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comparisons of the embryonic development of drosophila, nasonia, and tribolium.studying the embryogenesis of diverse insect species is crucial to understanding insect evolution. here, we review current advances in understanding the development of two emerging model organisms: the wasp nasonia vitripennis and the beetle tribolium castaneum in comparison with the well-studied fruit fly drosophila melanogaster. although nasonia represents the most basally branching order of holometabolous insects, it employs a derived long germband mode of embryogenesis, more like that of dro ...201723801665
does pupal communication influence wolbachia-mediated cytoplasmic incompatibility?wolbachia are widespread endosymbiotic bacteria found in terrestrial arthropods and filarial nematodes [1]. in insects, wolbachia generally rely on diverse strategies to manipulate their host's reproduction and favor their own vertical transmission through infected eggs [2]. one such mechanism is a sterility syndrome called 'cytoplasmic incompatibility'. cytoplasmic incompatibility occurs at fertilization, when a spermatozoon from a wolbachia-infected male fertilizes an uninfected egg. in this c ...201728118585
the venom gland transcriptome of the parasitoid wasp nasonia vitripennis highlights the importance of novel genes in venom function.prior to egg laying the parasitoid wasp nasonia vitripennis envenomates its pupal host with a complex mixture of venom peptides. this venom induces several dramatic changes in the host, including developmental arrest, immunosuppression, and altered metabolism. the diverse and potent bioactivity of n. vitripennis venom provides opportunities for the development of novel acting pharmaceuticals based on these molecules. however, currently very little is known about the specific functions of individ ...201627503142
comparative genomics of two closely related wolbachia with different reproductive effects on hosts.wolbachia pipientis are obligate intracellular bacteria commonly found in many arthropods. they can induce various reproductive alterations in hosts, including cytoplasmic incompatibility, male-killing, feminization, and parthenogenetic development, and can provide host protection against some viruses and other pathogens. wolbachia differ from many other primary endosymbionts in arthropods because they undergo frequent horizontal transmission between hosts and are well known for an abundance of ...201627189996
transcriptome analysis provides insight into venom evolution in a seed-parasitic wasp, megastigmus spermotrophus.one of the most striking host range transitions is the evolution of plant parasitism from animal parasitism. parasitoid wasps that have secondarily evolved to attack plants (ie gall wasps and seed-feeders) demonstrate intimate associations with their hosts, yet the mechanism of plant-host manipulation is currently not known. there is, however, emerging evidence suggesting that ovipositional secretions play a role in plant manipulation. to investigate whether parasites have modified pre-existing ...201627286234
superparasitism drives heritable symbiont epidemiology and host sex ratio in a wasp.heritable microbial symbionts have profound impacts upon the biology of their arthropod hosts. whilst our current understanding of the dynamics of these symbionts is typically cast within a framework of vertical transmission only, horizontal transmission has been observed in a number of cases. for instance, several symbionts can transmit horizontally when their parasitoid hosts share oviposition patches with uninfected conspecifics, a phenomenon called superparasitism. despite this, horizontal t ...201627322651
ogs2: genome re-annotation of the jewel wasp nasonia vitripennis.nasonia vitripennis is an emerging insect model system with haplodiploid genetics. it holds a key position within the insect phylogeny for comparative, evolutionary and behavioral genetic studies. the draft genomes for n. vitripennis and two sibling species were published in 2010, yet a considerable amount of transcriptiome data have since been produced thereby enabling improvements to the original (ogs1.2) annotated gene set. we describe and apply the evidentialgene method used to produce an up ...201627561358
analysis of 5' gene regions reveals extraordinary conservation of novel non-coding sequences in a wide range of animals.phylogenetic footprinting is a comparative method based on the principle that functional sequence elements will acquire fewer mutations over time than non-functional sequences. successful comparisons of distantly related species will thus yield highly important sequence elements likely to serve fundamental biological roles. rna regulatory elements are less well understood than those in dna. in this study we use the emerging model organism nasonia vitripennis, a parasitic wasp, in a comparative a ...201526482678
scrutinizing the immune defence inventory of camponotus floridanus applying total transcriptome sequencing.defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. this lifestyle potentially facilitates the rapid spread of pathogens between individuals. in concert with their innate immune system, social insects may apply external immune defences to manipulate the microbial community among individuals and within nests. ...201526198742
