Twisted-wing Parasite Research Articles

Collection methods and distribution modeling for Strepsiptera in the United States.

The twisted-wing parasite order (Strepsiptera Kirby, 1813) is difficult to study due to the complexity of strepsipteran life histories, small body sizes, and a lack of accessible distribution data for most species. Here, we present a review of the strepsipteran species known from New York State. We also demonstrate successful collection methods and a survey of species carried out in an old-growth deciduous forest dominated by native New York species (Black Rock Forest, Cornwall, NY) and a private site in the Catskill Mountains (Shandaken, NY). Additionally, we model suitable habitats for Strepsiptera in the United States with species distribution modeling. We base our models on host distribution and climatic variables to inform predictions of where these twisted-wing parasites are likely to be found. This work provides a useful reference for the future collection of Strepsiptera.

Have female twisted-wing parasites (Insecta: Strepsiptera) evolved tolerance traits as response to traumatic penetration?

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.

Xenosyangi sp. nov.: A new twisted-wing parasite species (Strepsiptera, Xenidae) from Gaoligong Mountains, Southwest China.

Here we report a new twisted-wing parasite species of the family Xenidae based on both morphological and molecular evidence. By using nearly complete mitogenomes, we confirmed the twisted-wing parasites on two wasps (Vespavelutina and Vespabicolor) (China: Yunnan) as the same species, and associated its neotenic females and alate males. Combining the mitogenomic data (COI) and morphological traits, this species was identified to be a new species of the genus Xenos, namely Xenosyangi Dong, Liu & Li, sp. nov. Detailed descriptions and illustrations are provided for the new species.

The mitochondrial genome of one ‘twisted-wing parasite’ Xenos cf. moutoni (Insecta, Strepsiptera, Xenidae) from Gaoligong Mountains, Southwest of China

The nearly complete mitochondrial genome (mitogenome) of Xenos cf. moutoni, one twisted-wing parasite on wasp Vespa velutina from Southwest of China, is described in this study. The total length of this mitogenome is 16,717 bp, containing 13 protein-coding genes (PCGs), 22 transfer RNA genes (tRNAs), two ribosomal RNA genes (rRNAs) and an incomplete A + T-rich control region . All of the 13 PCGs are initiated with canonical ATN (N represents A, T, G, C) as start codons; 8 PCGs are terminated with a complete typical stop codon TAA, and the remaining five PCGs (cox2, cox3, nad3, nad4 and nad5) have an incomplete stop codon with just a T. The phylogenetic analysis based on the nucleotide sequences of PCGs and rRNAs indicates that Xenos cf. moutoni has a close relationship with Xenos vesparum, confirming its placement in the family Xenidae.

Twisted-wing parasites equipped for colour vision

![Figure][1] Close-up of the eyes of a male Xenos peckii . Photo credit: Elke Buschbeck and Necati Kaval. When Xenos peckii twisted-wing parasite males emerge as adults from within the body of the hapless wasp that served as their incubator, the race is on. With an adult lifetime spanning

A new twisted-wing parasitoid from mid-Cretaceous amber of Myanmar (Strepsiptera)

A second Mesozoic twisted-wing parasite (Strepsiptera) is described and figured based on an exceptionally well-preserved male in mid-Cretaceous (Cenomanian) amber from northern Myanmar. Phthanoxenos nervosus Engel and Huang, gen. et sp. nov., is distinguished from other strepsipteran lineages, particularly the contemporaneous Cretostylops engeli Grimaldi and Kathirithamby, also in Burmese amber, and Protoxenos janzeni Pohl et al. in mid-Eocene Baltic amber, and assigned to a new family, Phthanoxenidae Engel and Huang, fam. nov. Phthanoxenos exhibit features indicative of a more primitive phylogenetic position than Cretostylopidae but still more derived than Protoxenidae. Brief remarks are made on the geological history of the Strepsiptera.

Repeated horizontal transfers of four DNA transposons in invertebrates and bats

BackgroundHorizontal transfer (HT) of transposable elements (TEs) into a new genome is considered as an important force to drive genome variation and biological innovation. However, most of the HT of DNA transposons previously described occurred between closely related species or insects.ResultsIn this study, we carried out a detailed analysis of four DNA transposons, which were found in the first sequenced twisted-wing parasite, Mengenilla moldrzyki. Through the homology-based strategy, these transposons were also identified in other insects, freshwater planarian, hydrozoans, and bats. The phylogenetic distribution of these transposons was discontinuous, and they showed extremely high sequence identities (>87%) over their entire length in spite of their hosts diverging more than 300 million years ago (Mya). Additionally, phylogenies and comparisons of transposons versus orthologous gene identities demonstrated that these transposons have transferred into their hosts by independent HTs.ConclusionsHere, we provided the first documented example of HT of CACTA transposons, which have been so far extensively studied in plants. Our results demonstrated that bats had continuously acquired new DNA elements via HT. This implies that predation on a large quantity of insects might increase bat exposure to HT. In addition, parasite-host interaction might facilitate exchanging of their genetic materials.Electronic supplementary materialThe online version of this article (doi:10.1186/s13100-014-0033-1) contains supplementary material, which is available to authorized users.

