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Mating ofXenos vesparum (Rossi) (Strepsiptera, Insecta) revisited
Abstract
The controversial mating of the strepsipteran Xenos vesparum was studied to investigate the possible sperm routes for fertilization. The female, which is a neotenic permanent endoparasite of Polistes wasps, extrudes only its anterior region, the "cephalothorax," from the host abdomen. This region has an opening where both mating and larval escape occur. Observations with scanning and transmission electron microscopy revealed spermatozoa not only in the hemocoel, but also in the "ventral canal" (an extragenital duct peculiar to strepsipteran females) and in the "genital ducts" (ectodermal invaginations connecting the ventral canal to the hemocoel) of recently mated females. Xenos vesparum spermatozoa can reach the oocytes either through the hemocoel as a result of a hypodermic insemination, or by moving along the extragenital ducts, which are later used by first instar larvae to escape. The hypothesis of hypodermic insemination is reconsidered in the light of behavioral and ultrastructural evidence.
... There are few detailed studies on the copulation of Stylopidia (i.e. all Strepsiptera with endoparasitic females : Lauterbach, 1954;Beani et al., 2005;Hrabar et al., 2014;Peinert et al., 2016). Lauterbach (1954) examined histological sections of freshly mated females of Stylops ovinae (Stylopidae) and found sperm neither in the brood canal nor in the birth organs. ...
... They observed that the penis is inserted in an invagination of the female cephalothorax and perforates its cuticle (Fig. 1D). As Beani et al. (2005) found no mating scars in the wall of the brood canal, the authors assumed this was evidence of non-traumatic insemination via the birth opening (Fig. 1E). They also suggested that sperm can enter the female body cavity via the brood canal and the birth organs, in addition to traumatic insemination. ...
... In two species with endoparasitic females (Stylopidia, i.e. S. ovinae and X. vesparum), we showed that sperm is transferred directly into the body cavity during the penetration process. This renders an alternative sperm route to the haemocoel of the female, the brood canal and birth organs as discussed by Beani et al. (2005), very unlikely. The widespread documented distribution of traumatic insemination in Strepsiptera suggests strongly that this specific trait belongs to the groundplan of the order. ...
Traumatic insemination refers to mating in which males pierce the female’s integument with his penis for insemination. Strepsiptera are often listed as an example for this mode of copulation. However, while traumatic insemination in Mengenillidae with free-living females is undisputed, its occurrence in Stylopidia with permanent endoparasitic females – 97% of the known species of Strepsiptera – has remained unclear. Rather, observations from a single study on Xenos vesparum (Xenidae) that questioned traumatic insemination in this species became generalized for Stylopidia. Here we show that integration of data from various imaging methods provides convincing evidence for traumatic insemination being phylogenetically widespread in Strepsiptera. Specifically, we provide the first evidence of injury wounds from traumatic insemination in species of Mengenillidae, Corioxenidae, Elenchidae, Halictophagidae and Xenidae. Using three-dimensional models of copulating pairs of Stylops ovinae (Stylopidae) and X. vesparum, we visualize the physical piercing of the female’s integument by the male’s penis. Finally, we show in species of Mengenillidae, Xenidae and Stylopidae that traumatic mating is associated with the injection of sperm in the female’s haemocoel. Our results significantly alter the understanding of the reproductive biology of Strepsiptera and imply that traumatic insemination has been the ancestral mode of copulation and retained in most, if not all, extant families.
... There are few detailed studies on the copulation of Stylopidia (i.e. all Strepsiptera with endoparasitic females : Lauterbach, 1954;Beani et al., 2005;Hrabar et al., 2014;Peinert et al., 2016). Lauterbach (1954) examined histological sections of freshly mated females of Stylops ovinae (Stylopidae) and found sperm neither in the brood canal nor in the birth organs. ...
... They observed that the penis is inserted in an invagination of the female cephalothorax and perforates its cuticle (Fig. 1D). As Beani et al. (2005) found no mating scars in the wall of the brood canal, the authors assumed this was evidence of non-traumatic insemination via the birth opening (Fig. 1E). They also suggested that sperm can enter the female body cavity via the brood canal and the birth organs, in addition to traumatic insemination. ...
... In two species with endoparasitic females (Stylopidia, i.e. S. ovinae and X. vesparum), we showed that sperm is transferred directly into the body cavity during the penetration process. This renders an alternative sperm route to the haemocoel of the female, the brood canal and birth organs as discussed by Beani et al. (2005), very unlikely. The widespread documented distribution of traumatic insemination in Strepsiptera suggests strongly that this specific trait belongs to the groundplan of the order. ...
Traumatic insemination refers to mating in which males pierce the female's integument with his penis for insemination. Strepsiptera are often listed as an example for this mode of copulation. However, while traumatic insemination in Mengenillidae with free-living females is undisputed, its occurrence in Stylopidia with permanent endoparasitic females-97% of the known species of Strepsiptera-has remained unclear. Rather, observations from a single study on Xenos vesparum (Xenidae) that questioned traumatic insemination in this species became generalized for Stylopidia. Here we show that integration of data from various imaging methods provides convincing evidence for traumatic insemination being phylogenetically widespread in Strepsiptera. Specifically, we provide the first evidence of injury wounds from traumatic insemination in species of Mengenillidae, Corioxenidae, Elenchidae, Halictophagidae and Xenidae. Using three-dimensional models of copulating pairs of Stylops ovinae (Stylopidae) and X. vesparum, we visualize the physical piercing of the female's integument by the male's penis. Finally, we show in species of Mengenillidae, Xenidae and Stylopidae that traumatic mating is associated with the injection of sperm in the female's haemocoel. Our results significantly alter the understanding of the reproductive biology of Strepsiptera and imply that traumatic insemination has been the ancestral mode of copulation and retained in most, if not all, extant families.
... Parasitized P. dominula females, the primary host 25,26 , do not develop ovaries, desert the colony early in the season without performing any social task 27 and forage on selected plants, rich of extra-floral nectaries secreting immune-stimulant compounds 28,29 . They form aberrant summer aggregations, where parasite mating occurs 30 , and may overwinter in sheltered sites with future queens 31 . Unlike the completely novel behaviour elicited by other manipulative parasites 32 , parasitized female wasps follow behavioural patterns and life-history trajectories that are still typical of the species, though usually confined to a specific caste: in fact, they all behave like gynes in non-reproductive phase 33,34 . ...
... In line with the extreme sex-dimorphism of X. vesparum (Supplementary Materials, Fig. S1), male and female parasites differentially affect host survival. The twisted-winged adult male emerges from its puparium in the summer, inseminates a female and dies 30 , as does its host a few days after parasite emergence 26,31 . The neotenic endoparasitic female, a "bag" of oocytes and adipocytes, may instead overwinter within the host hemocoel. ...
... Workers harboring a male died in the summer, shortly after the emergence of the parasite (Fig. 1). They had undeveloped ovaries and lower fat scores than workers hosting a Xenos female, probably due to the costly development of a holometabolous insect (i.e. the male parasite), involving two further moults (compared to females) and the production of a puparium 30 . Noticeably, although for a small sample, wasps died later if Xenos males did not extrude from their puparium, suggesting that a hole in the puparium may facilitate microbial infections in the host 26,27 . ...
In social wasps, female lifespan depends on caste and colony tasks: workers usually live a few weeks while queens as long as 1 year. Polistes dominula paper wasps infected by the strepsipteran parasite Xenos vesparum avoid all colony tasks, cluster on vegetation where parasite dispersal and mating occur, hibernate and infect the next generation of wasp larvae. Here, we compared the survival rate of infected and uninfected wasp workers. Workers’ survival was significantly affected by parasite sex: two-third of workers parasitized by a X. vesparum female survived and overwintered like future queens did, while all workers infected by a X. vesparum male died during the summer, like uninfected workers that we used as controls. We measured a set of host and parasite traits possibly associated with the observed lifespan extension. Infected overwintering workers had larger fat bodies than infected workers that died in the summer, but they had similar body size and ovary development. Furthermore, we recorded a positive correlation between parasite and host body sizes. We hypothesize that the manipulation of worker’s longevity operated by X. vesparum enhances parasite’s fitness: if workers infected by a female overwinter, they can spread infective parasite larvae in the spring like parasitized gynes do, thus contributing to parasite transmission.
... Peinert et al. 2016) and where the first instar larvae are released (e.g. Kathirith aMBy 1989; Beani et al. 2005). ...
... The postembryonic development of Stylopidia comprises three larval stages (KathirithaMBy et al. 1984;Beani et al. 2005;Manfredini et al. 2007). The extremely miniaturized and agile first instar larvae enter the host, in the case of X. vesparum larvae of Polistes dominula (Christ, 1791) (Vespidae) (Manfredini et al. 2007). ...
... After protruding the cephalothorax of the secondary larva the female moults to the tertiary larva and the adult. The old exuviae are not shed and adult females of Stylopidia are enclosed by three layers of cuticle, the exuviae of the secondary and tertiary larvae and the adult cuticle (Beani et al. 2005). The exuvia of the secondary larva is often referred to as puparium (e.g. ...
The female cephalothorax of Xenos vesparum (Strepsiptera, Xenidae) is described and documented in detail. The female is enclosed by exuvia of the secondary and tertiary larval stages and forms a functional unit with them. Only the cephalothorax is protruding from the host’s abdomen. The cephalothorax comprises the head and thorax, and the anterior half of the first abdominal segment. Adult females and the exuvia of the secondary larva display mandibles, vestigial antennae, a labral field, and a mouth opening. Vestiges of maxillae are also recognizable on the exuvia but almost completely reduced in the adult female. A birth opening is located between the head and prosternum of the exuvia of the secondary larva. A pair of spiracles is present in the posterolateral region of the cephalothorax. The musculature of the female cephalothorax is strongly reduced. Only muscles of the mandibles, foregut and a pair of longitudinal muscles are present. The nervous system is strongly flattened dorsoventrally. The brain is shifted to the prothoracic region together with the frontal ganglion. Well-developed optic nerves are present and vestiges of stemmata. The suboesophageal ganglion is fused with the thoracic and abdominal ganglia thus forming a compact undivided ganglionic mass. The dorsal vessel forms a ring-shaped structure around the brain. A valvula cardiaca is present between the posterior foregut and midgut. The midgut is strongly bloated and probably involved in inflating the cephalothorax during pheromone release of the female. The Nassonov’s glands are located on the ventral side of the cephalothorax. Structural features of the females of X. vesparum are compared to conditions found in the head and thorax of the free-living females of Mengenillidae and cephalothoracic characters of Stylops ovinae (Stylopidae). The highly modified morphology of female Stylopidia is dicussed with respect to their permanent endoparasitism and also with their neotenous development.
... The floor of the brood canal is lined by a cuticle and by the larval exuviae. It enables the first instar larvae to leave the female through the birth opening, which is also used for insemination 9,10 . ...
... Detailed studies on the copulation of Stylopidia were presented by Lauterbach 25 and recently by Beani et al. 10 and Hrabar et al. 26 . Lauterbach did not find spermatozoa in the brood canal and birth organs on histological sections of recently mated females. ...
... He interpreted them as mating signs and therefore concluded traumatic insemination. Beani et al. 10 , who used scanning and transmission electron microscopy, identified spermatozoa not only in the hemocoel, but also in the brood canal and birth organs of recently mated females of Xenos vesparum. Hrabar et al. 26 , who focussed on the precopulatory and postcopulatory behaviour of females of Xenos peckii, provided a detailed description and high-speed video sequences of the copulation. ...
In a few insect groups, males pierce the female’s integument with their penis during copulation to transfer sperm. This so-called traumatic insemination was previously confirmed for Strepsiptera but only in species with free-living females. The more derived endoparasitic groups (Stylopidia) were suggested to exhibit brood canal mating. Further, it was assumed that females mate once and that pheromone production ceases immediately thereafter. Here we examined Stylops ovinae to provide details of the mating behaviour within Stylopidia. By using μCT imaging of Stylops in copula, we observed traumatic insemination and not, as previously suggested, brood canal mating. The penis is inserted in an invagination of the female cephalothorax and perforates its cuticle. Further we show that female Stylops are polyandrous and that males detect the mating status of the females. Compared to other strepsipterans the copulation is distinctly prolonged. This may reduce the competition between sperm of the first mating male with sperm from others. We describe a novel paragenital organ of Stylops females, the cephalothoracic invagination, which we suggest to reduce the cost of injuries. In contrast to previous interpretations we postulate that the original mode of traumatic insemination was maintained after the transition from free-living to endoparasitic strepsipteran females.
... The presence of pigment scars in the invagination of the brood canal in S. melittae was evidence for Lauterbach (1954) that these scars were caused by traumatic insemination. Studying X. vesparum, Beani et al. (2005) present no conclusive evidence for traumatic insemination. They document insertion of sperm into the brood canal as previously observed (von Siebold, 1839(von Siebold, , 1843 but go on to speculate that the 'aedeagus could perforate the cuticle and the underlying epithelium near the opening . . . ...
... (hypodermic insemination) into the female haemocoel'. Beani et al. (2005) then argue that 'hypodermic insemination' is a possible mode of insemination in X. vesparum, although they could not determine the location where the aedeagus might have been inserted into the female. They proceed to suggest that traumatic insemination is a recent development in Strepsiptera 'to bias paternity'. ...
... In their review of traumatic insemination in terrestrial arthropods, Tatarnic et al. (2014) citing studies by Smith & Hamm (1914), Silvestri (1940), and Beani et al. (2005), conclude (with reference to Strepsiptera): 'It is widely accepted that mating occurs by traumatic insemination whereby a male seeks out a parasitized host insect and, using his needle-like aedeagus, stabs and inseminates the female through the cephalothorax, ejaculating into the haemocoel'. However, their conclusion contradicts the very references they cite in support of the claim: (1) Silvestri (1940) only witnessed traumatic insemination in Mengenillidae, where males seek out free-living rather than endoparasitic females as mates, inseminating them through the abdomen; (2) Smith & Hamm (1914) suggest parthenogenetic egg development, dismissing traumatic insemination as a means of reproduction in the Stylopidae; (3) Silvestri (1940Silvestri ( , 1941a refers to fertilization as 'extra-vulvar', which differs from traumatic insemination; and (4) Beani et al. (2005) did not find conclusive evidence for traumatic insemination, stating that it is not known whether mating in strepsipterans occurs via hypodermic injection directly into the hemocoel, or through the brood canal opening, or via both routes. ...
