Evolutionary trends in the male pheromone systems of arctiid moths: evidence from studies of courtship in Phragmatobia fuliginosa and Pyrrharctia isabella (Lepidoptera: Arctiidae)

Male Phragmatobia fuliginosa and Pyrrharctia Isabella evert tubular abdominal scent-organs (coremata: during courtship. The coremata secrete a pheromone that is derived from pyrrolizidine alkaloids (PAs) obtained during larval feeding. Field-collected males vary widely in the amount of pheromone they possess. The courtship behaviour of these species was studied to determine whether this variation among males serves as a basis for mate choice by females, in a wind-tunnel a male approaches a pheromone-releasing female from downwind with his coremata everted in flight. A female perceiving the pheromone responds by fluttering her wings and emitting a clicking sound. This response did not occur in all courtships, and successful copulation was not dependent on its occurrence. Males denied access as larvae to the PA-precursors of the corematal pheromone (PA-denicd males' mated as rapidly as males allowed access to pheromone precursor (PA-supplied males). Moreover, antennectomized females mated as rapidly as normal females. Comparative analyses of transitional probabilities indicated no differences among courtships involving ! I': PA-denicd males and normal females, (II) PA-supplied males and normal females, or antennectomized females and normal males of unspecified feeding history. Field observations of courtship interactions between laboratory-reared females and wild males indicated that males having little or no pheromone succeed in mating in a natural setting as do males having a relativelv large amount of pheromone. It is hypothesized that the failure of female Ph. fuliginosa and Py, Isabella to enforce the display of PA-derived pheromone is related to an cvolutionarv trend away from an ancestral larval host-range restricted to PA-containing plants toward the polyphagv shown by manv temperate and arctic arctiids in the lineage (subfamily Arctiinae: tribe Arctiini) to which Ph. fuliginosa and Py. Isabella belong. Parallels in other moth groups are cited to support the notion that a plesiomorphic courtship pheromone system could persist in a vestigial state, despite the loss of its adaptive raison dêtre.     

Mating behaviour and reproductive isolation of three species of reptile tick

The mating behaviour of three species of reptile tick, Aponomma hydrosauri, Amblyomma albolimbatum and Amb. limbatum is similar and involves a female sex pheromone which activates males to detach from their hosts and search. After contacting females, a stereotyped six-phase courtship sequence occurs. There are qualitative differences between the species in courtship behaviour at phase 3 (reversal of position by dorsally mounted males) and phase 6 (the copulation position). On-host observations of non-conspecific mating show that females of the three species have species-specific activation pheromones, which is contrary to reports in other species of tick. Such specificity should result in reproductive isolation of the three species; however, under certain circumstances it may not prevent non-conspecific contacts between the sexes. Off-host observations of courtship behaviour show that once males of the three species contact non-conspecific females, they attempt courtship and are persistent with their courtship. Rarely did non-conspecific courtships proceed beyond phase 4 of the courtship sequence, as non-conspecific females did not lift their bodies to allow males venter contact. Differences between the species in leg orientation in the copulation position, together with body size differences, are responsible for a complete barrier to successful non-conspecific copulation. The observations illustrate the role that behavioural mechanisms play in reproductively isolating these three species of tick.     

Interactions of the Males and Females of Three Sympatric Drosophila virilis-Group Species, D. montana, D. littoralis, and D. lummei, (Diptera: Drosophilidae) in Intra- and Interspecific Courtships in the Wild and in the Laboratory

Four species of the Drosophila virilis group, D. montana, D. littoralis, D. lummei, and D. ezoana, occur sympatrically in several locations in northern Europe. Courtship interactions between the flies of the three first-mentioned species were observed at malt baits in Kemi, northern Finland, to find out how the flies of different species recognize conspecific individuals and how interspecific courtships differ from intraspecific ones in the wild. Intraspecific courtships (including females of different reproductive stages) and interspecific courtships were also videotaped and analyzed in laboratory. In the wild the males courted both conspecific and allospecific females, even though the species varied in how much the males were attracted to females of different species. Interspecific courtships usually broke off when the male touched the female or when the male and/or the female vibrated his/her wings, producing acoustic cues. In the laboratory males courted conspecific females irrespective of the reproductive stage of the female, even though the courtships directed toward immature and fertilized females usually included only orienting and touching (no licking and singing). D. littoralis, and very rarely D. montana and D. lummei, males courted also allospecific females. In the few interspecific courtships between these three species, where the male proceeded to singing, females responded to male singing by vibrating their wings. This ended the courtship. It is suggested that both the chemical cues affecting female attractivity and the acoustic signals of males and females, which are produced by wing vibration, function in maintaining sexual isolation between these three species.     