the genome and methylome of a beetle with complex social behavior, nicrophorus vespilloides (coleoptera: silphidae).testing for conserved and novel mechanisms underlying phenotypic evolution requires a diversity of genomes available for comparison spanning multiple independent lineages. for example, complex social behavior in insects has been investigated primarily with eusocial lineages, nearly all of which are hymenoptera. if conserved genomic influences on sociality do exist, we need data from a wider range of taxa that also vary in their levels of sociality. here, we present the assembled and annotated ge ...201526454014
molecular cloning and functional studies of two kazal-type serine protease inhibitors specifically expressed by nasonia vitripennis venom apparatus.two cdna sequences of kazal-type serine protease inhibitors (kspis) in nasonia vitripennis, nvkspi-1 and nvkspi-2, were characterized and their open reading frames (orfs) were 198 and 264 bp, respectively. both nvkspi-1 and nvkspi-2 contained a typical kazal-type domain. real-time quantitative pcr (rt-qpcr) results revealed that nvkspi-1 and nvkspi-2 mrnas were mostly detected specifically in the venom apparatus, while they were expressed at lower levels in the ovary and much lower levels in oth ...201526248077
a venom gland extracellular chitin-binding-like protein from pupal endoparasitoid wasps, pteromalus puparum, selectively binds chitin.chitin-binding proteins (cbps) are present in many species and they act in a variety of biological processes. we analyzed a pteromalus puparum venom apparatus proteome and transcriptome and identified a partial gene encoding a possible cbp. here, we report cloning a full-length cdna of a sequence encoding a chitin-binding-like protein (ppcbp) from p. puparum, a pupal endoparasitoid of pieris rapae. the cdna encoded a 96-amino-acid protein, including a secretory signal peptide and a chitin-bindin ...201526633500
simple method for fluorescence dna in situ hybridization to squashed chromosomes.dna in situ hybridization (dna ish) is a commonly used method for mapping sequences to specific chromosome regions. this approach is particularly effective at mapping highly repetitive sequences to heterochromatic regions, where computational approaches face prohibitive challenges. here we describe a streamlined protocol for dna ish that circumvents formamide washes that are standard steps in other dna ish protocols. our protocol is optimized for hybridization with short single strand dna probes ...201525591075
phylogeny and oscillating expression of period and cryptochrome in short and long photoperiods suggest a conserved function in nasonia vitripennis.photoperiodism, the ability to respond to seasonal varying day length with suitable life history changes, is a common trait in organisms that live in temperate regions. in most studied organisms, the circadian system appears to be the basis for photoperiodic time measurement. in insects this is still controversial: while some data indicate that the circadian system is causally involved in photoperiodism, others suggest that it may have a marginal or indirect role. resonance experiments in the pa ...201424758403
dual mode of embryonic development is highlighted by expression and function of nasonia pair-rule genes.embryonic anterior-posterior patterning is well understood in drosophila, which uses 'long germ' embryogenesis, in which all segments are patterned before cellularization. in contrast, most insects use 'short germ' embryogenesis, wherein only head and thorax are patterned in a syncytial environment while the remainder of the embryo is generated after cellularization. we use the wasp nasonia (nv) to address how the transition from short to long germ embryogenesis occurred. maternal and gap gene e ...201424599282
parasitization by scleroderma guani influences expression of superoxide dismutase genes in tenebrio molitor.superoxide dismutase (sod) is an antioxidant enzyme involved in detoxifying reactive oxygen species. in this study, we identified genes encoding the extracellular and intracellular copper-zinc sods (eccuznsod and iccuznsod) and a manganese sod (mnsod) in the yellow mealworm beetle, tenebrio molitor. the cdnas for eccuznsod, iccuznsod, and mnsod, respectively, encode 24.55, 15.81, and 23.14 kda polypeptides, which possess structural features typical of other insect sods. they showed 20-94% identi ...201425042129
transcriptional activation is a conserved feature of the early embryonic factor zelda that requires a cluster of four zinc fingers for dna binding and a low-complexity activation domain.delayed transcriptional activation of the zygotic genome is a nearly universal phenomenon in metazoans. immediately following fertilization, development is controlled by maternally deposited products, and it is not until later stages that widespread activation of the zygotic genome occurs. although the mechanisms driving this genome activation are currently unknown, the transcriptional activator zelda (zld) has been shown to be instrumental in driving this process in drosophila melanogaster. her ...201425538246
nasonia vitripennis venom causes targeted gene expression changes in its fly host.parasitoid wasps are diverse and ecologically important insects that use venom to modify their host's metabolism for the benefit of the parasitoid's offspring. thus, the effects of venom can be considered an 'extended phenotype' of the wasp. the model parasitoid wasp nasonia vitripennis has approximately 100 venom proteins, 23 of which do not have sequence similarity to known proteins. envenomation by n. vitripennis has previously been shown to induce developmental arrest, selective apoptosis an ...201425319487