The cryptic entomophagous parasitoids in the order Strepsiptera exhibit specific adaptations to each of the 34 families that they parasitize, offering rich opportunities for the study of male–female conflict. We address the compelling question as to how the diversity of Strepsiptera (where cryptic speciation is common) arose. Studying 13 strepsipteran families, including fossil taxa, we explore the genitalic structures of males, the free-living females of the Mengenillidia (suborder), and the endoparasitic females of the Stylopidia (suborder). Inferring from similarity between aedeagi of males either between congeners, heterogeners, or between species within the same taxonomic family, the same of which is true of the cephalothoraces of females, we predict that male–female conflict and a co-evolutionary morphological arms race between sexes is not likely to exist in most species of Strepsiptera. We then review the non-genitalic structures that play a role during sexual communication, and present details of copulatory behaviour. We conclude that Strepsiptera fall within the synchronous sensory exploitation model where short-lived males take advantage of a pre-existing sensory system involving pheromone signals emitted by females.
... On a host nest (Fig. 1A) the viviparous larvae ( Fig. 1B) crawl out of their mother's brood canal (also termed ventral canal) through which she was inseminated the previous season (Beani et al. 2005), and quickly seek new host larvae into which they burrow. Once inside their host, the first instar larvae moult into a grub-like immotile form. ...
... Males, like females, also extrude their head and prothorax; their development differs in that they undergo an additional moult and pupation after they have extruded (Beani et al. 2005). The sclerotised portion comprising the shell of the previous larval instars serves as a puparium (Kinzelbach 1971;Kathirithamby 2005). ...
... Whether this is a widespread phenomenon in Strepsiptera is yet to be investigated but some information already implies that it may occur in species other than X. peckii. Studying mating of female Xenos vesparum (Rossi) in Polistes dominula (Christ) host wasps, Beani et al. (2005) noted the ''cephalothorax fully extruded from the tergite'', and Waloff (1981) and Hans Henderickx (University of Antwerp, Antwerp, Belgium) (personal communication) noted that a female Halictophagus silwoodensis (Waloff) ''heaved'' her cephalothorax towards the male during his attempts to inseminate her. Video recordings of the emergence process revealed that males use their mandibles to cut open the puparium, nearly severing the entire cephalotheca ( Fig. 2C; Supplementary Video 2). ...
We studied life history traits of Xenos peckii Kirby (Strepsiptera: Xenidae), a little-known parasite of the paper wasp Polistes fuscatus (Fabricus) (Hymenoptera: Vespidae) in North America. We field-collected 24 wasp nests in early July 2012, isolated parasitised wasps, tracked life history events of X. peckii, and recorded such behaviour as emergence of males and mating by normal-speed and high-speed cinematography. To emerge, males first cut the puparium with their mandibles along an ecdysial suture line, and then push aside the pupal cap during emergence. The endoparasitic females engage in active calling (pheromone release) behaviour by slowly inflating their cephalothorax, and then extruding it even farther out of, and tilting it away from, the host wasp abdomen. Seasonal and diel (afternoon) emergence periods of males coincide with seasonal and diel receptivity and calling periods of females. Males approach calling females in a swaying flight with smooth turns. They typically land on the anterior portion of the host wasp's abdomen, and then step backward until they make contact with the cephalothorax of the female. As soon as their mesothoracic legs contact the female's cephalothorax, they curl around it, and the male initiates mating. Thereafter, the female fully retreats and never re-mates.
... host-seeking first-instar larvae) into the immature stages of the wasp (Hughes et al. 2003;Beani and Massolo, 2007;Manfredini et al. 2007Manfredini et al. , 2010a. At the conclusion of endoparasitic larval development, female and male X. vesparum differ remarkably: neotenic females are permanently associated with the host while males pupate within the host and then emerge from their puparia as winged insects, leaving the host's body in search of a receptive female (Beani et al. 2005). Different aspects of this peculiar parasite-host association have been studied over the years, spanning from the parasite strategies to overcome the immune defences of its host to the dramatic physiological and behavioural changes driven by the parasite in the female host to favour its own transmission (Strambi and Strambi, 1973;Hughes et al. 2004a;Beani, 2006;Manfredini et al. 2010bManfredini et al. , c, 2013Beani et al. 2011). ...
... future queens), both healthy and parasitized by X. vesparum. Parasitized females leave their colonies before the emergence of the parasite and cluster in aberrant summer aggregations, usually at leks, where they stay inactive while the free-living winged X. vesparum males break their pupal cap and abandon their hosts to fertilize the permanently endoparasitic female (Hughes et al. 2004a;Beani et al. 2005). In a previous study we have shown that males are able to distinguish females of different putative caste, preferring gynes over workers; conversely, they are unable to recognize the presence of X. vesparum parasites in female partners and try to mate with them (Cappa et al. 2013). ...
... Parasitized females are transformed by the parasite into idle, gregarious 'zombies'. They leave their colonies before the emergence of the parasite without performing any social task on the nest, and cluster in aberrant summer aggregations where the mating of the parasite occurs (Hughes et al. 2004a;Beani et al. 2005). Similarly to parasitized females, infected male wasps also gather at leks, but, unlike females, they do not form nor join the aberrant aggregations of parasitized wasps; instead, they try to defend territories and sexually interact with females as healthy males do (L. ...
SUMMARY Host castration represents a mechanism used by parasites to exploit energy resources from their hosts by interfering with their reproductive development or to extend host lifespan by removing risks associated with reproductive activity. One of the most intriguing groups of parasitic castrators is represented by the insects belonging to the order Strepsiptera. The macroparasite Xenos vesparum can produce dramatic phenotypic alterations in its host, the paper wasp Polistes dominula. Parasitized female wasps have undeveloped ovaries and desert the colony without performing any social task. However, very little attention has been given to the parasitic impact of X. vesparum on the male phenotype. Here, we investigated the effects of this parasite on the sexual behaviour and the morpho-physiology of P. dominula males. We found that, differently from female wasps, parasitized males are not heavily affected by Xenos: they maintain their sexual behaviour and ability to discriminate between female castes. Furthermore, the structure of their reproductive apparatus is not compromised by the parasite. We think that our results, demonstrating that the definition of X. vesparum as a parasitoid does not apply to infected males of P. dominula, provide a new perspective to discuss and maybe reconsider the traditional view of strepsipteran parasites.
... With few exceptions females spend their entire life within their host and at sexual maturity extrude the apex of their cephalothorax (formed by fusion of the head and thorax) through an intersegmental membrane of the host's body wall. This exposes the female's integument, which the male pierces during mating, as well as the brood canal, a transverse fissure in the cephalothorax through which the female bears live young (7). ...
... Despite being the focus of study for over a century (e.g., 40,56,60,89), strepsipteran reproductive biology remains poorly understood (7). It is widely accepted that mating occurs by TI, whereby a male seeks out a parasitized host insect and, using his needle-like aedeagus, stabs and inseminates the female through the cephalothorax, ejaculating into the hemocoel (7,88,93). ...
... Despite being the focus of study for over a century (e.g., 40,56,60,89), strepsipteran reproductive biology remains poorly understood (7). It is widely accepted that mating occurs by TI, whereby a male seeks out a parasitized host insect and, using his needle-like aedeagus, stabs and inseminates the female through the cephalothorax, ejaculating into the hemocoel (7,88,93). In adult females the oocytes are free-floating within the hemocoel, where fertilization takes place (11,46). ...
Traumatic insemination is a bizarre form of mating practiced by some invertebrates in which males use hypodermic genitalia to penetrate their partner's body wall during copulation, frequently bypassing the female genital tract and ejaculating into their blood system. The requirements for traumatic insemination to evolve are stringent, yet surprisingly it has arisen multiple times within invertebrates. In terrestrial arthropods traumatic insemination is most prevalent in the true bug infraorder Cimicomorpha, where it has evolved independently at least three times. Traumatic insemination is the sole form of mating in the Strepsiptera and has recently been recorded in fruit fly and spider lineages. We review the putative selective pressures that may have led to the evolution of traumatic insemination across these lineages, as well as pressures that continue to drive divergence in male and female reproductive morphology and behavior. Traumatic insemination mechanisms and attributes are compared across independent lineages. Expected final online publication date for the Annual Review of Entomology Volume 59 is January 07, 2014. Please see http://www.annualreviews.org/catalog/pubdates.aspx for revised estimates.
... In addition, permanently endoparasite viviparous females develop " novel structures " (Kathirithamby 2000). Recent studies described a peculiar " masquerading " strategy for avoiding host immune response (Kathirithamby et al. 2003), a bizarre genome, to date the smallest one among insects (Johnston et al 2004), peculiar arrangements in mtDNA (Carapelli et al. 2006), unusual extra-genital mating modalities (Beani et al 2005), and the list goes on. Moreover, the phylogenetic relationships of this order is still controversial (the so-called " Strepsiptera problem " , Whiting et al. 1997), regardless of the use of molecular and morphological data (Whiting 1998, Huelsenbeck 2001, for reviews), the comparative analysis at the level of sperm ultrastructure (Carcupino et al. 1995, Dallai et al. 2003) and larvae (Pohl 2002), or the use of fossil strepsipterans in amber (Pohl et al. 2005, Grimaldi et al. 2005). ...
... Note that, after the moult of the 1st instar larva, apolysis is not followed by ecdysis, thus successive instars retain the exuvia of the previous stages. (From Beani et al. 2005). ...
... — b: At higher magnification, it is possible to observe the tarsal pad of the anterior legs. (From Beani et al. 2005). ...
The infection of Polistes dominulus wasps by the strepsipteran Xenos vesparum provides a suitable case study for exploring parasitic manipulation. One aim of this review is to summarize the life cycle of X. vesparum: from infection of immature wasps to the "stylopization" of adults, and from its mating at summer aberrant aggregations of infected wasps to the overwintering of fertilized Xenos inside the abdomen of hibernating wasps. The second aim of this review it to highlight how this parasite manipulates the flexible phenotype of the wasp to maximize its own reproductive success.
... There are hints of similar diversity in some other groups with traumatic insemination, such as anthocorid bugs and Strepsiptera (e.g. female cells that engulf sperm in strepsipterans – Beani et al., 2005). Special attention to discriminating female modifications that are appropriate to deal with sperm (a possible result of sexual selection by cryptic female choice) from those designed to deal with the physical damage and infections that can result from traumatic insemination (an expected result of sexually antagonistic coevolution) could help distinguish between the two hypotheses. ...
... However , the offspring also emerge here (Hughes-Schrader, 1924), so the opening could have evolved in the context of birth rather than mating. Males of Xenos vesparum sometimes deposit sperm through this opening into the brood canal (Beani et al., 2005). The inner end of each of the several internal branches of the brood canal lead to the haemocoel and is covered by a delicate epithelium that is only one cell thick (Hughes-Schrader, 1924); individual sperm cells presumably pass through this covering. ...
... In other cases, the male's aedeagus perforates the wall of the brood canal near the external opening, and introduces his sperm directly into the haemocoel (Lauterbach, 1954). Males generally die within a few minutes after copulating (Kithirithamby, 1989, Beani et al., 2005). In two species (Coriophagus rieki and Stichotremia dallotorreanum ), the male's aedeagus sometimes remains in the female after copulation (Kithirithamby, 1989). ...
Morphological traits involved in male-female sexual interactions, such as male genitalia, often show rapid divergent evolution. This widespread evolutionary pattern could result from sustained sexually antagonistic coevolution, or from other types of selection such as female choice or selection for species isolation. I reviewed the extensive but under-utilized taxonomic literature on a selected subset of insects, in which male-female conflict has apparently resulted in antagonistic coevolution in males and females. I checked the sexual morphology of groups comprising 500-1000 species in six orders for three evolutionary trends predicted by the sexually antagonistic coevolution hypothesis: males with species-specific differences and elaborate morphology in structures that grasp or perforate females in sexual contexts; corresponding female structures with apparently coevolved species-specific morphology; and potentially defensive designs of female morphology. The expectation was that the predictions were especially likely to be fulfilled in these groups. A largely qualitative overview revealed several surprising patterns: sexually antagonistic coevolution is associated with frequent, relatively weak species-specific differences in males, but male designs are usually relatively simple and conservative (in contrast to the diverse and elaborate designs common in male structures specialized to contact and hold females in other species, and also in weapons such as horns and pincers used in intra-specific battles); coevolutionary divergence of females is not common; and defensive female divergence is very uncommon. No cases were found of female defensive devices that can be facultatively deployed. Coevolutionary morphological races may have occurred between males and females of some bugs with traumatic insemination, but apparently as a result of female attempts to control fertilization, rather than to reduce the physical damage and infections resulting from insertion of the male's hypodermic genitalia. In sum, the sexually antagonistic coevolution that probably occurs in these groups has generally not resulted in rapid, sustained evolutionary divergence in male and female external sexual morphology. Several limitations of this study, and directions for further analyses are discussed.
... At sexual maturity it extrudes from the wasp abdomen with only its anterior region, the ''cephalothorax''. A ventral canal opens with a transversal fissure in the cephalothorax and connects the hemocoel to the exterior; through this opening, both insemination and release of triungulins occur (Hughes-Schrader, 1924;Beani et al., 2005). The adult male is a winged short-living organism (<5 h) that, after having spent all its pre-imaginal instars as an endoparasite, emerges from its puparium just to inseminate a female (Kathirithamby, 1989;Beutel and Pohl, 2006). ...
... Two days after the 1st instar larva has penetrated into the host, it molts to the 2nd instar: an apodous unpigmented larva that is well visible through the host's cuticle due to two black spots corresponding to the eyes (Beani et al., 2005). At this stage the sexes are not yet distinguishable. ...
... At the late 4th instar, the cephalothorax protrudes through the intersegmental membranes between the last tergites of the wasp. Soon after extrusion, the neotenic female may be inseminated (Beani et al., 2005). A semithin section of a ''young'' fertilized female shows that the hemocoel is filled with embryos at different developmental stages, intermingled with adipocytes (Fig. 8A). ...
