Description of a new genus and two new species of Corioxenidae from Jordan (Insecta: Strepsiptera)

Abstract

Two new species of twisted-wing insects (Strepsiptera) of the family Corioxenidae, Proceroxenos jordanicus n.gen., n.sp., and Dundoxenos breviphlebos n.sp., are described from Jordan. Identification keys to the subfamilies of the Corioxenidae, the genera of the subfamily Uniclavinae, and the species of the genus Dundoxenos are provided. A list of all described species of Corioxenidae is given, including information on geographic distribution, and host species when available.     

Mating of Xenos vesparum (Rossi) (Strepsiptera, Insecta) revisited

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.     

Reductions and new inventions dominate oogenesis of Strepsiptera (Insecta)

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.     

We do not select,nor are we choosy: reproductive biology of Strepsiptera (Insecta)

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.     

The first molecular phylogeny of Strepsiptera (Insecta) reveals an early burst of molecular evolution correlated with the transition to endoparasitism

A comprehensive model of evolution requires an understanding of the relationship between selection at the molecular and phenotypic level. We investigate this in Strepsiptera, an order of endoparasitic insects whose evolutionary biology is poorly studied. We present the first molecular phylogeny of Strepsiptera, and use this as a framework to investigate the association between parasitism and molecular evolution. We find evidence of a significant burst in the rate of molecular evolution in the early history of Strepsiptera. The evolution of morphological traits linked to parasitism is significantly correlated with the pattern in molecular rate. The correlated burst in genotypic-phenotypic evolution precedes the main phase of strepsipteran diversification, which is characterised by the return to a low and even molecular rate, and a period of relative morphological stability. These findings suggest that the transition to endoparasitism led to relaxation of selective constraint in the strepsipteran genome. Our results indicate that a parasitic lifestyle can affect the rate of molecular evolution, although other causal life-history traits correlated with parasitism may also play an important role.     

New findings on sperm ultrastructure of Xenos vesparum (Rossi) (Strepsiptera,Insecta)

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.     

Zum Feinbau des Komplexauges von Stylops spec. (Insecta,Strepsiptera)

Zusammenfassung Unter den Cornealinsen des Komplexauges von Stylops befindet sich ein Kristallkegel vom pseudoconen Typ, der von zahlreichen Pigmentzellen umhüllt wird. An seinem proximalen Ende liegen 6 meist pigmentfreie Zellen (Sempersche Zellen).Das Ommatidium besteht aus etwa 60 Retinulazellen. Ihre distal kranzartig miteinander verbundenen Mikrovillisäume bilden ein einziges offenes Rhabdom, das extrazelluläres (?) granuläres Material und die Basis der Semperschen Zellen umgibt. Stellenweise wird das Rhabdom samt granulärem Material von homogen erscheinenden distalen Ausläufern einzelner Retinulazellen überlagert. Proximad zerfällt das Rhabdom zunehmend in kleinere Rhabdomteile. Im zentralen Teil des Ommatidiums liegen 1–2 auffallend große Retinulazellen, die meist weniger elektronendicht erscheinen und kleinere Pigmentgrana haben.Die einzelnen Ommatidien werden von ungemein zahlreichen, sehr pigmentarmen Stützzellen umhüllt. Diese werden — wie die basalen Teile der Retinulazellen — teilweise durch Gliazellfortsätze isoliert.Bei Stylops, einem Vertreter der Strepsipteren, handelt es sich nicht um ocelläre Komplexaugen (Strohm, 1910), auch nicht um eucone Ommatidien (Kinzelbach, 1967), sondern um Ommatidien vom pseudoconen Typ. Zumindest der Bau des Rhabdoms ähnelt dem des Larvenauges (Stemma), dessen rezeptorischer Teil entgegen den Annahmen früherer Autoren in der Imago nicht reduziert wird.