Visual and Olfactory Female-Borne Cues Evoke Male Courtship in the Aphid Parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae)

We investigated the courtship and mating behavior of the pan-tropical polyphagous endoparasitoid Aphidius colemani Viereck. The courtship and mating displays, the magnitude of male-male sexual approaches and the role of female-borne cues evoking male courtship behavior were quantified. The sequence of events leading to copulation in this parasitoid did not differ from that found for other braconids. Females refused to copulate more than once. Same-sex courtships were observed among males and their possible role in an adaptive context is discussed. Olfactory female-borne cues played a key role in eliciting the courtship responses of males. Males were attracted by freshly dead females, but not by dead females soaked in hexane, nor by visual cues from females alone. Intense male wing fanning behavior was elicited by crushed abdomens of virgin females, suggesting that the female abdomen is the source of a short-distance pheromone crucial in evoking male courtship. Further studies are required to clarify the exact nature of the chemicals involved.     

Pheromonal inhibition of male courtship behaviour in the brown tree snake, Boiga irregularis: a mechanism for the rejection of potential mates

Pheromones play a central role in coordinating the events leading up to copulation in snakes. We report here a novel pheromone system in the brown tree snake in which females release a pheromone that inhibits male courtship behaviour. In a previous study, we made observations of female brown tree snakes releasing cloacal secretions (CS) during courtship that appeared to cause courting males to cease courtship. All snakes have glands that release CS through ducts located along the cloacal orifice. Although CS have been studied for many years, their function in the mediation of snake behaviour has not been experimentally well determined. We examined the role of CS in the reproductive behaviour of male and female brown tree snakes. We conducted four experiments to test the effect of both male and female CS on brown tree snake behaviour under two behavioural contexts, courtship and male-male ritualized combat. Within each experiment, we compared the effects of CS to a control. Female CS caused a decrease in the time that males spent courting females and a decrease in the intensity of courtship compared with the control treatment. Male CS did not, however, affect the time that males spent displaying courtship or the intensity of that courtship. Neither male nor female CS had significant effects on male ritualized combat behaviour, including time that males spent in combat or the intensity of combat behaviours displayed. Furthermore, neither female nor male CS had an effect on female courtship versus controls. The inhibition of brown tree snake reproductive behaviours is specific to female CS inhibiting male courtship behaviour. This pheromone acts in concert with the female sex pheromone to regulate the events leading to copulation.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Sexual behaviour of Anastrepha obliqua (Macquart) (Diptera: Tephritidae): Do laboratory domestication conditions influence male courtship behaviour?

We analysed the influence of laboratory domestication, under relaxed conditions, on the courtship behaviour of the fruit fly species Anastrepha obliqua, an important agricultural pest. We compared the temporal patterns of pheromone emission (Calling behaviour) and the frequencies and sequences of the courtship behavioural units of males of a laboratory lineage and a wild lineage. Our results indicated similarities in the temporal behavioural patterns of calling, the durations of their behavioural sequences, the final sequences of courtships resulting in copulation, of wild and laboratory males. Differences, however, were observed between the two populations in terms of the frequencies of the behavioural units executed and the initial sequence of courtship. Differences were noted in the presence or absence of some behavioural units within the courtship behavioural repertoires of the laboratory-reared and wild. The wild males did not show units such as Alignment, Contact, Fighting and Marking Leaf that were observed in the laboratory males' courtship behaviour under laboratory conditions; on the other hand, laboratory males did not show the Abdominal movements and Oscillation observed in the courtship behaviour of wild males. The rearing of A. obliqua males under relaxed conditions in the laboratory provides an environment adequate for the preservation of behavioural characteristics relevant to the successful mating, such as Movement, Arrowhead 1, and Attempt, and in temporal patterns of pheromone emission.     

