiphlebus testaceipes (Hymenoptera: Braconidae: Aphidiinae) is a generalist endoparasitoid attacking more than 100 aphid species. In L. testaceipes, wing fanning is a main male courtship display evoked by a female-borne sex pheromone. However, no information is available on the characteristics and behavioral role of male fanning during courtship in this parasitoid. Here, the courtship behavior of a wild strain of L. testaceipes was quantified and the male wing fanning performances were analyzed through high-speed video recordings and examined in relation to mating success. Courtship sequence of wild L. testaceipes did not substantially differ from that previously reported for other populations mass reared on aphids. We observed that the male courtship duration did not affect mating success. However, video analysis revealed that the males producing high-frequency fanning signals achieved higher mating success over those that display low-frequency fanning. Wing fanning before successful and unsuccessful courtship differed in amplitude of wing movements and alignment toward the mate, highlighting that frontal courtship positively influence the female mating decisions. This study increases knowledge on sexual behavior in a key parasitoid of aphids, highlighting the importance of wing fanning among the range of sensory modalities used in the sexual communication of L. testaceipes. From a practical point of view, this information is useful in L. testaceipes-based biocontrol strategies, since it can help to establish parameters for quality checking of mass-reared wasps over time.

Male Wing Fanning Performance During Successful and Unsuccessful Mating in the Parasitic Wasp Lariophagus distinguendus Förster (Hymenoptera: Pteromalidae)

Lariophagus distinguendus Forster (Hymenoptera: Pteromalidae) is a generalist solitary ectoparasitoid that parasitizes the immature stages of at least 11 foodstuff beetles from five families, including species developing in the seeds of Poaceae, Fabaceae and in dried natural products. In L. distinguendus, male wing fanning is a key phase in the courtship sequence and is elicited by a female-borne sex pheromone. However, studies aimed at understanding the role of wing vibration in L. distinguendus during courtship are lacking. In this research, the wing fanning performances of the L. distinguendus male towards other females and males were analyzed through high-speed video recordings and examined in relation to mating success. Only small differences were found between the fanning characteristics displayed toward females and young males, highlighting that young males are really perceived as females by older males. Male mating success was affected by the quality of the wing fanning in the courtship phase. Indeed, both immediately after the female perception and during mating attempts, fanning before a successful courtship differed compared to wing fanning performed prior to an unsuccessful courtship in terms of their mean frequency, but not their amplitude. Overall, our work increases knowledge of the courtship behavior of L. distinguendus and highlights the crucial importance of wing fanning among the range of sensory modalities used in the sexual communication of this parasitic wasp.

Dopamine neurons modulate pheromone responses in Drosophila courtship learning

Learning through trial-and-error interactions allows animals to adapt innate behavioural ‘rules of thumb’ to the local environment, improving their prospects for survival and reproduction. Naive Drosophila melanogaster males, for example, court both virgin and mated females, but learn through experience to selectively suppress futile courtship towards females that have already mated. Here we show that courtship learning reflects an enhanced response to the male pheromone cis-vaccenyl acetate (cVA), which is deposited on females during mating and thus distinguishes mated females from virgins. Dissociation experiments suggest a simple learning rule in which unsuccessful courtship enhances sensitivity to cVA. The learning experience can be mimicked by artificial activation of dopaminergic neurons, and we identify a specific class of dopaminergic neuron that is critical for courtship learning. These neurons provide input to the mushroom body (MB) γ lobe, and the DopR1 dopamine receptor is required in MBγ neurons for both natural and artificial courtship learning. Our work thus reveals critical behavioural, cellular and molecular components of the learning rule by which Drosophila adjusts its innate mating strategy according to experience.