Discovery of the twisted-wing parasite family Myrmecolacidae (Insecta: Strepsiptera) from China, with description of two new species of the genus Myrmecolax Westwood, 1861

The twisted-wing parasite family Myrmecolacidae is recorded from China for the first time based on the discovery of the genus Myrmecolax Saunders. Two species of Myrmecolax are described as new to science, Myrmecolax pachygnathus sp. nov. and Myrmecolax arcuatus sp. nov..

The Origin and Evolution of Six Miniature Inverted-Repeat Transposable Elements in Bombyx mori and Rhodnius prolixus

Miniature inverted-repeat transposable elements (MITEs) are a specific group of nonautonomous DNA transposons, and they are distributed in a wide range of hosts. However, the origin and evolutionary history of MITEs in eukaryotic genomes remain unclear. In this study, six MITEs were identified in the silkworm (Bombyx mori). Five elements are grouped into four known superfamilies of DNA transposons, and one represents a novel class of MITEs. Unexpectedly, six similar MITEs are also present in the triatomine bug (Rhodnius prolixus) that diverged from the common ancestor with the silkworm about 370 Ma. However, they show different lengths in two species, suggesting that they are different derivatives of progenitor transposons. Three direct progenitor transposons (Sola1, hobo/Ac/Tam [hAT], and Ginger2) are also identified in some other organisms, and several lines of evidence suggested that these autonomous elements might have been independently and horizontally transferred into their hosts. Furthermore, it is speculated that the twisted-wing parasites may be the candidate vectors for these horizontal transfers. The data presented in this study provide some new insights into the origin and evolutionary history of MITEs in the silkworm and triatomine bug.

Total Synthesis, Proof of Absolute Configuration, and Biosynthetic Origin of Stylopsal, the First Isolated Sex Pheromone of Strepsiptera

The asymmetric total synthesis of the diastereomers of stylopsal establishes the absolute configuration of the first reported sex pheromone of the twisted-wing parasite Stylops muelleri as (3R,5R,9R)-trimethyldodecanal. The key steps for the diastereo- and enantiodivergent introduction of the methyl groups are two different types of asymmetric conjugate addition reactions of organocopper reagents to α,β-unsaturated esters, whereas the dodecanal skeleton is assembled by Wittig reactions. The structure of the natural product was confirmed by chiral gas chromatography (GC) techniques, GC/MS and GC/electroantennography (EAD) as well as field tests. An investigation into the biosynthesis of the pheromone revealed that it is likely to be produced by decarboxylation of a 4,6,10-trimethyltridecanoic acid derivative, which was found in substantial amounts in the fat body of the female, but not in the host bee Andrena vaga. This triple-branched fatty acid precursor thus seems to be biosynthesized de novo through a polyketide pathway with two consecutive propionate-propionate-acetate assemblies to form the complete skeleton. The simplified, motionless and fully host-dependent female exploits a remarkable strategy to maximize its reproductive success by employing a relatively complex and potent sex pheromone.

First Sex Pheromone of the Order Strepsiptera: (3R,5R,9R)-3,5,9-Trimethyldodecanal in Stylops melittae Kirby, 1802

The twisted-wing parasites (Strepsiptera) are an unusual and small order of insects with about 600 known species. As obligate endoparasitoids, they develop and spend most of their lives living in other insects. Adults show an extreme sexual dimorphism: The free-living males have large eyes, branched antennae, reduced forewings, and well developed hind wings, while the neotenic females of most species lack all external characters that normally define an insect, remain endoparasitic, and only extrude the cephalothorax from the host. Due to the males' short life span of only a few hours, there must be an efficient means of mate finding. This is believed to be mediated by chemical cues released by virgin females. Here, we report the first identification and synthesis of a female-produced strepsipteran sex pheromone, (3R,5R,9R)-3,5,9-trimethyldodecanal, from Stylops melittae, a species parasitizing andrenid bees. We found this highly EAD-active compound to be present in cephalothoraxes of and released from unmated females, and synthetic samples proved to be extremely attractive when offered in the field during the swarming period of the males. The structural features of this new natural compound may further support the re-establishment of the Strepsiptera as the closest living relatives of the Coleoptera.