Male moth songs tempt females to accept mating: the role of acoustic and pheromonal communication in the reproductive behaviour of Aphomia sociella

Background

Members of the subfamily Galleriinae have adapted to different selective environmental pressures by devising a unique mating process. Galleriinae males initiate mating by attracting females with either chemical or acoustic signals (or a combination of both modalities). Six compounds considered candidates for the sex pheromone have recently been identified in the wing gland extracts of Aphomia sociella males. Prior to the present study, acoustic communication had not been investigated. Signals mediating female attraction were likewise unknown.

Methodology/Principal Findings

Observations of A. sociella mating behaviour and recordings of male acoustic signals confirmed that males initiate the mating process. During calling behaviour (stationary wing fanning and pheromone release), males disperse pheromone from their wing glands. When a female approaches, males cease calling and begin to produce ultrasonic songs as part of the courtship behaviour. Replaying of recorded courting songs to virgin females and a comparison of the mating efficiency of intact males with males lacking tegullae proved that male ultrasonic signals stimulate females to accept mating. Greenhouse experiments with isolated pheromone glands confirmed that the male sex pheromone mediates long-range female attraction.

Conclusion/Significance

Female attraction in A. sociella is chemically mediated, but ultrasonic communication is also employed during courtship. Male ultrasonic songs stimulate female sexual display and significantly affect mating efficiency. Considerable inter-individual differences in song structure exist. These could play a role in female mate selection provided that the female''s ear is able to discern them. The A. sociella mating strategy described above is unique within the subfamily Galleriinae.     

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.     

The role of signals of different modalities in initiating vibratory communication in Nezara viridula

Signals of different modalities are involved in the behaviour of the green stink bug, Nezara viridula (L.) (Pentatomidae, Heteroptera). Long range attraction is mediated by male pheromones, resulting in aggregation of bugs on the same plant where vibratory signals, vision and various chemical signals become important. Both males and females sing spontaneously. When both are on the plant, males start vibratory communication as often as females. Females induce the exchange of vibratory signals spontaneously or triggered by the male pheromone while males initiate the duet either spontaneously or after seeing the female. Males and females sing spontaneously and respond to signals of different modalities more often in the daylight than in the dark. Long lasting autonomous emission of the female calling song is present when triggered by the male pheromone and males respond to female calling predominantly by the emission of the courtship song.     

Sexual behaviour: female swift moth is not the aggressive partner

Observations on three naturally-occurring courtships of Hepialus show that sexual behaviour in these moths is similar to that of butterflies, with the male pursuing the female in flight and mating with her after she alights. Although the female appears to solicit courtship by flying past a hovering male, and although the male becomes flaccid immediately after copulation, it is not true that the female flies directly at the male and knocks him out of the air, as is widely held by moth-collectors.     

FUNCTIONAL ASPECTS OF DROSOPHILA COURTSHIP

1. The elements that make up the courtship behaviour of males and of females are briefly described. It is pointed out that some of the terms used, such as female ‘repelling’ behaviour, are misleading as they do not reflect the known functions of the behaviours. 2. Evidence has been presented for a number of distinct pheromones with different functions during courtship. These claims are critically examined as the evidence is incomplete and at times conflicting. It seems unlikely that any pheromones other than those acting over a very short distance are involved in courtship. There is sound evidence for an aphrodisiac pheromone produced by all females which stimulates male courtship. A pheromone, which may be the same one, is produced by males less than 12 h old, which also stimulates male courtship. No function is ascribed to this pheromone. Fertilized females either produce less aphrodisiac pheromone or they may, in addition, produce one that inhibits male courtship. Mature males may also produce an inhibitory pheromone. Females produce a contact pheromone which is species-specific and involved in sexual isolation. It is not at present clear whether this is different from the aphrodisiac pheromone. 3. There is considerable variability in the importance of vision in courtship. Many species will mate satisfactorily in the dark, suggesting that visual stimuli are not critical. Most species use vision to orient towards one another and for males to track and follow females. Even in light-independent species such as D. melanogaster, specific visual signals may be used in courtship although they are not obligatory. Thus the red eye of the male is a sexual signal for females. Conversely, some light-dependent species do not appear to make use of visual signals as a major factor in courtship. Some, however, do perform behaviours that are clearly visual and which may act to emphasize markings on wings, head or body. 4. The majority of Drosophila species perform courtship songs by vibrating one or both wings. The songs produced by males sexually stimulate the females. They are species specific and there is considerable indirect and some direct evidence that the songs are involved in sexual isolation. Males of many species produce two different songs during courtship and it is probable that one is concerned mainly with sexual stimulation and the other with species recognition. Females of certain species of Drosophila and Zaprionus also sing during courtship and these songs may aid species recognition by males. In addition males and unreceptive females perform ‘aggressive’ songs. 5. Almost all studies of Drosophila courtship have been made in very confined conditions in the laboratory. Interpretation of some of the results obtained in this way may require modification in the light of ecological research and observation of courtships under more natural conditions.     