whole-genome dna methylation profile of the jewel wasp (nasonia vitripennis).the epigenetic mark of dna methylation, the addition of a methyl (ch3) group to a cytosine residue, has been extensively studied in many mammalian genomes and, although it is commonly found at the promoter regions of genes, it is also involved in a number of different biological functions. in other complex animals, such as social insects, dna methylation has been determined to be involved in caste differentiation and to occur primarily in gene bodies. the role of methylation in nonsocial insects ...201424381191
the expression and phylogenetics of the inhibitor cysteine knot peptide oclp1 in the honey bee apis mellifera.small cysteine-rich peptides have diverse functions in insects including antimicrobial defense, phenoloxidase activity regulation, and toxic inhibition of ion channels of prey or predator. we combined bioinformatics and measurements of transcript abundance to start characterizing amoclp1, a recently discovered inhibitor cysteine knot peptide in the honey bee apis mellifera. we found that the genomes of ants, bees, and the wasp nasonia vitripennis encode orthologous sequences indicating that oclp ...201424721445
genomic imprinting and maternal effect genes in haplodiploid sex determination.the research into the drosophila melanogaster sex-determining system has been at the basis of all further research on insect sex determination. this further research has made it clear that, for most insect species, the presence of sufficient functional transformer (tra) protein in the early embryonic stage is essential for female sexual development. in hymenoptera, functional analysis of sex determination by knockdown studies of sex-determining genes has only been performed for 2 species. the fi ...201424356125
function and evolution of dna methylation in nasonia vitripennis.the parasitoid wasp nasonia vitripennis is an emerging genetic model for functional analysis of dna methylation. here, we characterize genome-wide methylation at a base-pair resolution, and compare these results to gene expression across five developmental stages and to methylation patterns reported in other insects. an accurate assessment of dna methylation across the genome is accomplished using bisulfite sequencing of adult females from a highly inbred line. one-third of genes show extensive ...201324130511
a new embryonic pattern in parasitic wasps: divergence in early development may not be associated with lifestyle.comparative embryogenesis of encarsia formosa and encarsia pergandiella (hymenoptera aphelinidae), two endoparasitoids of whiteflies (hemiptera aleyrodidae), revealed two strongly diverging developmental patterns. indeed, the centrolecithal anhydropic egg of e. formosa developed through a superficial cleavage, as it occurs in nasonia vitripennis, apis mellifera, and drosophila melanogaster. in contrast, the alecithal hydropic egg of e. pergandiella developed through holoblastic cleavage within a ...201324261443
origin and evolution of a new exon of 14-3-3ξ in bees and phylogenetic analysis.mutually exclusive splicing, one type of alternative splicing, involves selection of alternatively spliced exons arranged in tandem and creates protein products with substitution of one segment of the amino acid sequence for another. previous studies revealed that exon 5 of 14-3-3ξ from apis mellifera (western honeybee) had three mutually exclusive exons, while orthologous exon of nasonia vitripennis (parasitic wasp) had only two, suggesting that cases of exon gain or loss might have happened du ...201323706076
insect wing membrane topography is determined by the dorsal wing epithelium.the drosophila wing consists of a transparent wing membrane supported by a network of wing veins. previously, we have shown that the wing membrane cuticle is not flat but is organized into ridges that are the equivalent of one wing epithelial cell in width and multiple cells in length. these cuticle ridges have an anteroposterior orientation in the anterior wing and a proximodistal orientation in the posterior wing. the precise topography of the wing membrane is remarkable because it is a fusion ...201323316434
paternal transmission of an extrachromosomal factor in a wasp: evolutionary implications.females of the haplodiploid wasp, nasonia vitripennis, lay both fertilised eggs (= female) and unfertilised eggs (= male) following matings with ordinary males. matings with males that carry the extrachromosomal paternal-sex-ratio (psr) factor result in the production of all-male broods. these male offspring are haploid and inherit only the maternal genome, yet some also inherit the psr factor. the proportion of males inheriting psr is highly correlated with the proportion of eggs fertilised in ...20133610659
partial venom gland transcriptome of a drosophila parasitoid wasp, leptopilina heterotoma, reveals novel and shared bioactive profiles with stinging hymenoptera.analysis of natural host-parasite relationships reveals the evolutionary forces that shape the delicate and unique specificity characteristic of such interactions. the accessory long gland-reservoir complex of the wasp leptopilina heterotoma (figitidae) produces venom with virus-like particles. upon delivery, venom components delay host larval development and completely block host immune responses. the host range of this drosophila endoparasitoid notably includes the highly-studied model organis ...201323688557