Acoustic courtship songs in males of the fruit fly Anastrepha ludens (Diptera: Tephritidae) associated with geography, mass rearing and courtship success

The Sterile insect Technique (SiT) has been used successfully to control or eradicate fruit flies. The commonly observed inferiority of mass-reared males, compared with wild males, when they are paired with wild females, is apparently due to their inadequate courtship. Anastrepha ludens males produce two types of wing vibration during courtship and mating, the sound and the or precopulatory sound. There were clear differences in the calling songs between successful and unsuccessful courtships in sterile (irradiated) and fertile Mexican flies. Among sterile flies, successful males produce longer buzzes, shorter interpulses and a higher power spectrum in the signal. Fertile flies showed the same trend. For mating songs a significant dif- ference occurred in two parameters: power spectrum between sterile and fertile flies with respect to the type of song, and the signal duration and intensity were greater in non-irradiated flies. Calling songs of wild flies compared with laboratory grown flies from Mexico had shorter interpulses, longer pulses, and a greater power spectrum. However, in the case of premating songs, the only difference was in the intensity, which was sig- nificantly greater in wild males. An unexpected result was not observing pulses during pheromone deposition in wild males from Costa Rica. Comparing the premating songs of wild flies from Costa Rica and Mexico, no significant differences were observed in the duration, and the intensity of the signal was slightly greater in flies from Mexico. Rev. Biol. Trop. 57 (Suppl. 1): 257-265. Epub 2009 November 30.

Generalization of Courtship Learning in Drosophila Is Mediated by cis-Vaccenyl Acetate

Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male's strategy to suppress reproduction by competing males.

Female rock sparrows (Petronia petronia), not males, respond differently to simulations of different courtship interaction outcomes

AbstractAnimals communicate in networks which spread beyond the classic sender-receiver dyad. Researchers have often concentrated on networks of signalling males, but the network-level effects of male-female signalling interactions are largely unexplored, even though these can contain information when individuals of both sexes have access to a range of mating strategies. We tested whether rock sparrows (Petronia petronia) behave differently after hearing playbacks of vocal interactions simulating a successful courtship as opposed to playback of an unsuccessful courtship. We found no support for our prediction that males which heard a successful courtship simulation would increase the frequency of sexual behaviours compared with those which heard the unsuccessful courtship. Females which heard the successful courtship simulation stayed longer at the nest site and inside the nest box compared with those which heard the unsuccessful courtship simulation. Therefore, females responded to the treatments as if these represented different degrees of competition for either mates or nest sites. This is, to the best of our knowledge, among the first experimental demonstrations that female birds intercept signalling interactions between males and females and suggests that information available through communication networks can be relevant for an animal's choice of breeding strategy.

Mother's Milk: Frances Harper and the Circulation of Blood

Midway through Frances E. W Harper's Iola Leroy, one of the principal characters, Dr. Gresham, comes into the Union army hospital where Robert Johnson, attended by his cousin, Iola Leroy, is recovering from a wound. When Robert inquires into the doctor's recent whereabouts-a good question, since two earlier chapters of the book were devoted to his unsuccessful courtship of Iola-he launches into a rambling explanation: he was running down, was compelled to go on furlough, and is now preparing to go home, since the hospital is about to be closed. am glad this cruel strife is over, he remarks. seemed if I had lived through ages during these last few years. In the early part of the war I lost my arm by a stray shot, and my armless sleeve is one of the mementos of battle I shall carry with me through life. Then, without missing a beat, he turns respectfully toward Iola and asks her if he may ask her, as I would have some one ask my sister under the same circumstances, if you have matured any plans for the future, or if I can be of the least service to you? If so, I would be pleased to render you any service in my power.' The conversation shifts to Iola's postwar plans, and Dr. Gresham's missing arm, which has never been mentioned before, is never mentioned again. If this were an ordinary sentimental novel-or an ordinary novel, period-we would have learned of the armlessness of the heroine's suitor at an earlier moment, and the information would not have been presented in passing by the suitor himself. It would, instead, have been made visible and significant by the narrator very soon after Dr. Gresham's initial appearance in the text. And if, for some strange reason, his armlessness was at first unmentioned and then at last referred to in the course of a conversation, that reference would have led someone-the heroine, the brother, the narrator-to look at the armless sleeve. Not here. The characters in Harper's novel are quite often face-to-face with one another, insofar they spend most of their time engaged in conversation. But they almost never bestow on another character a look that gathers in such things height, weight, shape, clothing, bearing, facial expression, or the existence of limbs.

