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.     

Olfactory conditioning in mate searching by the parasitoid Aphidius ervi (Hymenoptera: Braconidae)

Despite the fact that insect learning capacity has been broadly demonstrated, the role that this process plays during mate searching has been scarcely explored. We studied whether the sexual behaviour of a male parasitic wasp can be conditioned to the odours from two alternative host plant complexes (HPCs) present during its first copulation. The experimental subjects were newly emerged males of the aphid parasitoid, Aphidius ervi, and two alternative HPCs (alfalfa or wheat). In the training protocol, copulation experience corresponded to an unconditioning stimulus and HPC odours to the conditioning stimuli. The initial (just after eclosion) and trained responses were assessed in a glass Y-olfactometer. The results showed that neither alfalfa HPC nor wheat HPC stimuli elicited sexual-related behaviours in initial male responses. Conversely, both HPCs triggered strong attraction and wing fanning courtship behaviour in trained responses when the male was exposed to a female plus HPC during training. In males trained with females plus a given HPC but tested with the alternative HPC in the olfactometer, trained response showed a similar trend to the non-associative treatments. Hence, through learning, the olfactory stimulus context present during copulation could become a predictive cue for further mate searching. These results are discussed in terms of parasitic wasp ecology and host fidelity.     

Evidence for acoustic communication in the parasitoid wasp Glyptapanteles flavicoxis

Females of the parasitoid wasp Glyptapanteles flavicoxis (Marsh) (Hymenoptera: Braconidae) deposit sex pheromone on substrate that elicits attraction and wing fanning in conspecific males. We tested the hypothesis that wing fanning sound induces a behavioral response from females which, in turn, affects the males’ orientation toward them. Females exposed to playback of the males’ wing fanning sound engaged in short flights, with sound characteristics different from those of the males’ wing fanning sound. In two‐choice bioassays, playback of the females’ flight sound attracted significantly more males than a silent control stimulus, and in combination with pheromone‐containing body extract of females it attracted more males than female body extract alone. Our data support the conclusion that the males’ wing fanning induces sound and visual reply signals from females that help males orient toward them.     

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.     

Search behavior of pheromone-stimulated potato tuber moth males (Lepidoptera: Gelechiidae)

The processes of female searching by male potato tuber moths,Phthorimaea operculella, were analyzed. The behavioral components to copulation were antennal cleaning, quiescence, walking, wing fanning, contact with female, hair brush display, copulation attempt, and copulation. Males did not always succeed in mating on their first attempt. Searching behavior of males changes to “area-restricted searching” after contact with a female. Males could, therefore, find females efficiently and copulate.     

Wing development in parasitized male and female Sitobion fragariae

Abstract.Different stages of presumptive winged morphs (males, gynoparae and alate virginoparae) of the blackberry‐cereal aphid, Sitobion fragariae , were exposed to attack by Aphidius ervi . Even though the mechanism influencing wing development in the three aphid morphs differs, the effects of parasitism were similar. Alatiform structures were completely inhibited in all three morphs when the initial attack took place in their first or early second stadium. The disruption of wing development also resulted in apterous/alate‐intermediate forms when aphids were attacked from first (males and gynoparae) or early second (alate virginoparae) up to the fourth larval stadium. The fact that wing development was still disrupted when aphids with well developed wingbuds were parasitized indicates that the early stages of parasitization were influential. Thus, the morphogenetic effects may be exerted by the parasitoid egg or calyx fluid.     

The influence of parasitism on wing development in male and female pea aphids

Wing formation in presumptive alate morphs (virginoparae and males) was observed for the pea aphid, Acyrthosiphon pisum, exposed to attack by the parasitoid, Aphidius ervi, at different stages of host development. Morphological abnormalities in parasitized aphids such as complete apterization (development of a wingless form), formation of rudimentary wing buds, and deformed wings indicate a possible disruption of the endocrine system. Changes in the body shape and the number of olfactory secondary rhinaria on the antennae could indicate an influence of juvenile hormone in parasitized A. pisum but the development of fifth-stadium supernumerary larvae (indicated by an extra moult and which can be induced by exogenous juvenile hormone treatments) was not found in parasitized aphids. In addition, while apterization of virginoparae can also be induced by the pro-allatocidal compound Precocene III, this was not possible in the male. Males which survived parasitoid attack without forming aphid mummies (indicating that oviposition had not occurred) developed as wingless individuals suggesting that the reproductive-tract-fluids from the female parasitoid were important in the wing inhibition process. Teratocytes from the parasitoid appeared to promote developmental arrest in parasitized aphids.     