Females of the endoparasite Xenos vesparum (Strepsiptera, Stylopidae) may survive for months inside the host Polistes dominulus (Hymenoptera, Vespidae). The midgut structure and function in larval instars and neotenic females has been studied by light and electron microscope and by stable carbon isotopic technique. The 1st instar larva utilizes the yolk material contained in the gut lumen, whereas the subsequent larval instars are actively involved in nutrient uptake from the wasp hemolymph and storage in the adipocytes. At the end of the 4th instar, the neotenic female extrudes with its anterior region from the host; the midgut progressively degenerates following an autophagic cell death program. First the midgut epithelial cells accumulate lamellar bodies and then expel their nuclei into the gut lumen; the remnant gut consists of a thin epithelium devoid of nuclei but still provided with intercellular junctions. We fed the parasitized wasps with sugar from different sources (beet or cane), characterized by their distinctive carbon isotope compositions, and measured the bulk (13)C/(12)C ratios of both wasps and parasites. Female parasites developing inside the wasp hemocoel are able to absorb nutrients from the host but, after their extrusion, they stop incorporating nutrients and survive thanks to the adipocytes content.
... Adult males always leave the host and have an excellent flying capacity. In their very short life span of only few hours they must find a female and mate (Pix et al. 1993;Beani et al. 2005;Straka et al. 2011). Adult females are wingless, neotenic, and either free living (Mengenillidae and probably Bahiaxenidae) or permanently endoparasitic (remaining Strepsiptera: Stylopidia) (Pohl et al. 2018). ...
... In the case of Xenos, Kathirithamby et al. (2015) hypothesized that the brood canal membrane is ruptured during the super-extrusion of the cephalothorax, thereby facilitating the release of pheromones during mate signaling. However, a perforation by the male penis during copulation is also possible (Beani et al. 2005). ...
The generic taxonomy and host specialization of Xenidae have been understood differently by previous authors. Although the recent generic classification has implied a specialization on the level of host families or subfamilies, the hypothesis that each xenid genus is specialized to a single host genus was also previously postulated. A critical evaluation of the classification of the genera of Xenidae is provided here based on morphology in accordance with results of recent molecular phylogenetic studies. External features of the female cephalothoraces and male cephalothecae were documented in detail with different techniques. Diagnoses and descriptions are presented for all 13 delimited genera. The earliest diverging genera are usually well characterized by unique features, whereas deeply nested genera are usually characterized by combinations of characters. Three new genera are described: Sphecixenos gen. nov., Tuberoxenos gen. nov., and Deltoxenos gen. nov. Five previously described genera are removed from synonymy: Tachytixenos Pierce, 1911, stat. res.; Brasixenos Kogan & Oliveira, 1966, stat. res.; Leionotoxenos Pierce, 1909, stat. res.; Eupathocera Pierce, 1908, stat. res.; and Macroxenos Schultze, 1925, stat. res. One former subgenus is elevated to generic rank: Nipponoxenos Kifune & Maeta, 1975, stat. res. Monobiaphila Pierce, 1909, syn. nov. and Montezumiaphila Brèthes, 1923, syn. nov. are recognized as junior synonyms of
... Dramatic alterations are also induced by the parasite on the behaviour of female wasps: if infected, they are turned into gregarious 'zombies' regardless of their putative rank, i.e. workers or gynes (Beani, 2006;Beani et al., 2011;Cappa et al., 2014;Geffre et al., 2017). They leave their colonies few days after emergence without performing any social task, select peculiar sites where they search for shelter and nutrients to survive outside the nest, cluster to favour the parasite mating (Hughes et al., 2004;Beani et al., 2005) and overwinter in aggregations with future queens (Beani et al., 2011). Conversely, males parasitized by one Xenos male or female maintain their sexual behaviour during lab trials (Cappa et al., 2013 and in the field, where they typically gather at leks and defend their territory. ...
... In this perspective, Polistes males represent a secondary host for Xenos (Hughes et al., 2004). They might act as a vector for the parasite when they fly at leks to mate (Beani et al., 2005;Cappa et al., 2014), enabling the parasite to easily find a mate nearby. However they are a dead end for the Xenos female, as they die in the autumn and by doing so they interrupt the life cycle of the female parasite: winter aggregations do not include males (Beani et al., 2011). ...
Parasitic castration is an adaptive strategy where parasites usurp the hosts’ reproductive physiology to complete their life cycle. The alterations in the host traits vary in their magnitude, from subtle changes in the host morpho-physiology and behaviour to the production of complex aberrant phenotypes, which often depend on the host gender. The strepsipteran macroparasite Xenos vesparum induces dramatic behavioural and physiological changes in its female host, the paper wasp Polistes dominula, while its effect on the male phenotype is largely unknown.
... Then, X. vesparum extrudes its anterior region between the host's abdominal segments. The male parasitoid emerges as a fully motile, winged adult that will disperse to mate [21,33,38], whereas the female remains neotenic, living permanently endoparasitic, with an extruded cephalothorax with no eyes or appendages [20,21,39]. ...
... Early emerging stylopized females desert their natal colonies in mid-summer, during peak colony activity, and form extranidal aggregations with stylopized females from other colonies [19,41]. This aberrant host behaviour occurs close to the time of male parasitoid emergence and appears to help facilitate mate location by the parasitoids [38]. Later, stylopized females are joined by unstylopized aggregating gynes, forming overwintering clusters. ...
Parasites can manipulate host behaviour to increase their own transmission and fitness, but the genomic mechanisms by which parasites manipulate hosts are not well understood. We investigated the relationship between the social paper wasp, Polistes dominula, and its parasite, Xenos vesparum (Insecta: Strepsiptera), to understand the effects of an obligate endoparasitoid on its host's brain transcriptome. Previous research suggests that X. vesparum shifts aspects of host social caste-related behaviour and physiology in ways that benefit the parasitoid. We hypothesized that X. vesparum-infested (stylopized) females would show a shift in caste-related brain gene expression. Specifically, we predicted that stylopized females, who would normally be workers, would show gene expression patterns resembling pre-overwintering queens (gynes), reflecting gyne-like changes in behaviour. We used RNA-sequencing data to characterize patterns of brain gene expression in stylopized females and compared these with those of unstylopized workers and gynes. In support of our hypothesis, we found that stylopized females, despite sharing numerous physiological and life-history characteristics with members of the worker caste, show gyne-shifted brain expression patterns. These data suggest that the parasitoid affects its host by exploiting phenotypic plasticity related to social caste, thus shifting naturally occurring social behaviour in a way that is beneficial to the parasitoid.
... They are described as paedomorphic, partially paedomorphic (Kin zelBach 1971), or more recently as neotenic (e.g. KathirithamBy 1989;KathirithamBy et al. 2015;Beani et al. 2005;erezyilmaz et al. 2014). KinzelBach (1971: 132) used the term paedomorphism (Pädomorphose) or paedomorphic (pädomorph) in the sense that an adult stage develops but retains larval features to a considerable degree. ...
... He mainly referred to lauterBach (1954), who demonstrated that the female of Stylops is enclosed by three layers of cuticle, interpreted as larval, pupal and adult cuticle. Using transmission electron microscopy Beani et al. (2005) also found three cuticular layers enclosing the female of Xenos vesparum Rossius, 1793 (Xenidae). They interpreted the female as the fourth neotenic instar and the cuticular layers as second, third and fourth instar cuticle. ...
External and internal features of the female cephalothorax of the strepsipteran species Stylops ovinae (Stylopidae) are described in detail. Many derived features are closely related with the obligatory endoparasitism. A conspicuous characteristic is the secondary tagmosis with an anterior cephalothorax and a large, sack-shaped posterior body region. The cephalothorax comprises the head, thorax and anterior half of abdominal segment I and protrudes from the host’s abdomen. It contains the mouth and birth opening, vestiges of cephalic appendages, and most internal organs including the large Nassonov’s glands. The posterior body part contains mainly the reproductive organs. The constriction of abdominal segment I probably prevents the exposed anterior body from slipping back into host’s body cavity. The narrow mouth opening is used for the uptake of the host’s hemolymph by the secondary larval stage and is maintained as a non-functional structure by the adult females. The tentorium is absent. The mandibles are immobilized in the adult female. They are used for penetrating the host’s body wall by the second larval instar. The brood canal formed by the larval and pupal exuvia is an autapomorphy of Stylopidia, the birth opening where the first instars are released from the female an autapomorphy of Stylopiformia, and the cephalothoracic invagination an autapomorphy of Stylops. A single pair of functional spiracles is laterally placed on abdominal segment I. An unusual circular hemolymph vessel is present in the pharyngeal region. The brain is shifted to the thorax. The suboesophageal complex and the thoracic and abdominal ganglia form a single ganglionic mass in the thoracic region. The musculature of the cephalothorax is extremely reduced. Nassonov’s glands, which produce sex pheromones, are the largest internal structures in the cephalothorax. Despite of the loss of the digestive function, the digestive tract is not degenerated including a foregut with well-developed muscles.
... Strepsiptera have been divided in two major groups, Mengenillidia and Stylopidia. Both are obligate entomophagous parasitoids during most of the larval stages and exhibit a variety of unusual phenotypic features [18][19][20][21][22][23][24][25]. Stylopidia exhibit extreme sexual dimorphism: the males remain endoparasitic in their hosts to pupate, emerging as freeliving adults, but the females remain endoparasitic as neotenic adults and have no distinct head, thorax or body appendages [18][19][20]22,25]. ...
... In contrast, in Mengenillidia both sexes leave their hosts before pupation and are free-living as adults, and the females possess all the body appendages typical of an insect, except wings ( Fig. 1a,b). Mengenillidia and Stylopidia also differ in their reproductive practices: in Mengenillidia the free-living females are fertilized by traumatic insemination, whereas females of Stylopidia are inseminated through the brood canal opening [18][19][20][21][22][23]25,26]. ...
Insect phylogeny has recently been the focus of renewed interest as advances in sequencing techniques make it possible to rapidly generate large amounts of genomic or transcriptomic data for a species of interest. However, large numbers of markers are not sufficient to guarantee accurate phylogenetic reconstruction, and the choice of the model of sequence evolution as well as adequate taxonomic sampling are as important for phylogenomic studies as they are for single-gene phylogenies. Recently, the sequence of the genome of a strepsipteran has been published and used to place Strepsiptera as sister group to Coleoptera. However, this conclusion relied on a data set that did not include representatives of Neuropterida or of coleopteran lineages formerly proposed to be related to Strepsiptera. Furthermore, it did not use models that are robust against the long branch attraction artifact. Here we have sequenced the transcriptomes of seven key species to complete a data set comprising 36 species to study the higher level phylogeny of insects, with a particular focus on Neuropteroidea (Coleoptera, Strepsiptera, Neuropterida), especially on coleopteran taxa considered as potential close relatives of Strepsiptera. Using models robust against the long branch attraction artifact we find a highly resolved phylogeny that confirms the position of Strepsiptera as a sister group to Coleoptera, rather than as an internal clade of Coleoptera, and sheds new light onto the phylogeny of Neuropteroidea.
... With the exception of the subfamily Mengenillidae, the neotenic females never leave their hosts (KATHIRITHAMBY 1989). Winged males fly away from their host only after the completion of their development, and subsequently inseminate females through an opening in her cephalothorax extending from the host's body (BEANI et al. 2005). The free adult males are notorious for their extremely short life span (often less than 5 hr; HUGHES et al. 2004). ...
... Infected individuals aggregate on vegetation and landmarks which are traditional nuptial arenas and on buildings which represent pre-hibernation sites (HUGHES et al. 2004; BEANI 2006). It appears that this manipulation enables male Xenos to more reliably find conspecific females (BEANI et al. 2005). The synchronised emergence of parasitised hosts in early spring could ensure the meeting of sexual partners in Stylops as well, even in the case of a low population density of their hosts. ...
Stylopised (= parasitised by Strepsiptera Stylopidae) imagoes of Andrena (Hymenoptera Andrenidae) bees are known to exhibit intersexual morphology. Until now, their abnormal morphology has been thought to result from undernourishment of parasitised larvae during development. This hypothesis, however, dos not fit to mass provisioning Hymenoptera. We hypothesised that induced changes in the suite of morphological characters might be a consequence of manipulation of sex-specific behavioural traits by a strepsipteran parasite. Thus, the masculinised morphology of stylopised females might be connected with shifts in their sexual behaviour. Here, we tested the effect of Stylops (Strepsiptera Stylopidae) infection on the timing of spring nest emergence in Andrena bees, where males generally emerged conspicuously ear-lier than conspecific females. We used two independent data samplings – pan trapping and direct observation – to avoid possible bias caused by one of the methods. In accordance with our hypothesis, we documented that the time of emergence/activity in stylopised females follows the temporal trend of uninfected, protandrous males. We ascribe this observation to host manipulation and briefly discuss the potential adaptive value of the altered host behaviour for the parasite. We discuss our results across three species: Andrena strohmella, A. minutula and A. vaga.
... Mating behaviour and morphology is highly derived in Strepsiptera and appears to provide little to the analysis of genital asymmetry. Copulation involves extragenital insemination (Kirkpatrick, 1937;Silvestri, 1941aSilvestri, , b, 1943Lauterbach, 1954;Kinzelbach, 1971a, b;Kathirithamby, 1989Kathirithamby, , 2000Beani et al., 2005) and this has presumably resulted in the simplification of the male copulatory organ and in the reduction or loss of the female primary copulatory organ (Kinzelbach, 1971a). During copulation, males use their sclerotized aedeagus to penetrate the female, either in an unspecified location of her body (in the 'basal' Mengenillidae, Silvestri, 1940b; however, this view may be mistaken: J. Cook, personal communication, March 2006), or in a secondary copulatory organ at the ventral side of the cephalothorax (in Stylopidia; Silvestri, 1940a). ...
... No asymmetry is known in either the male or female reproductive structures, and it is unknown if males in Stylopidia have to orient themselves properly relative to the female. Actually, both males and females in Stylopidia are quite consistently oriented toward each other (male facing forward on the host, female facing backward with her ventral side towards the host's tergites; Lindberg, 1939;Silvestri, 1941b;Kinzelbach, 1971b;Beani et al., 2005; but see Baumert, 1959), but this might result from orientation of both relative to the host. ...
Asymmetries are a pervading phenomenon in otherwise bilaterally symmetric organisms and recent studies have highlighted their potential impact on our understanding of fundamental evolutionary processes like the evolution of development and the selection for morphological novelties caused by behavioural changes. One character system that is particularly promising in this respect is animal genitalia because (1) asymmetries in genitalia have evolved many times convergently, and (2) the taxonomic literature provides a tremendous amount of comparative data on these organs. This review is an attempt to focus attention on this promising but neglected topic by summarizing what we know about insect genital asymmetries, and by contrasting this with the situation in spiders, a group in which genital asymmetries are rare.