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On the fine structure of the compound eye of Stylops spec. (Insecta, Strepsiptera)

Summary In the compound eye of Stylops a crystalline cone of the pseudocone type is found beneath the corneal lens. It is enveloped by several pigment cells. At the proximal part of the cone there are 6 cells (Semper cells) mostly pigment-free.The ommatidium consists of approximately 60 retinula cells. Their rhabdomeres distally rim-like connected to another form a single open rhabdom which encircles extracellular granular material as well as the bases of the Semper cells. Here and there the rhabdom plus granular material is overlain with distal protrusions of single retinula cells which appear to be homogeneous. Towards the proximal part the rhabdom increasingly divides up into smaller rhabdomal segments. One or two conspicuous large retinula cells were found in the central part of the ommatidium, appearing to be less electron-dense and containing pigment granules of a smaller size. Each ommatidium is surrounded by numerous cells (Stützzellen) lacking in pigment. These cells are partially insulated from another—as well as the basal parts of retinula cells—by protrusions of glia cells.Our investigations show that the eyes of Stylops (as a representative of Strepsiptera) are not of the ocellar complex eye type. At least the structure of the rhabdom resembles to that of the larval eye (stemma), the receptor part of which is not reduced in the imago.

Herrn Prof. Dr. Helmcke danke ich für die freundliche Unterstützung am Raster-Elektronenmikroskop.     

The mitochondrial genome of the entomophagous endoparasite Xenos vesparum (Insecta: Strepsiptera)

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.     

†Kinzelbachilla ellenbergeri – a new ancestral species,genus and family of Strepsiptera (Insecta)

A single male specimen of a new species (†Kinzelbachilla ellenbergeri gen. et sp.n. ) of a new family of the endoparasitic Strepsiptera (†Kinzelbachillidae fam.n.) from Burmese amber is described and evaluated with respect to its systematic placement. Its features come very close to the presumptive groundplan of the order suggested in recent studies. Preserved plesiomorphic features are the following: fully sclerotized head with long coronal suture, small ommatidia not separated by chitinous bridges, absence of microtrichia between ommatidia, eight antennomeres, robust mandibles with dicondylic articulation, galea distinctly developed, free pro‐ and mesotrochanters, slender five‐segmented tarsi without adhesive soles, and equally sclerotized abdominal tergites and sternites. An important character that is not recognizable due to damage is the shape of the metapostnotum. This structure is transverse in the groundplan of Strepsiptera and in †Protoxenos, but elongated and shield‐like in all other known strepsipterans. In a cladistic analyses of 82 characters of adult males and additional characters for females and immatures (scored as unknown for all included fossils) †Kinzelbachilla is placed as sister group of all remaining strepsipterans except for †Protoxenos, followed by †Cretostylops and †Mengea as the third and fourth branches in the stem group, respectively. The position of †Protoxenos as first branch is suggested by three unambiguous apomorphic features of all remaining Strepsiptera, the reduced size of less than 6 mm, mandibles distinctly narrowing distad the basalmost part, and fan‐shaped hindwings which are broader than they are long. The hitherto known fossil stem group strepsipterans do not distinctly narrow the large morphological gap separating this order from its sister group, the Coleoptera. This published work has been registered in ZooBank, http://zoobank.org/urn:lsid:zoobank.org:pub:07554C01-DEC3-4080-A337-B1F46BC9070F .     

A case of mistaken identification of an amber fossil male strepsipteran (Insecta: Strepsiptera)

A well-preserved specimen of amber Strepsiptera was erroneously described as Stylops neotropicallis Kogan and Poinar, 2010. The taxonomic position of the species was based on a count of six antennomeres (typical of the Stylopidae); however, further observations showed that there are actually seven antennomeres, which places the fossil in the family Myrmecolacidae, and it is herein redescribed in the genus Palaeomyrmecolax Kulicka, 2001. Furthermore, nuclear magnetic resonance spectroscopy analysis of a sample of the amber piece containing the fossil revealed that it was Baltic rather than Dominican amber as originally thought. The fossil was compared with another specimen from Baltic amber in the Poinar collection, which shows close affinity to Palaeomyrmecolax succineus Kulicka, 2001, the type species of the genus. Palaeomyrmecolax neotropicallis (n.comb.) differs from that specimen and seems to differ also from the other four species in the genus Palaeomyrmecolax.     

Fine structure of the Nassonow's gland in the neotenic endoparasitic of female Xenos vesparum (Rossi) (Strepsiptera, Insecta)

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.     