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

Lariophagus distinguendus Förster (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.     

Mating Status Effects on Sexual Response of Males and Females in the Parasitoid Wasp <Emphasis Type="Italic">Urolepis rufipes</Emphasis>

Although mate preferences are most commonly examined in females, they are often found in both sexes. In the parasitoid wasp Urolepis rufipes, both female and male mating status affected certain aspects of sexual interactions. Female mating status mattered only in the later stages of mating. Males did not discriminate between virgin and mated females in terms of which they contacted or mounted first. However, once mounted, most virgin females were receptive to copulation, whereas very few mated females were. Whether a male’s mating status affected his own sexual response depended on the female’s ability to respond and the stage of mating. Examining male behavior toward dead females allowed elimination of the role of female behavior in how males responded. Virgin and mated males are both attracted to dead females as evidenced by their fanning their wings at such females. However, mated males were quicker than virgin males to contact and to mount in an experiment with dead females, whereas there was no such differential response in an experiment with live females. This difference is consistent with greater female sexual responsiveness to virgin males. Male mating status also affected female receptivity to copulate. Once mounted, live virgin females were less likely to become receptive to copulation by mated males than to virgin males, but only in a choice experiment, not in a no-choice experiment.     

Inhibiting aphid wing development: is immune challenge important?

Aphids show inhibition of wing development when parasitized by hymenopteran parasitoids, especially when parasitism takes place early in the host's development. The present study tests the hypothesis that the aphid itself redirects the resources needed for the development of wings to support the immune response, rather than the parasitoid directly promoting wing inhibition. When the aphid's immune system is challenged with bacterial antigens and a fungal pathogen, neither immune challenge alters wing development, indicating that perhaps there is no redirection by the aphid of resources required for wing development to cover possible costs of mounting an immune response.     

Female wing spreading as acceptance signal in theDrosophila virilis group of species

Females of manyDrosophila species spread apart their wings prior to copulation. In the present study we found female wing spreading to provoke male copulation attempts inDrosophila virilis-group species, helping the males to attempt copulation when the female is ready to mate. The males of most species, however, rarely responded to female wing spreading by copulation attempt without licking the female genitalia before and/or after female wing spreading bout. Blocking the female genitalia (D. virilis, D. novamexicana) reduces males' tendency to attempt copulation after female wing spreading. In these, and most other species of the group, female wing spreading seems to be an efficient signal only when combined with stimuli from female genitalia.     

Location,morphology and histology of sex pheromone glands of the female gypsy moth, Lymantria dispar (L.)

Scanning electron microscopy, histology and a male wing fanning bioassay were used in this study to locate the sex pheromone-producing glands of the female gypsy moth, Lymantria dispar. When exposed to female sex pheromone, adult males exhibit a strong wing fanning behaviour prior to take off. We found that adult males showed positive response to calling females and to tissue extract from both dorsal and ventral portions of the intersegmental membrane between 8th and 9th-abdominal segments. A typical male response usually starts with elevation of antennae, movement of head in different directions, walking, wing fanning and onset of search flight. Histological and scanning electron microscopic studies suggested that the sex pheromone glands are located on the dorsal and ventral aspects of the intersegmental membrane. The glands appear as two highly convoluted integumentary areas with hypertrophied glandular epidermal cells.     

Lack of behavioural evidence for kin avoidance in mate choice in a hymenopteran parasitoid (Hymenoptera: Braconidae)

Mechanisms for inbreeding avoidance should be prevalent in insects that reproduce by arrhenotokous haplodiploidy because of the higher potential production of unviable diploid males in inbred matings. Few studies have focused on mating strategies in insect parasitoids and even less on kinship relationships during mate choice. In this study we tested avoidance of kin as mate in the parasitic wasp Aphidius matricariae (Hymenoptera: Braconidae) using an ethological approach. Key mating parameters, such as male wing fanning, latent period before genitalia contact and duration of copulation were measured. No evidence for kin avoidance in mate choice in both A. matricariae males and females was observed in our behaviour (no choice or choice tests) tests. This lack of ethological sib mating avoidance could be due to different factors such as sex determination rule different than the single locus complementary sex determination, making lower the proportion of diploid males in case of sib matings and thus its negative consequence. The existence of other inbreeding avoidance strategies and mechanisms that reduce the probability of 2 receptive relatives meeting in nature may be common, for example, inbred mating may be rare through differential dispersal, delayed maturation, or protandry.     