In spiders, only four independent origins of genital asymmetry are known, two in Theridiidae (Tidarren/Echinotheridion, Asygyna) and two in Pholcidae (Metagonia, Kaliana). In insects, on the other hand, genital asymmetry is a widespread and common phenomenon. In some insect orders or superorders, genital asymmetry is in the groundplan (e.g. Dictyoptera, Embiidina, Phasmatodea), in others it has evolved multiple times convergently (e.g. Coleoptera, Diptera, Heteroptera, Lepidoptera). Surprisingly, the huge but widely scattered information has not been reviewed for over 70 years. We combine data from studies on taxonomy, mating behaviour, genital mechanics, and phylogeny, to explain why genital asymmetry is so common in insects but so rare in spiders.
We identify further fundamental differences between spider and insect genital asymmetries: (1) in most spiders, the direction of asymmetry is random, in most insects it is fixed; (2) in most spiders, asymmetry evolved first (or only) in the female while in insects genital asymmetry is overwhelmingly limited to the male. We thus propose that sexual selection has played a crucial role in the evolution of insect genital asymmetry, via a route that is accessible to insects but not to spiders. The centerpiece in this insect route to asymmetry is changes in mating position. Available evidence strongly suggests that the plesiomorphic neopteran mating position is a female-above position. Changes to male-dominated positions have occurred frequently, and some of the resulting positions require abdominal twisting, flexing, and asymmetric contact between male and female genitalia. Insects with their median unpaired sperm transfer organ may adopt a one-sided asymmetric position and still transfer the whole amount of sperm. Spiders with their paired sperm transfer organs can only mate in symmetrical or alternating two-sided positions without foregoing transfer of half of their sperm.
We propose several hypotheses regarding the evolution of genital asymmetry. One explains morphological asymmetry as a mechanical compensation for evolutionary and behavioural changes of mating position. The morphological asymmetry per se is not advantageous, but rather the newly adopted mating position is. The second hypothesis predicts a split of functions between right and left sides. In contrast to the previous hypothesis, morphological asymmetry per se is advantageous. A third hypothesis evokes internal space constraints that favour asymmetric placement and morphology of internal organs and may secondarily affect the genitalia. Further hypotheses appear supported by a few exceptional cases only.
... The species Xenos vesparum Rossi, 1793 (Insecta: Strepsiptera: Xenidae), is a noteworthy organism representing an endoparasite of the European paper wasp -Polistes dominula (Christ, 1791) (Insecta: Hymenoptera). The species displays a peculiar lifecycle and demonstrates extensive sexual dimorphism (e.g., Beani et al. 2005;Cappa et al. 2014;Richter et al. 2017). Both sexes develop in their host. ...
The Strepsiptera species Xenos vesparum Rossi, 1793, is an endoparasite of wasps (genus Polistes) characterized by a specific lifecycle and significant sexual dimorphism. A total of 12 host specimens (Polistes dominula (Christ, 1791)) were caught using a beer trap-site Diviacka Nová Ves, period 25 July 2022-5 August 2022. The prevalence of X. vesparum were 83%. Overall, 33 parasites were present in 10 wasps (min. 1, max. 10, average 3.3). The highest number of parasites (13 specimens) was observed below terga T3 and T4. It appears that the parasite X. vesparum most commonly infects P. dominula on the dorsal side of the body under terga T3 and T4. In addition, beer traps seem to be a suitable mean of detecting and calculating the prevalence of this parasite.
... 2B, 3B). However, Beani et al. (2005) discussed an alternative sperm route in X. vesparum, namely by release of sperm into the brood canal: the sperm could then reach the hemocoel of the female via the birth organs. Previous studies have shown that the cuticle of the paragenital organ of S. ovinae and the cuticle of the anterior brood canal of X. vesparum is about three times thicker than the cuticle in spatial proximity (Löwe, Beutel & Pohl, 2016;Peinert et al., 2016;Richter et al., 2017). ...
Traumatic insemination describes an unusual form of mating during which a male penetrates the body wall of its female partner to inject sperm. Females unable to prevent traumatic insemination have been predicted to develop either traits of tolerance or of resistance, both reducing the fitness costs associated with the male-inflicted injury. The evolution of tolerance traits has previously been suggested for the bed bug. Here we present data suggesting that tolerance traits also evolved in females of the twisted-wing parasite species Stylops ovinae and Xenos vesparum. Using micro-indentation experiments and confocal laser scanning microscopy, we found that females of both investigated species possess a uniform resilin-rich integument that is notably thicker at penetration sites than at control sites. As the thickened cuticle does not seem to hamper penetration by males, we hypothesise that thickening of the cuticle resulted in reduced penetration damage and loss of haemolymph and in improved wound sealing. To evaluate the evolutionary relevance of the Stylops-specific paragenital organ and penis shape variation in the context of inter-and intraspecific competition, we conducted attraction and interspecific mating experiments, as well as a geometric-morphometric analysis of S. ovinae and X. vesparum penises. We found that S. ovinae females indeed attract sympatrically distributed congeneric males. However, only conspecific males were able to mate. In contrast, we did not observe any heterospecific male attraction by Xenos females. We therefore hypothesise that the paragenital organ in the genus Stylops represents a prezygotic mating barrier that prevents heterospecific matings.
... One example of a complex manipulation is the interaction between the endoparasitic insect Xenos vesparum (Rossi)(Strepsiptera, Xenidae) [13,14] and its host, the primitively eusocial wasp Polistes dominula (Christ)(Hymenoptera, Vespidae). If parasitized, putative workers are castrated, do not participate in colony tasks, and desert the nest to form aggregations on nearby plants, where X. vesparum completes its life cycle by mating and releasing infective larvae [15][16][17][18]. The behavior of parasitized wasps has some features that remind the non-reproductive phase of future queens: they are in ovary diapause, do not perform any colony task and overwinter in sheltered aggregations [19]. ...
Paper wasps ( Polistes dominula ), parasitized by the strepsipteran Xenos vesparum , are castrated and desert the colony to gather on plants where the parasite mates and releases primary larvae, thus completing its lifecycle. One of these plants is the trumpet creeper Campsis radicans : in a previous study the majority of all wasps collected from this plant were parasitized and focused their foraging activity on C . radicans buds. The unexpected prevalence and unusual feeding strategy prompted us to investigate the influence of this plant on wasp behavior and physiology through a multidisciplinary approach. First, in a series of laboratory bioassays, we observed that parasitized wasps spent more time than non-parasitized ones on fresh C . radicans buds, rich of extra-floral nectaries (EFNs), while the same wasps ignored treated buds that lacked nectar drops. Then, we described the structure and ultra-structure of EFNs secreting cells, compatible with the synthesis of phenolic compounds. Subsequently, we analysed extracts from different bud tissues by HPLC-DAD-MS and found that verbascoside was the most abundant bioactive molecule in those tissues rich in EFNs. Finally, we tested the immune-stimulant properties of verbascoside, as the biochemical nature of this compound indicates it might function as an antibacterial and antioxidant. We measured bacterial clearance in wasps, as a proxy for overall immune competence, and observed that it was enhanced after administration of verbascoside—even more so if the wasp was parasitized. We hypothesize that the parasite manipulates wasp behavior to preferentially feed on C . radicans EFNs, since the bioactive properties of verbascoside likely increase host survival and thus the parasite own fitness.
... The abdomen of a parasitized P. dominula wasp shows a typical irregular shape, due to the extrusion of the parasite between abdominal segments (see Fig 1). In summer, the winged male parasite emerges from his puparium, that protrudes from the host's abdomen, and wanders in search of a receptive female to inseminate, dying shortly after mating [20]. The neotenic female parasite instead is permanently confined within the hemocoel of her host and may overwinter inside the hosts. ...
The parasitic insect Xenos vesparum induces noticeable behavioral and physiological changes—e.g. castration—in its female host, the paper wasp Polistes dominula: parasitized putative workers avoid any colony task and desert the colony to survive in the nearby vegetation, like future queens and males do. In this long-term observational study, we describe the spectacular attraction of parasitized workers towards trumpet creeper bushes (Campsis radicans) in early-summer. Two thirds of all wasps that we sampled on these bushes were parasitized, whereas the parasite prevalence was much lower in our study area and most wasps sampled on other nearby flowering bushes were non-parasitized. First, we describe the occurrence and consistency of this phenomenon across different sites and years. Second, we evaluate the spatial behavior of parasitized wasps on C. radicans bushes, which includes site-fidelity, exploitation and defense of rich extra-floral nectaries on buds and calices. Third, we record two critical steps of the lifecycle of X. vesparum on C. radicans: the parasite’s mating and a summer release of parasitic larvae, that can infect larval stages of the host if transported to the host’s nest. In a nutshell, C. radicans bushes provide many benefits both to the parasite X. vesparum and to its host: they facilitate the parasite’s mating and bivoltine lifecycle, a phenomenon never described before for this parasite, while, at the same time, they provide the wasp host with shelter inside trumpet flowers and extrafloral gland secretions, thus likely enhancing host survival and making it a suitable vector for the infection.
... Despite its apparently counterproductive nature, traumatic insemination (TI) has evolved repeatedly in a variety of invertebrates. In terrestrial arthropods, it is known to occur in multiple families of true bugs in the infraorder Cimicomorpha (Insecta: Hemiptera) (Schuh and Slater, 1995;Tatarnic et al., 2006Tatarnic et al., , 2014, the twisted wing parasites (Order Strepsiptera) (Beani et al., 2005;Peinert et al., 2016;Silvestri, 1940), some fruit flies (Diptera: Drosophila) (Kamimura, 2007), and a single species of spider (Aranea: Harpactea sadistica) (Řezáč, 2009). In simultaneously hermaphroditic taxa it is even more common, having arisen independently in various phyla, including the Acanthocephala (Doyle and Gleason, 1991), Annelida (Rouse and Pleijel, 2006), Gastrotricha (Kutschera and Wirtz, 1986), Gnathostomulida (Sterrer, 1974), Mollusca (104), Nematoda (Hugot, 1984), Platyhemlinthes (Michiels, 1998), and Rotifera (Aloia and Moretti, 1973) (for a comprehensive list see Lange et al., 2013). ...
... Additionally, the act of strepsipteran mating is unlikely to last long (Muir 1906) or to be repeated (Hughes-Schrader 1924). Furthermore, in at least 2 strepsipteran species it has been noted that males die just a few minutes after mating (Kathirithamby 1989;Beani et al. 2005), but our (presumably unmated) specimens normally survived for hours when allowed to do so. ...
Strepsiptera are a small order of obligately endoparasitic insects. Adult females are neotenic and never leave their host, instead bearing motile young that seek out their own insect hosts to infect. Males eclose without killing their hosts. In their 4-h adult lifespan, they fly off to search for mating opportunities, assisted by unconventional eyes with few, but large, ommatidia. Such distinctive features make Strepsiptera interesting in their own right, but also offer an opportunity to better understand evolutionary innovation. Unfortunately, Strepsiptera also are minute, reclusive, and difficult to obtain, severely reducing the study thereof, especially species not infecting solitary bees or social wasps. Here we describe methods for the successful capture of a strepsipteran species. We placed an ultraviolet light trap among Spartina alterniflora Loisel (Poaceae) shoots to attract adult male Elenchus koebelei Pierce (Strepsiptera: Elenchidae) in salt marshes in the southeastern United States. In 72 d of sampling, 488 adult males were captured between 30 min before and 15 min after sunrise. None arrived more than 63 min before or 36 min after sunrise. The majority of E. koebelei were caught at wind speeds ranging from 0 to 10 km/h; however, a light breeze of about 1.5 km/h appears to be preferred. The highest daily catches occurred when the temperature was between 23 and 26 °C. No Strepsiptera were caught at temperatures below 17 °C. With 521 adult male E. koebelei caught in a single light trap, our results show this little-known parasite may be reliably obtained, enhancing opportunities for further study.
... In at least one strepsipteran and two bedbug species, as well as in the Lyctocoridae and Plokiophilidae (true bugs), female structures evolved that tolerate, or facilitate, rather than resist male intromission. At body sites in which sister species show copulatory wounds or thickened tissue to resist intromission, females in these groups evolved a novel opening in the (Usinger 1966;Carayon 1974Carayon , 1977Beani et al. 2005). As a result, sperm delivery is not (any more) associated with trauma. ...
... Among the derived families of the order Strepsiptera (the so called 'twisted-wing parasites'), in genera such as Xenos, male and female development is similar until the fourth larval instar (Beani et al., 2005). At this point, males continue to develop normally, undergoing one more moult before pupation and eclosion. ...
1. Insects with complete metamorphosis (holometaboly) are extremely successful, constituting over 60% of all described animal species. Complete metamorphosis confers significant advantages because it enables organisms to optimise life-history components through temporal partitioning, and thereby to exploit multiple ecological niches. Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis.
2. In this review, we discuss different strategies that have evolved that result in the loss of complete metamorphosis (type I and type II paedomorphosis). In addition, the ecological pressures and developmental modifications that facilitate this avoidance are considered, as well as the importance of life cycle complexity in life-history evolution.
3. Interestingly, only female holometabolous insects have entirely avoided complete metamorphosis, and it is always the ancestrally juvenile morphology that is retained. These findings point to a strong sex-biased trade-off between investment in reproduction and development. While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described.
4. Thus, complete metamorphosis, which originated only once in insects, appears to have been almost fully retained. This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.
... After fertilization in the ovaries, embryos develop and extract nutrition from the pseudoplacental organs (Hagan, 1931). Hemocoelic insemination also occurs in twisted-wing parasites (Strepsiptera), where embryonic development occurs in the hemocoel instead of in the genital ducts (Beani et al., 2005;Pohl & Beutel, 2008Kathirithamby et al., 2015. In female tsetse flies (Diptera: Glossina), eggs are fertilized by spermathecal sperm, as in oviparous dipterans, while a specialized maternal organ nourishes the hatched larvae in the uterus (adenotrophic viviparity: Benoit et al., 2015). ...