patterning the dorsal-ventral axis of the wasp nasonia vitripennis.regulatory networks composed of interacting genes are responsible for pattern formation and cell type specification in a wide variety of developmental contexts. evolution must act on these regulatory networks in order to change the proportions, distribution, and characteristics of specified cells. thus, understanding how these networks operate in homologous systems across multiple levels of phylogenetic divergence is critical for understanding the evolution of developmental systems. among the mo ...201323735637
evidence for compensatory evolution of ribosomal proteins in response to rapid divergence of mitochondrial rrna.rapid evolution of mitochondrial dna (mtdna) places intrinsic selective pressures on many nuclear genes involved in mitochondrial functions. mitochondrial ribosomes, for example, are composed of mtdna-encoded ribosomal rnas (rrnas) and a set of more than 60 nuclear-encoded ribosomal proteins (mrp) distinct from the cytosolic rps (crp). we hypothesized that the rapid divergence of mt-rrna would result in rapid evolution of mrps relative to crps, which respond to slowly evolving nuclear-encoded rr ...201322993236
sex chromosomes evolved from independent ancestral linkage groups in winged insects.the evolution of a pair of chromosomes that differ in appearance between males and females (heteromorphic sex chromosomes) has occurred repeatedly across plants and animals. recent work has shown that the male heterogametic (xy) and female heterogametic (zw) sex chromosomes evolved independently from different pairs of homomorphic autosomes in the common ancestor of birds and mammals but also that x and z chromosomes share many convergent molecular features. however, little is known about how of ...201222319158
unique features of odorant-binding proteins of the parasitoid wasp nasonia vitripennis revealed by genome annotation and comparative analyses.insects are the most diverse group of animals on the planet, comprising over 90% of all metazoan life forms, and have adapted to a wide diversity of ecosystems in nearly all environments. they have evolved highly sensitive chemical senses that are central to their interaction with their environment and to communication between individuals. understanding the molecular bases of insect olfaction is therefore of great importance from both a basic and applied perspective. odorant binding proteins (ob ...201222952629
capa-gene products in the haematophagous sandfly phlebotomus papatasi (scopoli)--vector for leishmaniasis disease.sandflies (phlebotominae, nematocera, diptera) are responsible for transmission of leishmaniasis and other protozoan-borne diseases in humans, and these insects depend on the regulation of water balance to cope with the sudden and enormous intake of blood over a very short time period. the sandfly inventory of neuropeptides, including those that regulate diuretic processes, is completely unknown. direct maldi-tof/tof mass spectrometric analysis of dissected ganglia of phlebotomus papatasi, combi ...201223266568
isolation of arsenophonus nasoniae from ixodes ricinus ticks in slovakia.the tick ixodes ricinus is the most prevalent and widely distributed tick species in central europe, commonly found in woodlands, heaths, and forests and particularly abundant in the alpine region. this tick readily bites humans and transmits a number of bacterial and viral pathogens. we collected 10 live nymphs of i. ricinus ticks from vegetation in the rovinka forest, slovakia, and isolated a strain of arsenophonus nasoniae from one tick using the bme/ctvm2 cell line. a new isolate was then su ...201223182269
genome-wide association between dna methylation and alternative splicing in an invertebrate.gene bodies are the most evolutionarily conserved targets of dna methylation in eukaryotes. however, the regulatory functions of gene body dna methylation remain largely unknown. dna methylation in insects appears to be primarily confined to exons. two recent studies in apis mellifera (honeybee) and nasonia vitripennis (jewel wasp) analyzed transcription and dna methylation data for one gene in each species to demonstrate that exon-specific dna methylation may be associated with alternative spli ...201222978521
raalin, a transcript enriched in the honey bee brain, is a remnant of genomic rearrangement in hymenoptera.we identified a predicted compact cysteine-rich sequence in the honey bee genome that we called 'raalin'. raalin transcripts are enriched in the brain of adult honey bee workers and drones, with only minimum expression in other tissues or in pre-adult stages. open-reading frame (orf) homologues of raalin were identified in the transcriptomes of fruit flies, mosquitoes and moths. the raalin-like gene from drosophila melanogaster encodes for a short secreted protein that is maximally expressed in ...201222404450