Host specialization and species diversity in the genus Stylops (Strepsiptera: Stylopidae), revealed by molecular phylogenetic analysis

Host specialization is an important ecological characteristic of parasitic species. The identification of the parasitic strategy of the genus Stylops (Strepsiptera; Stylopidae) is, however, ambiguous. According to the number of recognized species based on existing taxonomy, highly specialized and supergeneralistic species exist in this genus. Our research aims to clarify the concept of host specialization in the genus Stylops, in which all of the members are parasites of Andrena bees. Based on the phylogenetic analysis of the parasites (mostly females) and the mapping of hosts onto the phylogenetic tree, we tested three hypotheses of host specialization: (1) each species of the genus Stylops is associated with a single host species; (2) Stylops species are specialized to a group of closely related hosts; and (3) a single Stylops species is a generalist, parasitizing all host Andrena species in this particular region. Our evidence clearly shows a close relationship between the parasite and the host: one species of Stylops attacks one or a few host species of Andrena bees, usually from a single subgenus. Moreover, a moderate generalistic strategy is also likely in a few Stylops species. According to our results, the species diversity of the strepsipteran parasites of bees must be reconsidered. A single European species of Stylops should be divided into a higher number of valid species. © 2015 The Linnean Society of London     

A molecular phylogeny of the Odonata (Insecta)

Abstract. We estimated the phylogeny of the order Odonata, based on sequences of the nuclear ribosomal genes 5.8 S, 18S, and ITS1 and 2. An 18S‐only analysis resolved deep relationships well: the order Odonata, as well as suborders Zygoptera and Epiprocta (Anisoptera + Epiophlebia), emerged as monophyletic. Some other deep clades resolved well, but support for more recently diverged clades was generally weak. A second, simultaneous, analysis of the 5.8S and 18S genes with the intergenic spacers ITS1 and 2 resolved some recent branches better, but appeared less reliable for deep clades with, for example, suborder Anisoptera emerging as paraphyletic and Epiophlebia superstes recovered as an Anisopteran, embedded within aeshnoid‐like anisopterans and sister to the cordulegastrids. Most existing family levels in the Anisoptera were confirmed as monophyletic clades in both analyses. However, within the corduliids that form a major monophyletic clade with the Libellulidae, several subclades were recovered, of which at least Macromiidae and Oxygastridae are accepted at the family level. In the Zygoptera, the situation is complex. The lestid‐like family groups (here called Lestomorpha) emerged as sister taxon to all other zygopterans, with Hemiphlebia sister to all other lestomorphs. Platystictidae formed a second monophylum, subordinated to lestomorphs. At the next level, some traditional clades were confirmed, but the tropical families Megapodagrionidae and Amphipterygidae were recovered as strongly polyphyletic, and tended to nest within the clade Caloptera, rendering it polyphyletic. Platycnemididae were also non‐monophyletic, with several representatives of uncertain placement. Coenagrionids were diphyletic. True Platycnemididae and non‐American Protoneurids are closely related, but their relationship to the other zygopterans remains obscure and needs more study. New World protoneurids appeared relatively unrelated to old world + Australian protoneurids. Several recent taxonomic changes at the genus level, based on morphology, were confirmed, but other morphology‐based taxonomies have misclassified taxa considered currently as Megapodagrionidae, Platycnemididae and Amphipterygidae and have underestimated the number of family‐level clades.     

The phylogeny of Strepsiptera (Hexapoda)

Previous phylogenetic analyses of Strepsiptera have been limited to characters from only males or first instar larvae, and by poor taxonomic sampling. This investigation is the first cladistic analysis to use more than fourfold as many characters as any prior study, and a broader sampling of taxa. The analysis of 189 morphological characters of all stages of representatives of all extant strepsipteran families and characters of adult males of amber fossils results in the following branching pattern: (?Protoxenos+ (?Cretostylops + (?Mengea + (Mengenillidae + (Corioxenidae + (Bohartillidae + (Halictophagidae + (Elenchidae + (?Protelencholax + (Myrmecolacidae + (Callipharixenidae + (Xenidae + Stylopidae)))))))))))). The basal placement of the Baltic amber fossil ?Protoxenos and the Burmese amber fossil ?Cretostylops is well founded. Even though ?Cretostylops is older than ?Protoxenos it is almost certainly not the most basal strepsipteran group but the sister group of a clade comprising the Baltic amber fossil ?Mengea + Strepsiptera s. str. (excl. stemlineage). Monophyly of Mengenillidae, Stylopidia, Stylopiformia s.l., Corioxenidae, Xenidae, and Stylopidae is confirmed. Mengenillidia is paraphyletic (with respect to ?Mengea (Mengeidae)), Elenchidae (with respect to ?Protelencholax) and the genus Stichotrema (with respect to the Baltic amber fossils). Thus Protelencholacidae fam. n. is described, and S. weitschati and S. triangulum are transferred to Palaeomyrmecolax. A ground plan of adult male Strepsiptera is provided and evolutionary interpretations are presented based on the obtained cladograms. © The Willi Hennig Society 2005.     