Male Courtship Pheromones Affect Female Behaviour in the Swordtail Characin (Corynopoma riisei)

Pheromones constitute an important cue used by both males and females during courtship. Here, we investigate the effect of male pheromones on female behaviour in the swordtail characin (Corynopoma riisei), a species of fish where males have a caudal pheromone gland which has been suggested to affect female behaviour during courtship. We subjected female C. riisei to male courtship pheromones and investigated the effect on both female behaviour and brain serotonergic activity levels compared to a control group. While no difference in serotonergic activity was found, the pheromone‐treated females showed lower stress levels compared to the control group. Furthermore, pheromone‐treated females increased locomotor activity over time, while a decrease in locomotor activity was observed in the control group. These results suggest that the male courtship pheromones may serve to reduce female stress and increase female activity, possibly to aid males in gaining access to females and facilitating sperm transfer.     

Mate choice by wild and mass‐reared females of the Mediterranean fruit fly

The sterile insect technique (SIT) is used to control Mediterranean fruit fly, Ceratitis capitata (Wiedemann), but its effectiveness is limited by low sexual competitiveness of mass‐reared males. This study investigated whether wild and mass‐reared [from a temperature sensitive lethal (tsl) genetic sexing strain] females display similar mate preferences and thus exert similar selective forces on the evolution of male courtship behaviour. Wild females preferred wild males over tsl males, whereas tsl females mated indiscriminately. The probability that mounting resulted in copulation was related to the duration of pre‐mount courtship for wild females, and wild males performed longer courtships than tsl males. Copulation occurred independently of courtship duration in tsl females. Counter to the aim of the SIT, female choice by tsl females appears to promote the evolution of male behaviour disfavoured by wild females.     

Emergence, Mating, and Postmating Behaviors of the Oriental Beetle (Coleoptera: Scarabaeidae)

In a previous field-trapping study of the oriental beetle, Exomala orientalis (Waterhouse), by using synthetic sex pheromone on golf course fairways, numerous males were observed and trapped during the hours of peak mating activity. However, very few beetles were observed in the same areas when synthetic pheromone was absent. To investigate the hypothesis that mating in nature occurs cryptically within vegetation at the soil surface, laboratory studies on female emergence and pheromone release, male emergence and mate-locating, and female and male mating behaviors were conducted. Mate acquisition and copulation occurred on the soil surface near the female emergence site, with both sexes engaging in pheromone-mediated behaviors after having emerged from the soil. A highly stereotyped female pheromone release, or calling, behavior was observed, consisting of insertion of the female's head into the soil and elevation of the tip of her abdomen into the air. Bioassays conducted in a wind tunnel that simulated a turf fairway environment showed that walking and flying were both important in the upwind response of males to females. Mating and copulation occurred without an obvious complex courtship, but observations of postmating behaviors suggested that mate guarding occurs.     

Wing-flick Signals in the Courtship of the African Cave Cricket,Phaeophilacris spectrum

The male of the African cave cricket Phaeophilacris spectrum (Saltatoria: Grylloidea: Phalangopsidae) possesses tegmina without stridulatory organs, and both females and males lack tympanal organs. Therefore acoustic communication in the usual sense, which is typical for most crickets, is absent in this species. However, adaptations of the wing articulation allow the males to flick their wings forward over their heads. During courtship these movements are performed in series of 4–5 wing-flicks at a rate of 8–12 Hz (called wing-flick series = WFS) which elicit low-frequency air movements. Such signals may have taken over the functional significance of an acoustic ‘courtship song’. A quantitative analysis of the cricket's behaviour showed that in terms of frequency and total duration, ‘wing-flick series’ and ‘rocking’ behaviour are the most prominent signals of the male's courtship display. Moreover, analysis of the spatial relationships between male and female demonstrates that the wing-flicking is directed towards the female. The response of a female to a wing-flicking, courting male seems mainly to be calmed down and to reach a passive, receptive state, necessary for subsequent copulation. Females confronted with a male's courtship display exhibited a significantly higher threshold to disturbing stimuli than uncourted ones.     