discovery of defense- and neuropeptides in social ants by genome-mining.natural peptides of great number and diversity occur in all organisms, but analyzing their peptidome is often difficult. with natural product drug discovery in mind, we devised a genome-mining approach to identify defense- and neuropeptides in the genomes of social ants from atta cephalotes (leaf-cutter ant), camponotus floridanus (carpenter ant) and harpegnathos saltator (basal genus). numerous peptide-encoding genes of defense peptides, in particular defensins, and neuropeptides or regulatory ...201222448224
allatotropin, leucokinin and akh in honey bees and other hymenoptera.in the honey bee no allatotropin gene has been found, even though allatotropin stimulates the synthesis of juvenile hormone in this species. we report here that honey bees and other hymenoptera do have a typical allatotropin gene, although the peptides predicted have a somewhat different structure from that of other insect allatotropins. polyclonal antisera to honey bee allatotropin reacted with material in the neurohemal organs of the segmental nerves of abdominal ganglia. we were unable to fin ...201222406227
oligonucleotide primers for targeted amplification of single-copy nuclear genes in apocritan hymenoptera.published nucleotide sequence data from the mega-diverse insect order hymenoptera (sawflies, bees, wasps, and ants) are taxonomically scattered and still inadequate for reconstructing a well-supported phylogenetic tree for the order. the analysis of comprehensive multiple gene data sets obtained via targeted pcr could provide a cost-effective solution to this problem. however, oligonucleotide primers for pcr amplification of nuclear genes across a wide range of hymenopteran species are still sca ...201222768134
draft genome of the globally widespread and invasive argentine ant (linepithema humile).ants are some of the most abundant and familiar animals on earth, and they play vital roles in most terrestrial ecosystems. although all ants are eusocial, and display a variety of complex and fascinating behaviors, few genomic resources exist for them. here, we report the draft genome sequence of a particularly widespread and well-studied species, the invasive argentine ant (linepithema humile), which was accomplished using a combination of 454 (roche) and illumina sequencing and community-base ...201121282631
improvement in the prediction of the translation initiation site through balancing methods, inclusion of acquired knowledge and addition of features to sequences of mrna.the accurate prediction of the initiation of translation in sequences of mrna is an important activity for genome annotation. however, obtaining an accurate prediction is not always a simple task and can be modeled as a problem of classification between positive sequences (protein codifiers) and negative sequences (non-codifiers). the problem is highly imbalanced because each molecule of mrna has a unique translation initiation site and various others that are not initiators. therefore, this stu ...201122369295
comparative analyses of dna methylation and sequence evolution using nasonia genomes.the functional and evolutionary significance of dna methylation in insect genomes remains to be resolved. nasonia is well situated for comparative analyses of dna methylation and genome evolution, since the genomes of a moderately distant outgroup species as well as closely related sibling species are available. using direct sequencing of bisulfite-converted dna, we uncovered a substantial level of dna methylation in 17 of 18 nasonia vitripennis genes and a strong correlation between methylation ...201121693438
draft genome of the red harvester ant pogonomyrmex barbatus.we report the draft genome sequence of the red harvester ant, pogonomyrmex barbatus. the genome was sequenced using 454 pyrosequencing, and the current assembly and annotation were completed in less than 1 y. analyses of conserved gene groups (more than 1,200 manually annotated genes to date) suggest a high-quality assembly and annotation comparable to recently sequenced insect genomes using sanger sequencing. the red harvester ant is a model for studying reproductive division of labor, phenotyp ...201121282651
survival of submerged blowfly species and their parasitoids: implications for postmortem submersion interval.pupal survival of three blowfly species, chrysomya albiceps, chrysomya megacephala, and chrysomya putoria (diptera: calliphoridae) and the parasitoid species nasonia vitripennis (hymenoptera: pteromalidae) was studied after the pupae were experimentally submerged in water. non-parasitized pupae at different developmental stages, 0, 24, 48, and 72h, and parasitized pupae after 3, 8, 10, and 12 days of development were submerged for 6, 24, 48, or 72h. control groups for each pupal developmental st ...201121723056
molecular characterization and expression profile of map2k1ip1/mp1 gene from tiger shrimp, penaeus monodon.mapk kinase 1 interacting protein 1 (map2k1ip1) is an important scaffold proteins of the mitogen-activated protein kinase (mapk) pathway that form an active signaling module and enhance the specificity and spatiality of mapk signaling. in the present study, we identified and characterized a map2k1ip1 cdna from tiger shrimp penaeus monodon (designated as pmmap2k1ip1). the open reading frame of pmmap2k1ip1 is 372 bp encoding 123 amino-acid residues with a mapk interaction domain. the predicted pmm ...201122209950