Avoidance of maladaptive,precocious copulation in the cabbage white butterfly,Pieris rapae crucivora

In the cabbage white butterfly, Pieris rapae crucivora, copulation hinders normal expansion and hardening of the wings of newly emerged females. The resulting permanent wing deformation makes it impossible for females to fly and therefore, to find an oviposition site and nectar sources. An attempt was made to clarify whether the newly emerged female butterfly avoids copulation. Observation of wing expansion and hardening reveals that the wings are fully expanded and hard by 20–30 min after emergence. In the field, presentation of females with soft wings to males shows that males will attempt to copulate with these females. However, newly emerged females prevent successful completion of copulation by assuming the mate refusal posture, and thereby avoid a potentially maladaptive copulation. The discussion focusses on the question as to why females and not males avoid early copulation.     

May the wild male loose? Male wing fanning performances and mating success in wild and mass-reared strains of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae: Aphidiinae)

Aphidius colemani Viereck (Hymenoptera: Braconidae) is a pan-tropical broadly oligophagous endoparasitoid of many aphids of economic importance, including Aphis gossypii Glover and Myzus persicae (Sulzer). While the trophic interactions occurring among A. colemani and its hosts have been extensively studied, little is known about the male- and female-borne cues that guide mating dynamics. Male wing fanning has been found to play a key role in A. colemani courtship, as successful mounting of females without initial wing fanning has never been observed. In this research, we analyzed wing fanning performance and mating ability of males from three different strains of A. colemani: wasps commercially mass-reared on A. gossypii, wild wasps from parasitized A. gossypii, and wild wasps from parasitized Aphis nerii Boyer de Fonscolombe. Results showed that virgin females did not rely on particular male fanning features during mate choice. Moreover, when A. colemani individuals developed on A. gossypii, no major differences were detected in courtship and mating ability between field collected and mass-reared wasps. In contrast, courtship performance and mating success varied between wild A. colemani males reared on different hosts, with those developing on A. nerii having lower quality wing fanning performance during the mounting attempt phase, and reduced ability to compete for females with other males reared on A. gossypii.     

人工合成草地螟雌蛾性信息素的初步筛选

在初步筛选过程中,主要成份反11十四碳烯醋酸酯(E1114:AC)能引起草地螟Loxostege sticticaiis L.雄蛾完成从兴奋到搜索释放源的行为,但雄蛾对单个组分E1114:AL、E1114:OH、14:OH、14:AC、12:OH不呈现任何反应。当释放源为二元组分或三元组分时,可以明显增加雄蛾定向飞行和达到释放源的数量。筛选出二元组分为(E1114:AC):(E1114:AL)=1:1和三元组分(E1114:AC):(E1114:AL):(14:OH)=5:3:12时效果最佳。田间试验中进一步筛选出三元组分(E1114:AC):(E1114:AL):(14:OH)=5:3:12为最佳组分。     

Regulation of wing formation and adult development in an aphid host, Aphis fabae, by the parasitoid Aphidius colemani

Nymphs of presumptive winged gynoparae of Aphis fabae (Hemiptera: Aphididae), were exposed to female parasitoids, Aphidius colemani (Hymenoptera: Aphidiidae) and stung once with the ovipositor. Wing development was inhibited and, when aphids were parasitised during the early stages, they did not reach the adult stage but mummies with rudimentary or no wingbuds are observed in the host's fourth-stadium. These and previous studies have suggested that wing development may be inhibited by factor(s) from the maternal parasitoid injected into the host at the time of oviposition. In an attempt to identify such factor(s), saline extracts of whole female parasitoids, abdomens, ovaries and venom glands were prepared. When a saline extract of venom glands was injected into late-second-stadium aphids, many develop to fourth-stadium nymphs with rudimentary wingbuds, indicating an effect on wing formation but also showed developmental arrest and often died when attempting to moult to the adult stage. It appears that host death may be related to physiological/biochemical interactions of parasitoid and host rather than just late stage parasitoid larvae ingesting the host's vital organs. Injections with extracts into later host stadia gave similar results with regard to development to the adult, although aphids injected in the late-fourth-stadium develop normally to the adult stage with no effect on wing formation. The results indicate that the earlier the injection before the final moult the greater the effect of the injected extract on preventing adult development.Extracts prepared from head + thorax do not affect aphid development and the results indicate that there is an active factor(s) - likely a protein - in the female parasitoid's venom that disrupts wing development and/or inhibits development to the adult stage. Surprisingly, injections of extracts from male parasitoids have similar effects but the location and function of such a factor(s) in males are unknown.     