Protoxenidae fam. nov. (Insecta, Strepsiptera) from Baltic amber — a 'missing link' in strepsipteran phylogeny

A male specimen of a new strepsipteran genus and species ( Protoxenos janzeni gen. et sp. nov.) and family (Protoxenidae fam. nov.) found in Baltic amber is described and illustrated. It shows features which are apparently more plesiomorphic than in hitherto known strepsipterans, such as laterally inserted eight-segmented antennae, very robust mandibles with a broad base, a prominent galea, a comparatively short, transverse metapostnotum, hindwings that are feebly extended in a rostrocaudal direction, and equally sclerotized abdominal tergites and sternites. Based on a cladistic analysis of 46 characters of males of 11 genera and three outgroup taxa, P. janzeni is the sister group of all other known strepsipterans, and Mengea the sister group of Strepsiptera s.s . Eoxenos is the sister group of the remaining extant strepsipterans and Mengenillidae is therefore paraphyletic. Newly established groundplan features of Strepsiptera will facilitate the clarification of the systematic position of the Order in future studies.     

Testis morphology and spermatogenesis in two species of Elenchus (Strepsiptera : Elenchidae)

Testes ultrastructure and spermatogenesis were studied in two species of Strepsiptera (Insecta), namely, Elenchus tenuicornis and E. japonicus, using light and electron microscopy. In both species, the testis is paired and consists of several large irregularly shaped follicles. Each follicle consists of a single clone of germ cells surrounded by a thin epithelium. During the larval and pupal stages, all the germ cells of each testis develop synchronously, and at eclosion, the gonads contain solely mature sperm. One of the most interesting findings is the morphogenesis of a large nuclear vesicle bounded by the fenestrate part of the nuclear envelope. This vesicle contains an electron-dense spherical structure, the chromatoid body. At the end of spermiogenesis, both the nuclear vesicle and its chromatoid body are eliminated with the excess cytoplasm. Large drops of residual cytoplasm containing several nuclear vesicles are present in the lumen of the testis and inside the cytoplasm of phagocytic cells.     

The evolution of Strepsiptera (Hexapoda)

An evolutionary scenario for the enigmatic group Strepsiptera is provided, based on the results of a comprehensive cladistic analysis of characters of all life stages. A recently described fossil--+Protoxenos janzeni--the most archaic strepsipteran, sheds new light on the early evolution of the group and reduces the "morphological gap" between Strepsiptera and other insects. It weakens both current hypotheses--Coleoptera+Strepsiptera and Diptera+Strepsiptera (="Halteria"). The splitting into +Protoxenos (Protoxenidae) and the remaining Strepsiptera was linked with a distinct size reduction and many morphological changes. Unlike males of extant strepsipteran species, +Protoxenos was still able to process food. Mengeidae (+Mengea), with two small species, is the sister group of extant Strepsiptera. A unique characteristic of extant males (Strepsiptera s. str.) is the mouthfield sclerite. It is part of an air uptake apparatus which belongs to an extremely modified air-filled "balloon gut". Besides this, male strepsipterans possess specialised antennae and compound eyes, a strongly developed flight apparatus, large testes, and a sperm pump, whereas other organ systems are strongly reduced (e.g., fat body, malpighian tubules). Males are designed to find females within a few hours and to copulate. A dramatic change is linked with the split into Mengenillidae and Stylopidia. The change to pterygote hosts and the permanent endoparasitism of the females are evolutionary novelties acquired by the latter clade, and linked with far-reaching morphological transformations, e.g. the presence of unique brood organs. Hairy tarsal adhesive devices are present in males and guarantee efficient attachment to the host during copulation. A well-founded clade within Stylopidia is Stylopiformia, which are characterised by a unique fissure-shaped birth opening. The evolutionary development towards the most specialised and successful forms (parasites of aculeate Hymenoptera [e.g., Xenidae+Stylopidae], ca. 46% of the species) is a stepwise process. The presented evolutionary scenario comprises a complex network of functionally correlated morphological changes in primary larvae, secondary larvae, females and males.