complete bacteriophage transfer in a bacterial endosymbiont (wolbachia) determined by targeted genome capture.bacteriophage flux can cause the majority of genetic diversity in free-living bacteria. this tenet of bacterial genome evolution generally does not extend to obligate intracellular bacteria owing to their reduced contact with other microbes and a predominance of gene deletion over gene transfer. however, recent studies suggest intracellular coinfections in the same host can facilitate exchange of mobile elements between obligate intracellular bacteria-a means by which these bacteria can partiall ...201121292630
temperature affects the tripartite interactions between bacteriophage wo, wolbachia, and cytoplasmic incompatibility.wolbachia infections are a model for understanding intracellular, bacterial symbioses. while the symbiosis is often studied from a binary perspective of host and bacteria, it is increasingly apparent that additional trophic levels can influence the symbiosis. for example, wolbachia in arthropods harbor a widespread temperate bacteriophage, termed wo, that forms virions and rampantly transfers between coinfections. here we test the hypothesis that temperatures at the extreme edges of an insect's ...201122194999
suppression subtractive hybridization analysis reveals expression of conserved and novel genes in male accessory glands of the ant leptothorax gredleri.during mating, insect males eject accessory gland proteins (acps) into the female genital tract. these substances are known to affect female post-mating behavior and physiology. in addition, they may harm the female, e.g., in reducing its lifespan. this is interpreted as a consequence of sexual antagonistic co-evolution. whereas sexual conflict abounds in non-social species, the peculiar life history of social insects (ants, bees, wasps) with lifelong pair-bonding and no re-mating aligns the rep ...201020825642
two novel proteins expressed by the venom glands of apis mellifera and nasonia vitripennis share an ancient c1q-like domain.an in-depth proteomic study of previously unidentified two-dimensional polyacrylamide gel electrophoresis spots of honey bee (apis mellifera, hymenoptera) venom revealed a new protein with a c1q conserved domain (c1q-vp). blastp searching revealed a strong identity with only two proteins from other insect species: the jewel wasp, nasonia vitripennis (hymenoptera), and the green pea aphid, acyrthosiphon pisum (hemiptera). in higher organisms, c1q is the first subcomponent of the classical complem ...201020167013
the draft genome sequence of arsenophonus nasoniae, son-killer bacterium of nasonia vitripennis, reveals genes associated with virulence and symbiosis.four percent of female nasonia vitripennis carry the son-killer bacterium arsenophonus nasoniae, a microbe with notably different biology from other inherited parasites and symbionts. in this paper, we examine a draft genome sequence of the bacterium for open reading frames (orfs), structures and pathways involved in interactions with its insect host. the genome data suggest that a. nasoniae carries multiple type iii secretion systems, and an array of toxin and virulence genes found in photorhab ...201020167018
the host range of the male-killing symbiont arsenophonus nasoniae in filth fly parasitioids.the son-killer bacterium, arsenophonus nasoniae, infects nasonia vitripennis (hymenoptera: pteromalidae), a parasitic wasp that attacks filth flies. this gammaproteobacterium kills a substantial amount of male embryos produced by an infected female. aside from male death, the bacterium does not measurably affect the host, and how it is maintained in the host population is unknown. interestingly, this bacterial symbiont can be transmitted both vertically (from mother to offspring) and horizontall ...201021147118
the transformer gene of ceratitis capitata: a paradigm for a conserved epigenetic master regulator of sex determination in insects.the transformer gene in ceratitis capitata (cctra(ep)) is the founding member of a family of related sr genes that appear to act as the master epigenetic switch in sex determination in insects. a functional protein seems to be produced only in individuals with a female xx karyotype where it is required to maintain the productive mode of expression through a positive feedback loop and to direct female development by instructing the downstream target genes accordingly. when zygotic activation of t ...201020890720
a defensin antimicrobial peptide from the venoms of nasonia vitripennis.although many antimicrobial components (i.e. antimicrobial peptides) have been found in many social hymenoptera venoms, no antimicrobial compound is purified and characterized from parasitic hymenoptera. from the venoms of the ectoparasitic wasp, nasonia vitripennis, a defensin-like antimicrobial peptide named defensin-nv was purified and characterized. defensin-nv is composed of 52 amino acid residues including 6 cysteines forming 3 disulfide bridges. its amino acid sequence is vtcellmfggvvgdsa ...201020362606
characteristics of the genome of arsenophonus nasoniae, son-killer bacterium of the wasp nasonia.we report the properties of a draft genome sequence of the bacterium arsenophonus nasoniae, son-killer bacterium of nasonia vitripennis. the genome sequence data from this study are the first for a male-killing bacterium, and represent a microorganism that is unusual compared with other sequenced symbionts, in having routine vertical and horizontal transmission, two alternating hosts, and being culturable on cell-free media. the resulting sequence totals c. 3.5 mbp and is annotated to contain 33 ...201020167019