Ovoviviparity or viviparity has evolved independently in animals and involves adaptations in females to accommodate developing embryos for a prolonged duration in their bodies, a condition which has likely to have influenced the evolution of the male genitalia. We aimed to ascertain whether the elongated male genitalia of the ovoviviparous free-living earwig species Marava arachidis (Dermaptera: Spongiphoridae) delivers sperm directly to the female ovaries where fertilization occurs. Males mated coercively with females by grabbing the female antenna with their mouth parts. Although females resisted the mating attempts, pairs mated 3.3 times on average over 15 h. The elongated intromittent organ, known as a virga, was inserted into the long-tubed spermatheca during insemination. Surgical ectomy of the spermatheca confirmed that sperm migrated from here to the ovaries with a variable delay. A pair of sclerites in the male genitalia frequently inflicted wounds near the spermathecal opening, while the single, thin virga sometimes broke off during mating. However, unlike earwigs bearing a 'spare' virga, damage was restricted to the tip of the virga, without which the males could still inseminate the females. We discuss the evolution of the genitalia in this insect in the light of sexual selection and sexual conflict over mating and fertilization.
... The Strepsiptera are a small, cosmopolitan insect order, whose members exhibit extreme sexual dimorphism, with short-living flying males and neotenic endoparasite females (Kathirithamby, 1989;Beani et al., 2005). Besides the evident morphological oddities, strepsipterans also exhibit other peculiarities at the genetic and molecular level, such as having the smallest nuclear genome recorded among insects (Johnston et al., 2004), unique insertions in the nuclear 18S rRNA (Gillespie et al., 2005) and accelerated rates of molecular evolution in the 18S rRNA gene (Carmean and Crespi, 1995;Huelsenbeck, 1998). ...
In this study, the nearly complete sequence (14,519 bp) of the mitochondrial DNA (mtDNA) of the entomophagous endoparasite Xenos vesparum (Insecta: Strepsiptera) is described. All protein coding genes (PCGs) are in the arrangement known to be ancestral for insects, but three tRNA genes (trnA, trnS(gcu), and trnL(uag)) have transposed to derived positions and there are three tandem copies of trnH, each of which is potentially functional. All of these rearrangements except for that of trnL(uag) is within the short span between nad3 and nad4 and there are numerous blocks of unassignable sequence in this region, perhaps as remnants of larger scale predisposing rearrangements. X. vesparum mtDNA nucleotide composition is strongly biased toward A and T, as is typical for insect mtDNAs. There is also a significant strand skew in the distribution of these nucleotides, with the J-strand being richer in A than T and in C than G, and the N-strand showing an opposite skew for complementary pairs of nucleotides. The hypothetical secondary structure of the LSU rRNA has also been reconstructed, obtaining a structural model similar to that of other insects.
... Except for acting as a retainer for developing embryos, the neotenic female has few functions. The cephalothorax provides a mechanism for copulation, wherein the male inserts sperm cells via the brood canal (Meinert, 1896; Kathirithamby, 2000; Beani et al., 2005), which may also occur, at least in some species, via traumatic insemination as the result of the aedeagus piercing the body of the neotenic female (Silvestri, 1941d; Lauterbach, 1954; Pohl and Beutel, 2008). Giusti et al. (2007) proposed that after extrusion of the cephalotheca, there appears to be no absorption of nutrients from the host in the strepsipteran Xenos veparum, leaving the neotenic female to survive on previously formed adipocytes. ...
The order Strepsiptera comprises an enigmatic group of insects with a complex life cycle that includes a long, obligate endoparasitic phase. Due to the unusual characteristics of the strepsipteran life cycle, its natural history and classification have long been a source of confusion. Unique life-history strategies and extreme morphological modifications within this group have promoted many philosophical discussions between systematists and entomologists. Although this situation had left the relationship of strepsipterans with other insect groups continually in question for many years, the current general consensus is that Strepsiptera is a sister group to Coleoptera. Members of the Strepsiptera exhibit pronounced sexual dimorphism, 2 distinct larval forms, a pupal stage, host manipulation, and morphological characteristics that include many unusual differences from other insects.
... than resist male intromission. At body sites in which sister species show copulatory wounds or thickened tissue to resist intromission, females in these groups evolved a novel opening in the integument (Usinger 1966;Carayon 1974Carayon , 1977Beani et al. 2005). As a result, sperm delivery is not (any more) associated with trauma. ...
Copulatory wounding (CW) is widespread in the animal kingdom, but likely underreported because of its cryptic nature. We use four case studies (Drosophila flies, Siphopteron slugs, Cimex bugs, and Callosobruchus beetles) to show that CW entails physiological and life-history costs, but can evolve into a routine mating strategy that, in some species, involves insemination through the wound. Although interspecific variation in CW is documented, few data exist on intraspecific and none on individual differences. Although defensive mechanisms evolve in the wound recipient, our review also indicates that mating costs in species with CW are slightly higher than in other species. Whether such costs are dose- or frequency-dependent, and whether defense occurs as resistance or tolerance, decisively affects the evolutionary outcome. In addition to sexual conflict, CW may also become a model system for reproductive isolation. In this context, we put forward a number of predictions, including (1) occasional CW is more costly than routine CW, (2) CW is more costly in between- than within-population matings, and (3) in the presence of CW, selection may favor the transmission of sexually transmitted diseases if they induce resource allocation. Finally, we outline, and briefly discuss, several medical implications of CW in humans.
Copyright © 2015 Cold Spring Harbor Laboratory Press; all rights reserved.
... A recent first report of intra-genitalic TI in Drosophila (Kamimura 2007), one of the most wellstudied of all the insects, suggests that intra-genitalic TI might be more prevalent in insects than currently appreciated. Examples of extra-genitalic TI come from only the orders Strepsiptera (Beani et al. 2005), Lepidoptera and Heteroptera. All heteropteran examples are from the infraorder Cimicomorpha ( Tatarnic et al. 2006), perhaps the best known example being the bed bug, Cimex lectularius (Stutt & Siva-Jothy 2001). ...
Spiders of the genus Harpactea (Araneae: Dysderidae) are non-web building predators that forage on the ground and on tree trunks at night. During the day, they hide in silk retreats under stones or wood, in leaf litter or under tree bark. They occur mainly in xerothermic forests (see Deeleman-Reinhold 1993). Harpactea is the second most speciose dysderid genus (after Dysdera), with 149 described and valid species (Platnick 2007). Interestingly, almost all species appear to be endemics that are narrowly restricted to parts of the Mediterranean, with only some representatives also found in adjacent areas (Platnick 2007). The contributions to the Harpactea fauna of the Middle East were made by Denis (1955), who described the two new species from Lebanon (Harpactea rugichelis Denis, 1955 and H. straba Denis, 1955), and by Brignoli (1978), who described the species Harpactea herodis Brignoli, 1978 from Israel.
... Noskiewicz and Poluszy nski (1928 [see table 7]) identified few spermatozoa within eggs of S. ovinae and Beani et al. (2005) within eggs of Xenos vesparum Rossi, 1793 (Xenidae, Strepsiptera). The precise process of entering the egg has not been observed and documented yet. ...
External features of the embryonic development of Stylops ovinae (Strepsiptera) were examined. Eighteen distinct embryological stages are suggested. Many embryological traits are closely correlated to the parasitic life style of the first instar larvae or to vivparity. The high number of eggs, their small size, the characteristic egg membrane, and the lack of micropyles are derived groundplan features of Strepsiptera. The development with a semi-long germ embryo is shared with several other groups of Holometabola. The reduction of the labrum and antennae are autapomorphies of Strepsiptera. The cephalic ventral plate of the first instar larva of S. ovinae is formed by parts of the head capsule and the anlagen of the maxillae and labium. It is involved in the formation of the specific entognathous condition, and the entire character complex is autapomorphic for Stylopidae. The trochanter is recognizable in the anlagen of all three legs. Its fusion with the femur in the later stages is an autapomorphy of Stylopidia. The extreme spiralization and compression of the abdomen during blastokinesis is a derived feature, like the reduction of the anlagen of the anterior abdominal appendages. The caudal bristles on segment XI are possibly re-activated cerci. The same is likely in the case of segment XI.
... Among the morphophysiological changes induced by the parasite, the most dramatic is the castration of female hosts (Strambi et al. 1982;Beani et al. 2011). Infected females aggregate near leks, where the parasite mates (Beani et al. 2005), increasing their chances of encountering sexually active males. Thus, discriminating between healthy fertile and parasite-castrated gynes should also be beneficial for males because only the former will be able to reproduce the following season. ...
Discrimination among potential partners is a critical step in sexual selection to avoid wasting reproductive
resources on an unsuitable mate. In the female-dominated hymenopteran societies males have
often been regarded as ‘flying sperm containers’ spending all their time and energy in trying to acquire a
mate.We investigated the male sexual preference for potential partners using as a model the primitively
eusocial wasp Polistes dominula in which female caste is rather flexible and difficult to determine. By
means of laboratory bioassays, we compared the males’ behaviour towards females of different reproductive
potential. Males were able to recognize female castes, strongly preferring reproductive females to
workers, regardless of female age or health. The results show that in this species caste plays a key role in
orienting male discrimination and preference, presumably through chemical cues, towards reproductive
females both healthy and parasite-castrated. Overall, our study shows that social Hymenoptera males are
not always ‘small mating machines’ eager to mate.
... Strepsiptera are extremely specialized in all life stages and also in their development and reproductive biology, including a very atypical fertilization of eggs floating freely in the hemolymph in the body cavity of the highly modified females (e.g., Beani et al., 2005;Pohl and Beutel, 2008;H. Pohl pers. ...
... Considering the highly simplified copulatory mechanism of Strepsiptera associated with the sessile, larviform adult females in the suborder Stylopidia, selective pressures on sperm size, structure, and function must presumably be singularly distinct from insects whose sexually mature females are motile and not larviform as in Mengenillidae (suborder Mengenillidia). Sperm is inserted in the brood canal opening of the extruded cephalothorax in all the endoparasitic females in the suborder Stylopidia [3,19], while in Mengenillidae (one of the two families in the primitive suborder Mengenillidia), traumatic insemination takes place where the male pierces any part of the free-living female to insert the sperm [20]. ...
The unusual life style of Strepsiptera has presented a long-standing puzzle in establishing its affinity to other insects. Although Strepsiptera share few structural similarities with other insect orders, all members of this order share a parasitic life style with members of two distinctive families in the Coleopterathe order now considered the most closely related to Strepsiptera based on recent genomic evidence. Among the structural features of several strepsipteran families and other insect families that have been surveyed are the organization of testes and ultrastructure of sperm cells. For comparison with existing information on insect sperm structure, this manuscript presents a description of testes and sperm of a representative of the most primitive extant strepsipteran family Mengenillidae, Eoxenos laboulbenei. We compare sperm structure of E. laboulbenei from this family with that of the three other families of Strepsiptera in the other strepsipteran suborder Stylopidia that have been studied as well as with members of the beetle families OPEN ACCESS Insects 2013, 4 464 Meloidae and Rhipiphoridae that share similar life histories with Strepsiptera. Meloids, Rhipiphorids and Strepsipterans all begin larval life as active and viviparous first instar larvae. This study examines specific ultrastructural features of their organelles.
... At this time, parasitized female wasps have already deserted their colony, where they did not perform any social task, to cluster in aberrant summer aggregations (first observed by W. D. Hamilton in several species of Polistes; Hughes 2002). Here, the free-living winged X. vesparum males break their pupal cap and abandon their hosts to fertilize the permanently endoparasitic female (Beani et al. 2005). A Xenos male dies within a few hours of emergence, whereas a female may survive until the next spring, well protected inside the abdomen of a female wasp. ...
The macroparasite Xenos vesparum affects both the behaviour and the physical traits of its host, the social wasp Polistes dominulus. Female wasps, if parasitized, do not perform any social tasks and desert the colony to gather at specific sites, where the parasite mates; at the end of summer they form prehibernating clusters joined by healthy future queens to overwinter. Parasitized wasps become highly gregarious. In April, healthy wasps leave the aggregations to found new colonies, while parasitized wasps remain in overwintering groups and release parasites to infect wasp larvae only later in the season. We studied the prolonged gregarious behaviour of parasitized wasps and analysed the morphology of parasitized and healthy wasps in aggregations collected over a 7-year period to determine whether the parasite affects host size, wing symmetry, ovarian development and lipid stores. All parasitized wasps were smaller and had undeveloped ovaries and more wing fluctuating asymmetry than unparasitized wasps, irrespective of time of year, parasite load and parasite sex. If infected only by one or two X. vesparum females, the wasps had large fat bodies, which could facilitate their overwintering. In contrast, wasps infected by at least one male parasite had little lipid and died at the end of the summer. Thus, X. vesparum, may play a role in the fate of its host, by exploiting wasps' tendency to form aggregations outside the colony and by altering its caste system, nutrient allocation, diapause timing and life span to achieve its own reproduction and dispersal.
... Thereafter, the parasite develops within the wasp's hemocoel in perfect synchronization with the wasp's developmental maturation, until the wasp reaches adulthood ). Unlike healthy workers, parasitized wasps do not contribute to the growth and welfare of the colony but instead abandon the nest early in their adult life and aggregate in groups where mating of the parasites may occur (Hughes et al. 2004;Beani et al. 2005). Wasps with female parasites overwinter in large aggregations with healthy future queens (Beani et al. 2011). ...
Successful invaders often become established in new ranges by outcompeting native species. The "evolution of increased competitive ability" hypothesis predicts that invasive species are subjected to less predation and parasitization than sympatric native species, and thus can allocate resources from defence and immunity to growth and fecundity, thereby achieving higher fitness. In this study, we examined whether American invasive Polistes dominula paper wasps have reduced immunocompetence. To explore this scenario, we tested their susceptibility towards parasites and pathogens at both the individual (immune defence) and colony levels, i.e. hygienic behaviour (removal of diseased individuals by nestmates). First, we examined the response to the specific coevolved parasite Xenos vesparum (lost after invasion) in terms of individual host susceptibility and hygienic behaviour. Second, we explored the response against general pathogens by quantifying the bacterial clearance in individual wasps after a challenge with Escherichia coli and hygienic behaviour after a challenge with the fungus Beauveria bassiana. Our results show that American invasive P. dominula have a higher response against X. vesparum at the colony level, but at the individual level their susceptibility is not significantly different from conspecifics of the native range. On the other hand, invasive P. dominula display lower response after a challenge with general pathogens at both the individual and colony levels. While supporting the hypothesis of a reduction of immunocompetence towards general pathogens in invasive species, these findings also suggest that the response against coevolved parasites might follow different evolutionary pathways which are not always easily predictable.
... A putative pitfall for phylogenetic comparisons is that the traumatic origin of a given copulatory mechanism is often masked. For example, females of the parasitic strepsipteran, Xenos vesparum have evolved an extragenital duct system into which sperm can be delivered non-traumatically (Beani et al., 2005). This observation shows how traumatic mating can disappear phylogenetically. ...