The courtship behaviour of Yponomeuta padellus

The sequence of behavioural steps from male attraction until copulation is described and analyzed for Yponomeuta padellus L. (Yponomeutidae, Lepidoptera). Males respond to a pheromone emitting female with wing fanning followed by upwind zigzagging flight. Males will land near the females and then walk while wing fanning. The antennae drum onto the substratum and the abdominal-hair pencils are displayed. When in contact with a female the male drums with his antennae onto wings, head and antennae. Mostly a clasping attempt follows. A male has a higher chance to be accepted when he firt encounters the rear of a female instead of the head. Females refuse males by walking away or wing fanning or a combination of both.

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Résumé Les séquences du comportement depuis l'attraction du mâle jusqu'à la copulation ont été décrites et analysées chez Y. padellus (L.). Les mâles réagissent à une femelle émenttant une phéromone par un hattement d'ailes suivi d'un vol en zigzag contre le vent. Les mâles atterriront près des femelles et marcheront avec leurs ailes en battement. Les antennes tambourinent le substrat et les pinceaux abdominaux sont déplyés. Lorsqu'il est au contact de la femelle, le mâle tambourine avec ses antennes les ailes, la tête et les antennes. Généralement suit une tentative d'étreinte. Les chances de succès sont les plus élevées quand les premiers contacts du mâle sont avec la partie postérieure de la femelle plutôt qu'avec la tête. Les femelles refusent les mâles en s'écartant ou en battant des ailes ou les deux à la fois.Il semble qu'en plus des stimuli cliniques, des stimuli mécaniques fournis par les écailles sont nécessaires pour que les mâles localisent la femelle et s'orientent pour une tentative d'étreinte.

     

A sex-linked locus controls wing polymorphism in males of the pea aphid,Acyrthosiphon pisum (Harris)

Discrete variation in wing morphology is a very common phenomenon in insects and has been used extensively in the past 50 years as a model to study the ecology and evolution of dispersal. Wing morph determination can be purely genetic, purely environmental, or some combination of the two. The precise genetic determinants of genetically based wing morph variation are unknown. Here we explore the genetic basis of wing polymorphism in the pea aphid, which can produce either winged or wingless males. We confirm that three types of pea aphid clones coexist in natural populations, those producing winged males only, those producing wingless males only, and those producing a mixture of both. A Mendelian genetic analysis reveals that male wing polymorphism in pea aphids is determined by a single locus, two alleles system. Using microsatellite loci of known location, we show that this locus is on the X chromosome. The existence of a simple genetic determinism for wing polymorphism in a system in which genetic investigation is possible may help investigations on the physiological and molecular mechanisms of genetically-based wing morph variation. This locus could also be used in the search for genes involved in the wing polyphenism described in parthenogenetic females and to investigate the interplay between polymorphisms and polyphenisms.     

Using multiple traits to estimate the effects of heat shock on the fitness of Aphidius colemani

Extreme temperature events are a great challenge for most ectotherms, particularly for the immature stages of parasitoids, as they do not possess the ability to behaviourally thermoregulate. In this study, we measured the effect of an acute heat shock, combined with desiccation stress (34 °C and 35% r.h. during 10 h) during the mummy stage on several fitness‐related traits of emerging adults of the aphid parasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae: Aphidiinae). Our results showed that the emergence rate was strongly affected by the heat shock (63 ± 2.3 vs. 96.1 ± 0.7% for stress vs. control conditions, respectively), and the resulting population was male biased. Heat stress reduced the lifespan of emerged parasitoids but had no effect on fat reserves and female size. Egg load at emergence and parasitism rate were also reduced by heat treatment. The antennal symmetry was disturbed by the heat treatment, and stressed individuals had reduced mating success compared to control parasitoids. Specifically, time before wing fanning, a typical male courtship behaviour, was significantly longer in parasitoid pairs involving females that had emerged from heat‐treated mummies. Additionally, olfactometry tests on experimental females indicated that their response to host odour was similar to that of control individuals, but they required a longer time for perception. These results highlight that exposure to high temperatures during the mummy stage has cumulative detrimental effects that may strongly impact parasitoid populations under natural conditions and hinder the success of biological control programs.