functional characterization of transcription factor motifs using cross-species comparison across large evolutionary distances.we address the problem of finding statistically significant associations between cis-regulatory motifs and functional gene sets, in order to understand the biological roles of transcription factors. we develop a computational framework for this task, whose features include a new statistical score for motif scanning, the use of different scores for predicting targets of different motifs, and new ways to deal with redundancies among significant motif-function associations. this framework is applie ...201020126523
maternal control of haplodiploid sex determination in the wasp nasonia.all insects in the order hymenoptera have haplodiploid sex determination, in which males emerge from haploid unfertilized eggs and females are diploid. sex determination in the honeybee apis mellifera is controlled by the complementary sex determination (csd) locus, but the mechanisms controlling sex determination in other hymenoptera without csd are unknown. we identified the sex-determination system of the parasitic wasp nasonia, which has no csd locus. instead, maternal input of nasonia vitri ...201020431014
cool-weather activity of the forensically important hairy maggot blow fly chrysomya rufifacies (macquart) (diptera: calliphoridae) on carrion in upstate south carolina, united states.the hairy maggot blow fly chrysomya rufifacies (macquart) (diptera: calliphoridae) has expanded its range in the united states since its introduction into texas (ca. 1980) and has been collected in 15 states. we investigated the bionomics of immature and adult c. rufifacies collected from carcasses of a raccoon procyon lotor (linnaeus) and white-tailed deer odocoileus virginianus zimmerman in upstate south carolina during november 2007, and used these insects to estimate the minimum period of in ...201020042303
chitinase-like proteins encoded in the genome of the pea aphid, acyrthosiphon pisum.in insects, chitinases play an essential role in the degradation of old exoskeleton and turnover of the gut lining. in silico screening of the entire genome of the pea aphid (hemimetabola), acyrthosiphon pisum, detected nine genes encoding putative chitinase-like proteins, including six enzymatically active chitinases, one imaginal disc growth factor, and one endo-beta-n-acetylglucosaminidase. screening of the genomes of aedes aegypti, anopheles gambiae, apis mellifera, bombyx mori, culex quinqu ...201020482649
inventory and phylogenomic distribution of meiotic genes in nasonia vitripennis and among diverse arthropods.the parasitoid jewel wasp nasonia vitripennis reproduces by haplodiploidy (arrhenotokous parthenogenesis). in diploid females, meiosis occurs during oogenesis, but in haploid males spermatogenesis is ameiotic and involves a single equational division. here we describe the phylogenomic distribution of meiotic genes in n. vitripennis and in 10 additional arthropods. homologues for 39 meiosis-related genes (including seven meiosis-specific genes) were identified in n. vitripennis. the meiotic genes ...201020167026
molecular cloning, characterization, and expression analysis of an estrogen receptor-related receptor homologue in the cricket, teleogryllus emma.the estrogen receptor-related receptors (errs) are a group of nuclear receptors that were originally identified on the basis of sequence similarity to estrogen receptors. the three mammalian err genes have been implicated in diverse physiological processes ranging from placental development to maintenance of bone density, but the function and regulation of errs in invertebrates are not well understood. a homologue of human err was isolated from the cricket teleogryllus emma (ohmachi and matsumur ...201021265615
functional and evolutionary insights from the genomes of three parasitoid nasonia species.we report here genome sequences and comparative analyses of three closely related parasitoid wasps: nasonia vitripennis, n. giraulti, and n. longicornis. parasitoids are important regulators of arthropod populations, including major agricultural pests and disease vectors, and nasonia is an emerging genetic model, particularly for evolutionary and developmental genetics. key findings include the identification of a functional dna methylation tool kit; hymenopteran-specific genes including diverse ...201020075255
discovery of a novel insect neuropeptide signaling system closely related to the insect adipokinetic hormone and corazonin hormonal systems.neuropeptides and their g protein-coupled receptors (gpcrs) play a central role in the physiology of insects. one large family of insect neuropeptides are the adipokinetic hormones (akhs), which mobilize lipids and carbohydrates from the insect fat body. other peptides are the corazonins that are structurally related to the akhs but represent a different neuropeptide signaling system. we have previously cloned an orphan gpcr from the malaria mosquito anopheles gambiae that was structurally inter ...201020068045
transfers of mitochondrial dna to the nuclear genome in the wasp nasonia vitripennis.many organisms carry nuclear sequences of mitochondrial origin (numts). we have identified 76 numts in 25 genomic locations in the jewel wasp nasonia vitripennis. the total amount of numts in nasonia is 42 972 bp exceeding over four-fold that found in tribolium castaneum and almost fifty-fold that found in drosophila melanogaster, whereas apis mellifera has an even larger number of numts in its genome (over 230 kb). the nasonia numts were inserted by multiple independent events and frequently in ...201020167015