Copulation can involve the wounding of the mating partner by specialised devices. This type of mating, which we term traumatic mating, has been regarded as exceptional. Its prevalence, however, has not been compared across taxa, nor have its functions and putative evolutionary pathways. A categorisation has been lacking to date. We here show that traumatic mating is a widespread and diverse phenomenon that likely evolved via several pathways. Its putative functions include: (i) anchorage during mating; (ii) stimulation of short-term female reproductive investment; (iii) male paternity advantages; and (iv) enhanced fertilisation efficiency in transitions to internal fertilisation. Both natural and sexual selection have likely contributed to the parallel evolution of traumatic intromittent organs in phylogenetically distant taxa. These organs are sometimes remarkably similar in shape and often, but not always, inject sperm. The target sites of trauma infliction and the nature of secretions delivered alongside sperm are thus far poorly studied, but data on both are needed to elucidate the function of traumatic mating. The few existing studies that explicitly quantify fitness impacts of traumatic mating indicate that this strategy may often be costly to the party being wounded. However, a comprehensive approach to assess overall investments and returns for both sexes is a major target for future work. Finally, for the first time, we corroborate quantitatively the hypothesis that traumatic mating evolved relatively more often among hermaphroditic than among gonochoric taxa.
... A recent first report of intra-genitalic TI in Drosophila (Kamimura 2007), one of the most wellstudied of all the insects, suggests that intra-genitalic TI might be more prevalent in insects than currently appreciated. Examples of extra-genitalic TI come from only the orders Strepsiptera (Beani et al. 2005), Lepidoptera and Heteroptera. All heteropteran examples are from the infraorder Cimicomorpha ( Tatarnic et al. 2006), perhaps the best known example being the bed bug, Cimex lectularius (Stutt & Siva-Jothy 2001). ...
The males of invertebrates from a few phyla, including arthropods, have been reported to practise traumatic insemination (TI; i.e. injecting sperm by using the copulatory organ to penetrate the female's body wall). As all previously reported arthropod examples have been insects, there is considerable interest in whether TI might have evolved independently in other arthropods. The research reported here demonstrates the first case of TI in the arthropod subphylum Chelicerata, in particular how the genital morphology and mating behaviour of Harpactea sadistica (Rezác 2008), a spider from Israel, has become adapted specifically for reproduction based on TI. Males have needle-like intromittent organs and females have atrophied spermathecae. In other spiders, eggs are fertilized simultaneously with oviposition, but the eggs of H. sadistica are fertilized in the ovaries (internal fertilization) and develop as embryos before being laid. Sperm-storage organs of phylogenetically basal groups to H. sadistica provide males with last male sperm priority and allow removal of sperm by males that mate later, suggesting that TI might have evolved as an adaptive strategy to circumvent an unfavourable structure of the sperm-storage organs, allowing the first male to mate with paternity advantage. Understanding the functional significance of TI gives us insight into factors underlying the evolution of the genital and sperm-storage morphology in spiders.
... These are found in females of a variety of insect species and other taxa (Carayon 1966, Carayon 1977Eberhard 1985). In some species they occur very frequently or even regularly (van Damme et al. 1998;Sota and Kubota 1998;Fraser et al. 1999;Crudgington and Siva-Jothy 2000;Blanckenhorn et al. 2002;Nunez et al. 2004;Beani et al. 2005;Kamimura 2007). In humans, micro traumata in the mucus layer of the genitalia that arise from sexual intercourse, if rarely investigated (Fraser et al. 1999;van Damme et al. 1998;Nunez et al. 2004) are one of the main entrance areas for STDs into the body. ...
Male genitalia are more variable between species (and populations) than other organs, and are more morphologically complex in polygamous compared to monogamous species. Therefore, sexual selection has been put forward as the major explanation of genital variation and complexity, in particular cryptic female choice for male copulatory courtship. As cryptic female choice is based on differences between males it is somewhat paradoxical that there is such low within-species variation in male genitalia that they are a prime morphological identification character for animal species. Processes other than sexual selection may also lead to genitalia variation but they have recently become neglected. Here I focus on pleiotropy and natural selection and provide examples how they link genitalia morphology with genital environments. Pleiotropy appears to be important because most studies that specifically tested for pleiotropic effects on genital morphology found them. Natural selection likely favours certain genital morphology over others in various environments, as well as by reducing re-infection with sexually transmitted diseases or reducing the likelihood of fertilisation with aged sperm. Both pleiotropy and natural selection differ locally and between species so may contribute to local variation in genitalia and sometimes variation between monogamous and polygamous species. Furthermore, the multitude of genital environments will lead to a multitude of genital functions via natural selection and pleiotropy, and may also contribute to explaining the complexity of genitalia.
... The Strepsiptera are a small, cosmopolitan insect order, whose members exhibit extreme sexual dimorphism, with short-living flying males and neotenic endoparasite females (Kathirithamby, 1989;Beani et al., 2005). Besides the evident morphological oddities, strepsipterans also exhibit other peculiarities at the genetic and molecular level, such as having the smallest nuclear genome recorded among insects (Johnston et al., 2004), unique insertions in the nuclear 18S rRNA (Gillespie et al., 2005) and accelerated rates of molecular evolution in the 18S rRNA gene (Carmean and Crespi, 1995;Huelsenbeck, 1998). ...
In this study, the nearly complete sequence (14,519 bp) of the mitochondrial DNA (mtDNA) of the entomophagous endoparasite Xenos vesparum (Insecta: Strepsiptera) is described. All protein coding genes (PCGs) are in the arrangement known to be ancestral for insects, but three tRNA genes (trnA, trnS(gcu), and trnL(uag)) have transposed to derived positions and there are three tandem copies of trnH, each of which is potentially functional. All of these rearrangements except for that of trnL(uag) is within the short span between nad3 and nad4 and there are numerous blocks of unassignable sequence in this region, perhaps as remnants of larger scale predisposing rearrangements. X. vesparum mtDNA nucleotide composition is strongly biased toward A and T, as is typical for insect mtDNAs. There is also a significant strand skew in the distribution of these nucleotides, with the J-strand being richer in A than T and in C than G, and the N-strand showing an opposite skew for complementary pairs of nucleotides. The hypothetical secondary structure of the LSU rRNA has also been reconstructed, obtaining a structural model similar to that of other insects.
... They are larviparous permanent endoparasites, which at maturity fill most of the wasp hemocoelic cavity, and lack distinct antennae, mouthparts, eyes, wings, legs, and external genitalia. The opening of the ventral canal in the cephalothorax allows both the extragenital insemination and the escape of the triungulins (Beani et al., 2005a). ...
To successfully complete its endoparasitic development, the strepsipteran Xenos vesparum needs to elude the defense mechanisms of its host, the wasp Polistes dominulus. SEM and TEM observations after artificial infections allow us to outline the steps of this intimate host-parasite association. Triungulins, the mobile 1st instar larvae of this parasite, are able to "softly" overcome structural barriers of the larval wasp (cuticle and epidermis) without any traumatic reaction at the entry site, to reach the hemocoel where they settle. The parasite molts 48 h later to a 2nd instar larva, which moves away from the 1st instar exuvium, molts twice more without ecdysis (a feature unique to Strepsiptera) and pupates, if male, or develops into a neotenic female. Host encapsulation involves the abandoned 1st larval exuvium, but not the living parasite. In contrast to the usual process of encapsulation, it occurs only 48 h after host invasion or later, and without any melanization. In further experiments, first, we verified Xenos vesparum's ability to reinfect an already parasitized wasp larva. Second, 2nd instar larvae implanted in a new host did not evoke any response by hemocytes. Third, we tested the efficiency of host defense mechanisms by implanting nylon filaments in control larval wasps, excluding any effect due the dynamic behavior of a living parasite; within a few minutes, we observed the beginning of a typical melanotic encapsulation plus an initial melanization in the wound site. We conclude that the immune response of the wasp is manipulated by the parasite, which is able to delay and redirect encapsulation towards a pseudo-target, the exuvia of triungulins, and to elude hemocyte attack through an active suppression of the immune defense and/or a passive avoidance of encapsulation by peculiar surface chemical properties.
Polyandry, the practice of females mating with multiple males, is a strategy found in many insect groups. Whether it increases the likelihood of receiving beneficial genes from male partners and other potential benefits for females is controversial. Strepsiptera are generally considered monandrous, but in a few species females have been observed copulating serially with multiple males. Here we show that the offspring of a single female can have multiple fathers in two Strepsiptera species: Stylops ovinae (Stylopidae) and Xenos vesparum (Xenidae). We studied female polyandry in natural populations of these two species by analysis of polymorphic microsatellite loci. Our results showed that several fathers can be involved in both species, in some cases up to four. Mating experiments with S. ovinae have shown that the first male to mates with a given female contributes to a higher percentage of the offspring than subsequent males. In X. vesparum, however, we found no significant correlation between mating duration and offspring contribution. The prolonged copulation observed in S. ovinae may have the advantage of reducing competition with sperm from other males. Our results show that monandry may not be the general pattern of reproduction in the insect order Strepsiptera.
Polyembryony is a unique form of asexual reproduction whereby multiple offspring are produced from a single egg or zygote. To use Craig et al.’s (1997) words, polyembryony is a paradoxical combination of two reproductive modes—sexual and asexual reproduction. Nevertheless, it has evolved and been maintained in a wide range of taxa, including rust fungi (Alexopoulos 1952; Craig et al. 1997), algae (Searles 1980), and animals (Craig et al. 1997; Sköld et al. 2009), including the well-known phenomenon of identical twins in humans.
An annotated taxonomic and nomenclatural catalogue of the insect order Strepsiptera is presented. Known distributions and host associations are given as they are currently known. As of this publication, there are 627 valid species, 28 of which are known only from fossils. The misspelling of Viridipromontorius as Viridopromontoriusn. syn. (Roy and Niladri, 2016) is corrected to include Viridipromontorius aequus n. comb.Caenocholax pierci is moved to the genus Myrmecolax and becomes Myrmecolax pierci (Chattopadhyay and Chaudhuri, 1980) n. comb. Stichotrema trinadadensisGuenther, 1949) n. comb. is moved from Stichotrema to Myrmecolax. Halictophagus bohartiAbdulla, 1974 n. stat. was previously a junior synonym of Halictophagus variatus due to its being an invalid renaming of a homonym. The following species are reinstated as valid: Pseudoxenos andradeiLuna de Carvalho, 1953; Pseudoxenos atlanticusLuna de Carvalho, 1969 n. stat.; Pseudoxenos corcyricusSaunders, 1872; Pseudoxenos klugii (Saunders, 1852); Pseudoxenos lusitanicusLuna de Carvalho, 1960; Pseudoxenos schaumiiSaunders, 1872; Pseudoxenos seyrigi Monod, 1926; Stylops aburanaeKifune and Maeta, 1990 n. stat.; Stylops ainoKifune and Maeta, 1990 n. stat.; Stylops alfkeniHofeneder, 1939 n. stat; Stylops bimaculatae Perkins, 1918 n. stat.; Stylops bisalicidis Pierce, 1918 n. stat.; Stylops championi Pierce, 1918 n. stat.; Stylops collinusKifune and Maeta, 1990 n. stat.; Stylops dentataeKifune and Maeta, 1990 n. stat.; Stylops dominiqueiPierce, 1909 n. stat.; Stylops duboisi Bohart, 1937 n. stat.; Stylops duriensisLuna de Carvalho, 1974 n. stat.; Stylops esteponensisLuna de Carvalho, 1974 n. stat.; Stylops flavipedisHofeneder, 1923 n. stat.; Stylops fukuiensis Kifune, 1991 n. stat.; Stylops giganteusLuna de Carvalho, 1974 n. stat.; Stylops hirashimaiKifune and Maeta, 1990 n. stat.; Stylops izumoensisKifune and Maeta, 1990 n. stat.; Stylops krygeri Pierce, 1918 n. stat.; Stylops mandibularisPierce, 1911 n. stat.; Stylops medionitansPierce, 1919 n. stat.; Stylops moestae Pierce, 1918 n. stat.; Stylops muelleri Borchert, 1971 n. stat.; Stylops neonanae Pierce 1918 n. stat.; Stylops nipponicusKifune and Maeta, 1990 n. stat.; Stylops nitidaePasteels 1954 n. stat.; Stylops nitidiusculaePoluszyński 1927 n. stat.; Stylops oblongulusKifune and Hirashima, 1985 n. stat.; Stylops oklahomaePierce, 1909 n. stat.; Stylops orientisKifune and Maeta, 1990 n. stat.; Stylops pacificusBohart, 1936 n. stat.; Stylops perkinsiPasteels 1949 n. stat.; Stylops saliciflorisPierce, 1909 n. stat.; Stylops subcircularisKifune and Maeta, 1990 n. stat.; Stylops swenkiPierce 1909 n. stat.; Stylops truncatoidesKifune and Hirashima, 1985 n. stat. Stylops truncatusKifune and Hirashima, 1985 n. stat.; Xenos myrapetrus (Trois, 1988).
No consensus exists for the homology and terminology of the male genitalia of the Hexapoda despite over a century of debate. Based on dissections and the literature, genital skeletomusculature was compared across the Hexapoda and contrasted with the Remipedia, the closest pancrustacean outgroup. The pattern of origin and insertion for extrinsic and intrinsic genitalic musculature was found to be consistent among the Ectognatha, Protura, and the Remipedia, allowing for the inference of homologies given recent phylogenomic studies. The penis of the Hexapoda is inferred to be derived from medially-fused primary gonopods (gonopore-bearing limbs), while the genitalia of the Ectognatha are inferred to include both the tenth-segmental penis and the ninth-segmental secondary gonopods, similar to the genitalia of female insects which comprise gonopods of the eighth and ninth segments. A new nomenclatural system for hexapodan genitalic musculature is presented and applied, and a general list of anatomical concepts is provided. Novel and refined homologies are proposed for all hexapodan orders, and a series of groundplans are postulated. Emphasis is placed on the Endopterygota, for which fine-grained transition series are hypothesized given observed skeletomuscular correspondences.
Beani L., Massolo A. – Polistes dominulus wasps (Hymenoptera Vespidae), if parasitized by Xenos vesparum (Strepsiptera
Stylopidae), wander among nests during the pre-emergence phase.