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.     

Pheromonal emission during the mating behavior ofEurycotis floridana (Walker) (Dictyoptera: Blattidae)

The sexual behavior of males and females ofEurycotis floridana was investigated and the various associated behavioral sequences are described. Olfactometer data proved that the male produces a volatile sex pheromone attractive at a distance to conspecific females. The male initiates courtship behavior by exposing the glandular areas on the anterior parts of abdominal tergites 2, 7, and 8. This male calling behavior was observed throughout the day. The males can mate when 8 days old, whereas virgin females are sexually receptive 18 days after becoming adults. Once attracted near the male, the female opens her genital atrium and climbs on the back of the male, where she feeds on the glandular secretions that oozed around a little tuft of setae on the first tergite. These setae are mechanoreceptors and they are stimulated when licked by the females, which informs the male that she is in a proper position for copulation.     

Mating behavior ofPhytoecia rufiventris Gautier (Coleoptera: Cerambycidae)

Sexual behavior between males and females, as well as between males, is described and discussed for the cerambycid beetlePhytoecia rufiventris. The beetles' taxis toward plants taller than average height brings the sexes together from a distance. A male may mount another individual (male or female) and attempt copulation without sex discrimination. The male can discern the sex of another individual only when the terminal part of his abdomen touches the ventral surface of the fifth visible sternite of the latter. No evidence of a sex pheromone is found in this species. Within 1.5–5.5 cm the substrateborne vibrations produced by a moving individual may be the important factor which elicits males to approach a moving individual and attempt copulation. If a female is receptive when a male touches her, he can copulate with her without any courtship display. However, if the female runs away and appears unreceptive, the male will perform courtship displays. Copulation is usually terminated by males. Homosexual behavior between males is discussed.     

Female Choice or Male Sex Drive? The Advantages of Male Body Size during Mating in Drosophila Melanogaster

The mating success of larger male Drosophila melanogaster in the laboratory and the wild has been traditionally been explained by female choice, even though the reasons are generally hard to reconcile. Female choice can explain this success by virtue of females taking less time to mate with preferred males, but so can the more aggressive or persistent courtships efforts of large males. Since mating is a negotiation between the two sexes, the behaviors of both are likely to interact and influence mating outcomes. Using a series of assays, we explored these negotiations by testing for the relative influence of male behaviors and its effect on influencing female courtship arousal threshold, which is the time taken for females to accept copulation. Our results show that large males indeed have higher copulation success compared to smaller males. Competition between two males or an increasing number of males had no influence on female sexual arousal threshold;—females therefore may have a relatively fixed ‘arousal threshold’ that must be reached before they are ready to mate, and larger males appear to be able to manipulate this threshold sooner. On the other hand, the females’ physiological and behavioral state drastically influences mating; once females have crossed the courtship arousal threshold they take less time to mate and mate indiscriminately with large and small males. Mating quicker with larger males may be misconstrued to be due to female choice; our results suggest that the mating advantage of larger males may be more a result of heightened male activity and relatively less of female choice. Body size per se may not be a trait under selection by female choice, but size likely amplifies male activity and signal outputs in courtship, allowing them to influence female arousal threshold faster.     

Courtship Behaviour and Mating in Two Cow Dung Inhabiting Sphaerocerid Flies (Diptera: Sphaeroceridae)

Adults and larvae of Coproica lugubris and Chaetopodella scutellaris (Diptera: Sphaeroceridae) occur in great numbers on cow droppings. Courtship behaviour and copulation were analyzed and compared. Striking differences were found in the complexity and number of courtship patterns. In contrast to C. lugubris, where males usually mount females without performing any displays, courtship of Ch. scutellaris is rather complex: a male approaches a female and positions himself facing her; he then starts to circle her in a fashion very similar to a male courtship pattern in Drosophila species. Females usually respond to circling with a typical behaviour pattern I called swaying. Its function is discussed. The complex courtship behaviour of Ch. scutellaris is interpreted as a mechanism for female choice. In Ch. scutellaris copulation takes about 60 min longer than in C. lugubris, but the mechanism based upon this obvious difference is not understood. Females of both species can effectively prevent males from copulating.