Sequential Learning of Pheromonal Cues Modulates Memory Consolidation in Trainer-Specific Associative Courtship Conditioning

Associative memory formation requires that animals choose predictors for experiences they need to remember. When an artificial odor is paired with an aversive experience, that odor becomes the predictor. In more natural settings, however, animals can have multiple salient experiences that need to be remembered and prioritized. The mechanisms by which animals deal with multiple experiences are incompletely understood. Here we show that Drosophila males can be trained to discriminate between different types of female pheromones; they suppress courtship specifically to the type of female that was associated with unsuccessful courtship. Such "trainer-specific" learning is mediated by hydrocarbon olfactory cues and modifies the male's processing of those cues. Animals that are unable to use olfactory cues can still learn by using other sensory modalities, but memory in this case is not specific to the trainer female's maturation state. Concurrent and serial presentation of different pheromones demonstrates that the ability to consolidate memory of pheromonal cues can be modified by the temporal order in which they appear. Suppression of memory by new learning demonstrates that the dynamics of memory consolidation are subject to plasticity in Drosophila. This type of metaplasticity is essential for navigation of experience-rich natural environments.

DECISIONS DURING COURTSHIP BY MALE AND FEMALE MEDFLIES (DIPTERA, TEPHRITIDAE): CORRELATED CHANGES IN MALE BEHAVIOR AND FEMALE ACCEPTANCE CRITERIA IN MASS-REARED FLIES

Analyses of more than 300 videotaped courtships of wild and mass-reared medflies from Costa Rica showed that the tendency for male and female to align themselves facing directly toward each other increased, and that the distance between them decreased as courtship proceeded. More direct alignments and shorter distances between the flies at the moment the male jumped onto the female were correlated with greater female acceptance of copulation. There were no consistent differences in durations of components of intermittent buzzing songs or male size between successful and unsuccessful courtship in either strain. Several possible cues may release different courtship responses: males of both strains tend to initiate both continuous vibration and intermittent buzzing after reduction of the distance to the female; slow creeping toward the female was associated with longer courtships that had failed to lure the female close; and females tended to turn to face more directly toward the male soon after the male began continuous vibration, and especially after he began intermittent buzzing. Females became progressively more immobile as courtship progressed, especially soon after intermittent buzzing began. There were numerous differences between strains. Mass-reared males were more likely to mount females without previous courtship than were wild males. Wild males initiated continuous wing vibration when farther from the female and when the female was looking less directly toward them, but the two strains did not differ in the distances and angles at which males initiated intermittent buzzing and jumped. Wild males were more likely to creep toward the female during intermittent buzzing. Mass-reared females but not wild females were more likely to copulate when the proportion of time the male had spent in intermittent buzzing was low, and if the courtship began when the flies were nearer each other. Wild but not mass-reared females were less likely to copulate if courtship was shorter. Possible coevolution of female responses with the five different male courtship traits that differ between mass-reared and wild flies are discussed.

Signals and responses of females and males in successful and unsuccessful courtships of three Hawaiian lek-mating Drosophilaspecies

Drosophila planitibia, D. heteroneura and D. silvestris are the three most recently evolved species of the Hawaiian picture-winged D. planitibia subgroup. Drosophila planitibiafrom Maui is the presumed ancestor of the other two species, which occur partly sympatrically on the island of Hawaii. Drosophila silvestrisis split into two morphologically different populations. The behaviour of the flies of these species/populations in successful and unsuccessful courtships was investigated. The most crucial differences between species were found in female responses (standing and walking) to male circling and in male responses to female standing and walking. Differences between D. silvestris strains were small compared with species differences. There were major differences between successful and unsuccessful matings in the response patterns most characteristic of different species.