This study is focused on the spatial behaviour of overwintered Polistes dominulus wasps, either unparasitized or
parasitized by Xenos vesparum (Strepsiptera). The neotenic female endoparasites protrude their cephalothorax from
the host abdomen and, after winter diapause, hundreds of 1st instar larvae, the infective free-living stage, emerge alive
and move from the brood canal of the cephalothorax to the substrate. We carried out spring transects along artificial
hibernation/nesting sites showing a high site-attachment of healthy wasps before and mainly after nest foundation,
whereas parasitized ones moved from one colony to another just when wasp larvae, the target of infection, are present
in nests. These data support the hypothesis of a direct release of Xenos larvae on/close to nests although phoresy,
assumed as the usual infection mechanism for Strepsipterans, is also possible.
KEY WORDS: Strepsiptera, paper wasps, spatial behaviour, phoretic infection, nest infection.
The first-instar larvae of strepsipteran parasites, commonly referred to as “triungulins”, are the host-seeking stage: they must locate, invade and successfully develop in the new host, in order to start their parasitic cycle. Little information is available about the behaviour of Xenos vesparum triungulins. They emerge in batches from the endoparasitic female infecting Polistes dominulus, the primary host, and reach the nest through a vector (a foraging wasp or the parasitised wasp itself). Once there, they have the possibility to penetrate into wasp immatures at different developmental stages. In this study, we performed preliminary analyses aimed to investigate which cues are important to direct triungulin movements during their brief stay in wasp nests. In laboratory conditions we selectively presented different stimuli to Xenos larvae: apparently, the host larva itself is attractive in an open arena, but not inside a confined space, nor are epicuticular compounds of wasp larvae able to control triungulin movements. These are more likely oriented by their gregarious behaviour, whereas light (positive phototaxy) may at a previous stage enhance their emergence via the brood canal opening in the female cephalothorax.
A representative sample of first instar larvae of stylopid parasites (Strepsiptera) was investigated. The main focus was on the external morphology, which was recorded with scanning electron microscopy. The anatomy of a plesiomorphous taxon (Mengenilla chobauti) and an apomorphous taxon (Stylops melittae) was investigated by means of light microscopy. The results were used in a cladistic analysis of the phylogenetically relevant characters. In addition, the first instar larvae of Strepsiptera were compared with larvae of those taxa which have recently been proposed as sistergroups of the Strepsiptera.
The head capsule of the first instar larvae is strongly flattened dorsoventrally. The ventral attachment of the head can be formed in three ways: ventrum of the cervix (Mengenillidae, Corioxenidae, Halictophagidae, Myrmecolacidae, Xeninae, Paraxeninae), rostral part of the pleural membrane of the prothorax (Elenchidae), or a hypostomal bridge (Stylopinae). A gula is never found. There are two external openings of the head: an apical and a ventral opening. The true mouth opening is situated at the ventro-caudal margin of the preoral cavity. The maxillae are fused medially and form the ventral margin of the preoral cavity. The prognathous mandibles can be moved in the horizontal plane, and are situated at the rostral border of the preoral cavity. Maxillary palps are present in all taxa; labial palps are absent in the Stylopidae. Six pairs of stemmata are present in the primary state. The "antennal field" which is found in several taxa is interpreted as the antennal primoridum. Unlike the adults, the first instar larvae possess a tentorium. The mandibles articulate at the anterior tentorial arms. A tentorial bridge across the posterior tentorial arms is absent. Both M. chobauti and S. melittae have the stomodaeum present as a skeleton, which is referred to as the "pharyngeal rod".
The nota of the thorax have paired setae. These setae are arranged in three longitudinal rows on each side in the Mengenillidae, and in two rows in the remaining families. Stout spinulae are present at the caudal margin of the terga in the Stylopinae. The sternal plates, medio-caudal processes of the sternum, are developed in very different ways. The legs are divided into coxa, trochanterofemur, tibia and a one-segmented tarsus. The tarsi are structurally modified in the individual genera. Ungues are never present. There is probably a correlation between the form and size of the tarsi and the features of the specific hosts.
The abdomen consists of eleven segments. The caudal margins of terga and sterna are covered with stout spinulae in the Stylopinae. In all the other taxa, only the ventral parts of the terga and sterna have spinulae. There are setae on the terga and sterna. The Mengenillidae have a greater number of setae than the Stylopidia. The first eight abdominal segments are homonomous in structure. Segments nine and ten are fused dorsally and are strongly sclerotisised in all taxa with the exception of some Stylopinae. In the Stylopinae the tenth abdominal segment is much reduced in size, and the eleventh segment is divided medially. In all taxa the eleventh segment has two stout caudal setae, which are interpreted as cerci. Limb vestiges on segment nine appear in the form of stout paired setae. The musculature of the first seven abdominal segments is identical in M. chobauti and S. melittae. Probably all first instar larvae can jump, with the exception of the Stylopinae. The jumping mechanism was clarified through studies of Eoxenos laboulbenei and M. chobauti.
The central nervous system is strongly concentrated and located far back in the thorax. It consists of the supraoesophageal ganglion and a suboesophageal ganglionic mass. The number of ganglia in the suboesophageal ganglionic mass is four in both M. chobauti and S. melittae. The alimentary canal is clearly divided into stomodaeum, mesenteron and proctodaeum. The mesenteron is closed to the proctodaeum.
A quantitative cladistic analysis of the characters of the first instar Strepsiptera larvae that were examined resulted in: 1. bifurcation between the Mengenillidia and Stylopidia; 2. the Elenchidae and Corioxenidae are placed at the base of the Stylopidia; 3. the Halictophagidae are the sister-group of the Xeninae + Myrmecolacidae + Stylopinae; 4. the Xeninae are the sister-group of the Myrmecolacidae + Stylopinae. This larval tree disagrees in some points with the tree given by Kinzelbach (1978, 1990), which was based mainly on characters of the adults. An attempt was made to resolve these inconsistencies through a comparison with the characters of the adults.
Synapomorphies with the larvae of the Coleoptera, Diptera, Mecoptera and Siphonaptera could not be found. The shift of the brain back into the thorax in Strepsiptera and Diptera could be interpreted as a derived character shared with the Diptera.
Development in the totally endoparasitic female Strepsiptera has been clarified by light and electron microscopy. At the end of the 4th instar the cuticle sclerotizes anteriorly to form the cephalothorax and collar, the former of which is later extruded through the host cuticle. Posteriorly, the cuticle remains unsclerotized, and this region is within the host. The moult to the neotenic adult takes place within the 4th instar cuticle, and the epicuticles of the previous instars are retained as persistent sheaths. The gut, which is present in the earlier endoparasitic stages, is lost after extrusion of the cephalothorax, and a novel structure develops on the ventral surface of the neotenic female. Due to the position of this novel structure in the neotenic female, this area is called an apron. The detailed structure of the membranes in the apron in Stichotrema dallatorreanum Hofeneder from Oro Province, and of another female myrmecolacid (which has a different host) from West New Britain in Papua New Guinea, is described. A dual function for the apron is proposed.
The morphology, biology and life history of the immature stages, the free-living and the neotenic females (of the suborders Mengenillidia and Stylopidia respectively) and the free-living males of the order Strepsiptera are discussed. Strepsiptera are entomophagous parasitoids and are known to parasitize seven orders and thirty-five families of Insecta. The morphological and physiological changes they cause to the host insect are outlined. The classification of the order is revised; the geographical distribution, phylogenetic system and keys to the families, subfamilies and genera (when possible) are given. As the sexes are dimorphic, separate keys are provided for adult males and neotenic females.
Summary. hough the paper wasp genus, Polistes, is well studied, we know little of the incidence of parasitism in this group. Here we present details of 45 nest dissections for 4 species: P. dominulus (Christ), P. gallicus (L.), P. stabilinus Richards and P. carnifex (F.) to detail levels of parasitism of colony members by the obligate parasitic group of insects, the Strepsiptera. All 4 species showed evidence of parasitism among immature members. For 3 species, more than 50% of inspected nests were parasitized and the levels of parasitism among brood (larvae and pupae) was very high and did not differ significantly between parasitized nests. One species, P. stabilinus, suffered very low levels of parasitism, which may be related to its habitat choice. The number of parasites per host was positively related to the proportion of infected brood (parasite prevalence) and in some cases reached phenomenally high levels, which casts doubt on previ ously assumed mechanisms of infection for nest-making Hymenoptera, i.e. phoresy. We also document cases of egg parasitism and encapsulation in Polistes nests. Our data show that parasitism levels greatly varied among areas. Finally, the recent debate on the competitive advantage of P. dominulus in its introduced range, USA, has credited an absence of strepsipteran parasites of this species in facilitating its spread. For the first time, we document levels of parasitism for this species in its nature P range and this would appear to corroborate previous claims. We place our work in the context of other studies of parasitism of social insects and posit that the genus Polistes may have much to offer to this field.
Infection of the paper wasp, Polistes dominulus (Christ), by the strepsipteran parasite Xenos vesparum Rossi results in a dramatic behavioral change, which culminates in colony desertion and the formation of extranidal aggregations, in which up to 98% of occupants are parasitized females. Aggregations formed on prominent vegetation, traditional lek-sites of Polistes males, and on buildings, which were later adopted as hibernating sites by future queens. First discovered by W.D. Hamilton, these aberrant aggregations are an overlooked phenomenon of the behavioral ecology of this intensively studied wasp. For 3 months in the summer of 2000, during the peak of colony development, we sampled 91 extranidal aggregations from seven areas, numbering 1322 wasps. These wasps were parasitized by both sexes of X. vesparum, but males were more frequent from July until mid-August, during the mating season of the parasite. Aggregations were present for days at the same sites (in one case a leaf was occupied for 36 consecutive days) and were characterized by extreme inactivity. After artificial infection, parasitized "workers" deserted the nest 1 week after emergence from their cell and before the extrusion of the parasite through the host cuticle. Infected individuals did not work, were more inactive, and did not receive more aggression than did controls. We suggest that early nest desertion and subsequent aggregations by parasitized nominal workers and "future queens" is adaptive manipulation of host behavior by the parasite to promote the completion of its life cycle. Copyright 2004.
The Strepsiptera are an enigmatic group of parasitic insects whose phylogenetic relationships are hotly debated. Male Strepsiptera have very unusual compound eyes, in which each of a small number of ommatidia possesses a retina of at least 60 retinula cells. We analysed the optomotor response of Xenos vesparum males to determine whether spatial resolution in these eyes is limited by the interommatidial angle or by the higher resolution potentially provided by the extended array of retinula cells within each ommatidium. We find that the optomotor response in Strepsiptera has a typical bandpass characteristic in the temporal domain, with a temporal frequency optimum at 1-3 Hz. As a function of spatial wavelength, the optomotor response is zero at grating periods below 12 degrees and reaches its maximum strength at grating periods between 60 degrees and 70 degrees. To identify the combination of interommatidial angles and angular sensitivity functions that would generate such a spatial characteristic, we used motion detection theory to model the spatial tuning function of the strepsipteran optomotor response. We found the best correspondence between the measured response profile and theoretical prediction for an irregular array of sampling distances spaced around 9 degrees (half the estimated interommatidial angle) and an angular sensitivity function of approximately 50 degrees, which corresponds to the angular extent of the retina we estimated at the centre of curvature of the lens. Our behavioural data strongly suggest that, at least for the optomotor response, the resolution of the strepsipteran compound eye is limited by the ommatidial sampling array and not by the array of retinula cells within each ommatidium. We discuss the significance of these results in relation to the functional organisation of strepsipteran compound eyes, their evolution and the role of vision in these insects.
Male bed bugs pierce females through the body wall and inseminate directly into the body cavity. It has previously been shown that such traumatic insemination carries costs for females, and sexual conflict regarding the mode of insemination should thus propel male-female coevolution. Since males accumulate sexually antagonistic adaptations, females should evolve counter-adaptations that efficiently abate the costs to females of sexual interactions. Yet, unambiguous experimental evidence for female counter-adaptations is lacking. In bed bugs, the spermalege (a highly modified region of the abdomen where the male usually pierces the female) may represent a female counter-adaptation. We assess the female costs of traumatic insemination by varying the rate of insemination on the one hand, and the rate and mode of piercing trauma to females on the other. Our results show that female mating costs are not extreme-elevated mating rate shortened female lifespan but had no significant effect on lifetime egg production. More importantly, additional abdominal piercing in the spermalege had no effect on females whereas even a very low rate of such piercing outside the spermalege reduced female lifetime egg production by 50%. Thus, females are well counter-adapted to the intrusive mode of insemination exhibited by male bed bugs and the costs of elevated mating are comparable with those in other insects, as predicted by theory. We therefore demonstrate that the spermalege efficiently reduces the direct costs of piercing trauma to females, and hence provide experimental evidence for a female counter-adaptation to a sexually antagonistic male trait.
Nassonow's gland consists of a number of cells with ducts that open on to the ventral surface of the brood canal in the cephalothoracic region of a neotenic female strepsipteran. The structural organization of the gland is reminiscent of the class 3 of the epidermal gland cells as defined by Noirot and Quennedey [Ann. Rev. Entomol. 19 (1974) 61], which consists of secretory and duct forming cells. The ultrastructure of the Nassonow's gland is described in female Xenos vesparum (Rossi) parasitic in the social wasp Polistes dominulus Christ. The large secretory cells are clustered in groups of three to four, rich in smooth endoplasmic reticulum and produce a secretion made up of lipids. In young females, just before mating, the ultrastructure of the cells and their inclusions indicate that they are active. In old-mated females the Nassonow's gland degenerates. Microvilli line an extracellular cavity and there are pores present in the irregularly thick cuticle of the efferent duct. The small duct forming cells, intermingle with epidermal cells, overlap secretory cells and produce a long efferent duct, the cuticle of which becomes thick close to its opening in the brood canal. Nassonow's gland could be the source of a sex pheromone, which might be capable of attracting the free-living male to a permanently endoparasitic female.
Insects and arachnids display the most impressive diversity of mating and social behaviour among all animals. This book investigates sexual competition in these groups, and the variety of ways in which males and females pursue, persuade, manipulate, control and help one another, enabling us to gain a better understanding of how conflicts and confluences of interest evolve together. Each chapter provides a comprehensive review of mating systems in particular insect and arachnid groups, discusses intrinsic and extrinsic factors responsible for observed mating strategies, and suggests fruitful avenues for further research. The book culminates in a synthesis, reviewing the date in terms of the theory of sexual conflict. This broad-based book will be of immense value to students and researchers interested in reproductive strategies, behavioural ecology, entomology and arachnology.