Erratum to: Stylopsal: The first Identified Female-produced Sex Pheromone of Strepsiptera

The following reference and statement were inadvertently omitted from this paper during processing. The Editors regret the error. “TOLASCH, T., Kehl, S., and Dotterl, S. 2010. Sex pheromone of a twisted-wing parasite. Poster at the ISCE 2010 Meeting in Tours, France (p. 176 in the book of abstracts).” “Independently of our work, and roughly at the same time, other researchers were working on the structure of the Stylops pheromone. The ultimate outcome of this work also is being published in this issue. Tolasch et. al. (this issue).”

Genomic and Morphological Evidence Converge to Resolve the Enigma of Strepsiptera

The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention. However, the evolutionary roots of one intriguing group of insects, the twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate. Strepsiptera exhibit exceptional larval developmental features, consistent with a predicted step from direct (hemimetabolous) larval development to complete metamorphosis that could have set the stage for the spectacular radiation of metamorphic (holometabolous) insects. Here we report the sequencing of a Strepsiptera genome and show that the analysis of sequence-based genomic data (comprising more than 18 million nucleotides from nearly 4,500 genes obtained from a total of 13 insect genomes), along with genomic metacharacters, clarifies the phylogenetic origin of Strepsiptera and sheds light on the evolution of holometabolous insect development. Our results provide overwhelming support for Strepsiptera as the closest living relatives of beetles (Coleoptera). They demonstrate that the larval developmental features of Strepsiptera, reminiscent of those of hemimetabolous insects, are the result of convergence. Our analyses solve the long-standing enigma of the evolutionary roots of Strepsiptera and reveal that the holometabolous mode of insect development is more malleable than previously thought.

The strepsipteran parasite Elenchus japonicus (Strepsiptera, Elenchidae) of planthoppers consists of three genotypes

The twisted-wing parasite Elenchus japonicus is a major parasitoid of rice planthoppers (Hemiptera: Delphacidae), including the brown planthopper Nilaparvata lugens, the white-backed planthopper Sogatella furcifera, and the small brown planthopper Laodelphax striatellus. Another Elenchus species, E. yasumatsui, which is considered to be synonymous with E. japonicus, has also been described in southern Asia. However, limited biological and molecular data on this important parasitoid of rice planthoppers are available. In this study, E. japonicas-stylopized planthoppers were obtained from various regions in Asia and Japan. Sequences of the nuclear 18S ribosomal RNA gene and the mitochondrial cytochrome oxidase I gene of the strepsipterans were analyzed from 40 samples of E. japonicus: 14 from N. lugens, 6 from S. furcifera and 20 from L. striatellus. Sequence analysis of these samples revealed three genotypes of E. japonicus. Of the three types of E. japonicus, one was isolated only from L. striatellus from northern Japan. The other two types were found in all three rice planthopper species collected from a wide area in Asia. These results suggest that the three different genotypes of Elenchus can be associated with a particular geographical region and/or planthopper species. The relationship between two previously described Elenchus species and the present three genotypes needs to be elucidated.

Assessing the odd secondary structural properties of nuclear small subunit ribosomal RNA sequences (18S) of the twisted‐wing parasites (Insecta: Strepsiptera)

We report the entire sequence (2864 nts) and secondary structure of the nuclear small subunit ribosomal RNA (SSU rRNA) gene (18S) from the twisted-wing parasite Caenocholax fenyesi texensis Kathirithamby & Johnston (Strepsiptera: Myrmecolacidae). The majority of the base pairings in this structural model map on to the SSU rRNA secondary and tertiary helices that were previously predicted with comparative analysis. These regions of the core rRNA were unambiguously aligned across all Arthropoda. In contrast, many of the variable regions, as previously characterized in other insect taxa, had very large insertions in C. f. texensis. The helical base pairs in these regions were predicted with a comparative analysis of a multiple sequence alignment (that contains C. f. texensis and 174 published arthropod 18S rRNA sequences, including eleven strepsipterans) and thermodynamic-based algorithms. Analysis of our structural alignment revealed four unusual insertions in the core rRNA structure that are unique to animal 18S rRNA and in general agreement with previously proposed insertion sites for strepsipterans. One curious result is the presence of a large insertion within a hairpin loop of a highly conserved pseudoknot helix in variable region 4. Despite the extraordinary variability in sequence length and composition, this insertion contains the conserved sequences 5'-AUUGGCUUAAA-3' and 5'-GAC-3' that immediately flank a putative helix at the 5'- and 3'-ends, respectively. The longer sequence has the potential to form a nine base pair helix with a sequence in the variable region 2, consistent with a recent study proposing this tertiary interaction. Our analysis of a larger set of arthropod 18S rRNA sequences has revealed possible errors in some of the previously published strepsipteran 18S rRNA sequences. Thus we find no support for the previously recovered heterogeneity in the 18S molecules of strepsipterans. Our findings lend insight to the evolution of RNA structure and function and the impact large insertions pose on genome size. We also provide a novel alignment template that will improve the phylogenetic placement of the Strepsiptera among other insect taxa.