Courtship and intersexual signaling in the parasitic waspCotesia rubecula (Hymenoptera: Braconidae)

The courtship behavior of the parasitic wasp Cotesia rubeculawas studied in a flight tunnel using standard quantitative ethological techniques. Emission of a female sex pheromone induces searching and signaling behavior in males. Males combine wing-fanning, which produces low-frequency airborne sound, with “pulsing” behavior, which transmits a vibrational signal through the substrate to the female and induces her receptivity. Female receptivity is indicated by a stereotyped antennal position, which may provide a visual or tactile signal to courting males. Comparison of successful and unsuccessful courtships indicated that courtship success was dependent primarily on the effective production or reception of the male pulse signal. Overall, the sequence of courtship behavior was similar to that reported for other parasitic wasps.

Courtship in Drosophila montana: the effects of male auditory signals on the behaviour of flies

In Drosophila montana (a species of the D. virilis group) the sounds produced by the courting male are a prerequisite for copulation. The mating behaviour of four experimental groups was recorded. Two groups consisted of single pairs of normal flies with successful and unsuccessful courtship, respectively. The third group consisted of single pairs of normal males and deaf females and the fourth group of single pairs of mute males and normal females. In successful courtships (i.e. those ending in copulation) touching and licking by the male led to female standing. Female standing led to male wing vibrating, male wing vibrating to female wing lifting, and female wing lifting to copulation. In unsuccessful courtships, the males did not vibrate their wings in response to female standing. In the groups lacking male auditory signals (deaf females or mute males) the females hummed their wings in response to male licking and wing vibrating. Although the males responded to wing humming by more licking and by producing more sounds, the courtships did not proceed to copulation. It is concluded that the willingness of the female to mate with a conspecific male depends on the detection of sound at the appropriate time in the courtship sequence as a response to female behaviour.

The courtship behavior of the cabbage moth,Mamestra brassicae (Lepidoptera: Noctuidae), and the role of male hair-pencils

The courtship behavior of the cabbage moth, Mamestra brassicae(L.), was studied in moving air conditions in a wind tunnel, using video techniques. Quantitative analyses were undertaken to determine the behavioral sequence occurring in the courtship. Comparison of successful and unsuccessful courtship suggested that courtship success was more dependent on the behavior of the female than that of the male. In an attempt to elucidate the function of the male hair-pencils (HPs), courtships involving males without HPs were also studied. HP removal did not affect the overall courtship success rate of males, but detailed analysis showed significant changes infernale behavior during such courtships. HP removal also affected female behavior following pair formation, with females struggling more when paired with males without HPs. Consequently, it is proposed that the HP volatiles act as an arrestant for the female, both during courtship and after pair formation, to increase female acceptance and to prevent premature termination of copulation. Experiments were also conducted to test previous hypotheses for HP function. However, no evidence was found to suggest that the HP volatiles in M. brassicaeact to attract females, affect female calling behavior, or affect the behavior of other males. A further possible function of HPs in defense is discussed.

Male displays and female preferences in the courtship of a gregarious cricket

The courtship of males of the gregarious cricket Amphiacusta maya involves a variety of signals. The quantitative aspects of both successful and unsuccessful courtship sequences were examined to determine whether certain aspects of male displays were correlated with female mating preferences regardless of which male performed them. Although variability among males was high for most courtship components measured, I found no evidence of female choice with respect to the courtship variables studied. About 35% of the duration of each male courtship sequence is devoted to chirping, but there were no differences in either the likelihood of copulation or the latency to copulation between normal males and experimentally silenced males. The possibility that intrinsic differences in male quality explained the variability in courtship duration was examined with a two-way analysis of variance. The variance in courtship duration was attributable to variance among females, not to variance among males. Thus the courtship behaviour of male A. maya is variable enough to allow females to exert stabilizing or disruptive selection on displays, but there is no evidence that females use the available information.