How often, in turning over the pages of his check-list, has the American collector of beetles allowed his eyes to rest a moment upon those lines of type which announce the existence in our fauna of the mysterious family Stylopidæ, with its two genera, Stylops and Xenos ; each represented by a single species; but, recognizing in these names only the records of captures almost legendary in their antiquity, he has turned the page with a feeling that they represent to him unattainalble rarities.
Infection of the paper wasp, Polistes dominulus (Christ), by the strepsipteran parasite Xenos vesparum Rossi results in a dramatic behavioral change, which culminates in colony desertion and the formation of extranidal aggregations, in which up to 98% of occupants are parasitized females. Aggregations formed on prominent vegetation, traditional lek-sites of Polistes males, and on buildings, which were later adopted as hibernating sites by future queens. First discovered by W.D. Hamilton, these aberrant aggregations are an overlooked phenomenon of the behavioral ecology of this intensively studied wasp. For 3 months in the summer of 2000, during the peak of colony development, we sampled 91 extranidal aggregations from seven areas, numbering 1322 wasps. These wasps were parasitized by both sexes of X. vesparum, but males were more frequent from July until mid-August, during the mating season of the parasite. Aggregations were present for days at the same sites (in one case a leaf was occupied for 36 consecutive days) and were characterized by extreme inactivity. After artificial infection, parasitized "workers" deserted the nest 1 week after emergence from their cell and before the extrusion of the parasite through the host cuticle. Infected individuals did not work, were more inactive, and did not receive more aggression than did controls. We suggest that early nest desertion and subsequent aggregations by parasitized nominal workers and "future queens" is adaptive manipulation of host behavior by the parasite to promote the completion of its life cycle. Copyright 2004.
Sexual selection is the mechanism that favors an increase in the frequency of alleles associated with reproduction (Darwin, 1871). Darwin distinguished sexual selection from natural selection, but today most evolutionary scientists combine the two concepts under the name, natural selection. Sexual selection is composed of intrasexual competition (competition between members of the same sex for sexual access to members of the opposite sex) and intersexual selection (differential mate choice of members of the opposite sex). Focusing mainly on precopulatory adaptations associated with intrasexual competition and intersexual selection, postcopulatory sexual selection was largely ignored even a century after the presentation of sexual selection theory. Parker (1970) was the first to recognize that male-male competition may continue even after the initiation of copulation when males compete for fertilizations. More recently, Thornhill (1983) and others (e.g. Eberhard, 1996) recognized that intersexual selection may also continue after the initiation of copulation when a female biases paternity between two or more males' sperm. The competition between males for fertilization of a single female's ova is known as sperm competition (Parker, 1970), and the selection of sperm from two or more males by a single female is known as cryptic female choice (Eberhard, 1996; Thornhill, 1983). Although sperm competition and cryptic female choice together compose postcopulatory sexual selection (see Table 6.1), sperm competition is often used in reference to both processes (e.g. Baker & Bellis, 1995; Birkhead & Moller, 1998; Simmons, 2001; Shackelford, Pound, & Goetz, 2005).
The endoparasitic life of strepsipterans (Insecta), especially neotenic females, reduces to a great extent external and internal organs. Light and electron microscopic investigation of ovaries of Elenchus tenuicornis (Kirby) confirms the following: (1) somatic tissues of ovaries are totally reduced, with the exception of some cells surrounding germ cell clusters; (2) a previtellogenic growth phase of oocytes is reduced; (3) nurse cells remain diploid and their membranes degenerate at the onset of vitellogenesis; (4) vitellogenesis is reduced, vitellin and fat vacuoles contribute only 50% to the final egg volume; and (5) chorionogenesis is reduced to a vitellin membrane. However, some features of normal development remain, allowing classification of the ovary type as polytrophic meroistic: (1) germ cells undergo synchronized, incomplete divisions, following the 2n rule, where all former intercellular bridges become localized in one cystocyte, while the other has none; and (2) only one cell is determined as the oocyte, all other cystocytes serve as nurse cells and the surrounding somatic cells transform into follicular cells. Novel events in oogenesis of strepsipterans include fission of clusters during the phase of cluster mitoses, and protection of oocyte nuclei, while nurse cell nuclei degenerate in the same cytoplasm.
The Strepsiptera are considered to be a monophyletic order. They show plesiomorphic characters already lost in most of the other holometabolous insects and many very peculiar autapomorphies related to their specialized endoparasitism. A series of non morphological arguments supports this point of view. Clear synapomorphies to other insect orders are absent; possibly the opisthomotorism and the resulting special structure of the metendosternite may be synapomorphies of the Coleoptera. The Strepsiptera thus are considered to be a sister-group of the Coleoptera.
Previous uncertainty concerning the number of larval stages in a strepsipteran (Elenchus tenuicornis) was resolved by transmission and scanning electron microscope observations. The first larval instar (triungulinid) is free-living: after entering the host (a delphacid) it undergoes a normal ecdysis. The resulting second instar larva undergoes two further apolyses without ecdysis. In the male, the cuticle of the fourth instar larva tans to form the puparium, while the female becomes sexually mature without a further moult after extrusion of the cephalothorax through the host cuticle. The discarded exuviae of the triungulinid remain in the host abdomen; subsequent larval staging is made possible by the retention of the exuviae ensheathing the larva as each apolysis is accomplished.
I . Intrasexual seiection may have played a large part in insects in the evolution of copulation with internal fertilization from indirect spermatophore-transferring acts.
2. ‘Sperm competition’ may be defined as the competition within a single female between the sperm from two or more males over the fertilization of the ova.
3. There is considerable evidence from sperm-marking experiments that sperm competition is very common in insects as a result of multiple matings. Insects so far examined show that sperm from all inseminations can be used (to a varying extent) in the fertilization of subsequent offspring, but mating does not always result in successful insemination. In most cases (so far examined), the last male to mate tends to predominate in fertilizing the offspring.
4.Insects are preadapted to sustaining a very high level of sperm competition, compared with several other animal groups. The main preadaptations may be sum- marized as follows: (a)Females often mate several times within the duration of effec- tiveness of a given ejaculate. There may be several reasons for this. Though most usually females are unreceptive for some time after mating, some species appear ‘promiscuous’. Unreceptive females are also sometimes raped. Male persistence is sometimes prolonged, so that full female receptivity is advantageous. It is advan- tageous for a female to become receptive again when fertility first begins to decline; this is not when all the first ejaculate is used up. (b) Female insects typically possess specialized sperm storage organs in which sperm can be maintained in a viable condi- tion for a very long time, often until the death of the female. (c) Extremely efficient utilization of stored sperm at the time of fertilization appears to be an insect charac- teristic. In Drosophila the number of stored sperm virtually equals the possible number of fertilizations. Overlapping of effective ejaculates is therefore high. Second insemina- tions almost invariably reduce the fertility which would have been experienced by the first male to mate.
5. It is argued that this preadaptation to a very high level of sperm competition has led to intense intrasexual selective pressures on the male. In response to these pressures, two main lines of sexually selected adaptation are predicted: (a) towards mechanisms by which a male inseminates a female in such a way as to achieve pre- cedence over previously stored sperm and (b) accentuated by the above adaptation, mechanisms will evolve by which a male which mates with a given female will reduce the occurrence or success of subsequent inseminations with that female. These two forms of adaptation are diametrically opposed ; a high selective advantage would be gained by a male which superseded previous sperm and prevented any subsequent successful inseminations.
6. Several adaptations in male insects can be interpreted in the light of the above predictions, though many of these may also have other adaptive values through natural selection. The adaptation which evolves is not necessarily that which yields the maxi- mum possible egg gain to a given male (i.e. total sperm precedence), but that which results in the highest fertilization rate.
7. Sperm precedence is achieved in Drosophila by sperm displacement, where sperm from a second male predominate over previously stored sperm by directly displacing them from the sperm stores. Sperm displacement may occur in many insects.
8. Several behavioural and physiological adaptations of male insects may help to reduce the effectiveness, or occurrence of second inseminations of the same female by other males. These include : ( a ) Mating plugs (sphragis, spermat0phragmata)-male accessory gland secretions, usually transferred after insemination, which coagulate and form plugs within the female genital tract. Plugs may often serve to ‘guard’ the female until unreceptivity is initiated. In many insects, agents in the seminal fluid or male accessory gland secretions induce unreceptivity in the female. (b)Prolonged copu- lation-sometimes copulation takes much longer than seems necessary merely to transfer the sperm. This may have the same functions as that of a mating plug, but renders the male unfree to search for further females. (c) Passive phases (amplexus, tandem behaviour)-stages of the male’s reproductive behaviour during which he remains mounted on or otherwise attached to the female but without true genital contact between the two sexes. Postcopulatory passive phases sometimes serve to guard the female during oviposition where high densities of searching males are pre- valent. The postcopulatory passive phase of Scatophaga has an extremely high intra- sexual selective advantage which exceeds any apparent natural selective advantage by two orders of magnitude. (d)Non-contact guarding phases-reproductive behaviour phases during which the male remains close but not in contact with the female, guard- ing her from other males. Postcopulatory non-contact guarding phases appear to have the same selective advantage as postcopulatory passive phases.
9. Mechanisms to avoid ‘take-over ’ during copulation, passive, and non-contact guarding phases also serve to reduce sperm competition. These include increased efficiency of grasping apparatus, specialized rejection reactions which serve to dispel or ‘trick’ the recognition mechanism of the attacker, and emigrations from the site of highest probability of ‘take-over ’. There is quantitative evidence in Scatophaga that the emigration threshold of copulating males is determined by this form of intrasexual selective pressure.
10.Precopulatory passive phases may serve mainly to keep the sexes together until the female becomes receptive, but share several features in common with postcopula- tory passive phases. Territoriality of male insects may have arisen primarily through sexual selection as a mechanism by which a male guards an area into which a female is most likely to enter.
The accessory functions subserved by the seminal fluid have long been of interest, and much is now known about the activation of the spermatozoa and the formation of spermatophores and various kinds of vaginal and bursal plugs such as spermatophragma. During the last few years, it has become clear that by means of peptides and other substances in the seminal fluid, the males of a number of species of insects control the physiology of mated females in several important ways, and recent work on this subject is briefly summarized.
In Saccharomyces cerevisiae, the HMR-E silencer blocks site-specific interactions between proteins and their recognition sequences
in the vicinity of the silencer. Silencer function is correlated with the firing of an origin of replication at HMR-E. An
essential gene with a role in transcriptional silencing was identified by means of a screen for mutations affecting expression
of HMR. This gene, known as ORC2, was shown to encode a component of the origin recognition complex that binds yeast origins
of replication. A temperature-sensitive mutation in ORC2 disrupted silencing in cells grown at the permissive temperature.
At the restrictive temperature, the orc2-1 mutation caused cell cycle arrest at a point in the cell cycle indicative of blocks
in DNA replication. The orc2-1 mutation also resulted in the enhanced mitotic loss of a plasmid, suggestive of a defect in
replication. These results provide strong evidence for an in vivo role of ORC in both chromosomal replication and silencing,
and provide a link between the mechanism of silencing and DNA replication.
Because the costs and benefits of polygamy differ for males and females, copulation is not always a cooperative venture between the sexes. Sperm competition can build on this asymmetry, producing male traits that harm females thereby generating coevolutionary arms races between the sexes. We have found that the male genitalia of the bean weevil Callosobruchus maculatus damage the female genitalia, and that females act to reduce the extent of this damage. We propose that these functionally diametric sexual traits form the basis of reproductive conflict.
Recent studies suggest that insects use pattern recognition molecules to distinguish prokaryotic pathogens and fungi from "self" structures. Less understood is how the innate immune system of insects recognizes endoparasitic Hymenoptera and other eukaryotic invaders as foreign. Here we discuss candidate recognition factors and the strategies used by parasitoids to overcome host defense responses. We suggest that host-parasitoid systems are important experimental models for studying how the innate immune system of insects recognizes foreign invaders that are phylogenetically more closely related to their hosts. The strategies used by parasitoids suggest that insects may employ "hidden-self" recognition molecules for attacking foreign objects intruding the open circulatory system. BioEssays 23:344-351, 2001.
The systematic position of insect order Strepsiptera is still under debate. It was, therefore, thought of interest to examine the ultrastructure of a strepsipteran in a search for synapomorphies shared with Coleoptera, Diptera, or any other insect order. The fine structure of spermatozoa and the spermatid from Xenos vesparum (Rossi) was re-examined using scanning and transmission electron microscopy and a fixation technique that permits the visualization of the macromolecular organization of the organelles. The spermatozoon was shown to possess several traits that are characteristics of insects in general, such as a 9 + 9 + 2 axoneme, two mitochondrial derivatives containing a crystalline material and two 'zipper lines' present along the sperm tail. Seventeen protofilaments occurred along most of the accessory tubules, which reduced to 16 posteriorly. An acrosome is absent. The neck region contains a prominent centriolar adjunct, which gives rise to two accessory bodies which adhere to the mitochondrial derivatives, and to slender strands of the so-called intertubular material found between the accessory tubules. Of interest is the finding that the glycocalyx consists of prominent filamentous strands, similar to those found in siphonapterans, mecopterans and basal dipterans.
Insects. Their sper-matozoa and phylogeny. Oxford: IBH. Kathirithamby J. 1989. Review of the order Strepsiptera
- Jamieson Bgm
- R Dallai
- Ba
Jamieson BGM, Dallai R, Afzelius BA. 1999. Insects. Their sper-matozoa and phylogeny. Oxford: IBH. Kathirithamby J. 1989. Review of the order Strepsiptera. Syst Entomol 14:41–92.
Sperm competition and its evolutionary con-sequences in the insects Studies in the experimental anal-ysis of the sex. Part 11. On Stylops and stylopisation
- Lw Simmons
Simmons LW. 2001. Sperm competition and its evolutionary con-sequences in the insects. Princeton, NJ: Princeton University Press. Smith MAG, Hamm AH. 1914. Studies in the experimental anal-ysis of the sex. Part 11. On Stylops and stylopisation. Q J Microsc Sci 60:435– 461.
Sperm ultrastructure of Xenos vesparum (Rossi) and its significance in the taxonomy and phylogeny of Strepsiptera
- M Carcupino
- G Profili
- J Kathirithamby
- M Mazzini
Carcupino M, Profili G, Kathirithamby J, Mazzini M. 1995.
Sperm ultrastructure of Xenos vesparum (Rossi) and its significance in the taxonomy and phylogeny of Strepsiptera (Insecta).