genomics and peptidomics of neuropeptides and protein hormones present in the parasitic wasp nasonia vitripennis.neuropeptides and protein hormones constitute a very important group of signaling molecules, regulating central physiological processes such as reproduction, development, and behavior. using a bioinformatics approach, we screened the recently sequenced genome of the parasitic wasp, nasonia vitripennis, for the presence of these signaling molecules and annotated 30 precursor genes encoding 51 different mature neuropeptides or protein hormones. twenty-four of the predicted mature nasonia neuropept ...201020695486
the genetic basis of interspecies host preference differences in the model parasitoid nasonia.the genetic basis of host preference has been investigated in only a few species. it is relevant to important questions in evolutionary biology, including sympatric speciation, generalist versus specialist adaptation, and parasite-host co-evolution. here we show that a major locus strongly influences host preference in nasonia. nasonia are parasitic wasps that utilize fly pupae; nasonia vitripennis is a generalist that parasitizes a diverse set of hosts, whereas nasonia giraulti specializes in p ...201020087393
the cys-loop ligand-gated ion channel gene superfamily of the parasitoid wasp, nasonia vitripennis.members of the cys-loop ligand-gated ion channel (cyslgic) superfamily mediate chemical neurotransmission and are studied extensively as potential targets of drugs used to treat neurological disorders, such as alzheimer's disease. insect cys-loop lgics also have central roles in the nervous system and are targets of highly successful insecticides. here, we describe the cyslgic superfamily of the parasitoid wasp, nasonia vitripennis, which is emerging as a highly useful model organism and is depl ...201020087392
phylogeography of nasonia vitripennis (hymenoptera) indicates a mitochondrial-wolbachia sweep in north america.here we report evidence of a mitochondrial-wolbachia sweep in north american populations of the parasitoid wasp nasonia vitripennis, a cosmopolitan species and emerging model organism for evolutionary and genetic studies. analysis of the genetic variation of 89 n. vitripennis specimens from europe and north america was performed using four types of genetic markers: a portion of the mitochondrial cytochrome oxidase i gene, nine polymorphic nuclear microsatellites, sequences from 11 single-copy nu ...201020087396
egf signaling and the origin of axial polarity among the insects.the eggs of insects are unusual in that they often have bilateral symmetry when they are laid, indicating that both anterior-posterior (ap) and dorsal-ventral (dv) symmetries are broken during oogenesis. the molecular basis of this process is well understood in drosophila melanogaster, in which symmetry breaking events for both axes depend on the asymmetric position of the oocyte nucleus and on germline-soma signaling mediated by the tgf alpha-like epidermal growth factor (egf) ligand gurken. ge ...201020471269
antimicrobial peptide-like genes in nasonia vitripennis: a genomic perspective.antimicrobial peptides (amps) are an essential component of innate immunity which can rapidly respond to diverse microbial pathogens. insects, as a rich source of amps, attract great attention of scientists in both understanding of the basic biology of the immune system and searching molecular templates for anti-infective drug design. despite a large number of amps have been identified from different insect species, little information in terms of these peptides is available from parasitic insect ...201020302637
metabolic enzymes associated with xenobiotic and chemosensory responses in nasonia vitripennis.the numbers of glutathione s-transferase, cytochrome p450 and esterase genes in the genome of the hymenopteran parasitoid nasonia vitripennis are about twice those found in the genome of another hymenopteran, the honeybee apis mellifera. some of the difference is associated with clades of these families implicated in xenobiotic resistance in other insects and some is in clades implicated in hormone and pheromone metabolism. the data support the hypothesis that the eusocial behaviour of the honey ...201020167025
the insect chemoreceptor superfamily of the parasitoid jewel wasp nasonia vitripennis.chemoreception is important for locating food, mates and other resources in many insects, including the parasitoid jewel wasp nasonia vitripennis. in the insect chemoreceptor superfamily, nasonia has 58 gustatory receptor (gr) genes, of which 11 are pseudogenes, leaving 47 apparently intact proteins encoded. no carbon dioxide receptors, two candidate sugar receptors, a dmgr43a orthologue, and several additional gr lineages were identified, including significant gene subfamily expansions related ...201020167023
identification and characterization of nasonia pax genes.pax genes are a group of critical developmental transcriptional regulators in both invertebrates and vertebrates, characterized by the presence of a paired dna-binding domain. pax proteins also often contain an octapeptide motif and a c-terminal homeodomain. the genome of nasonia vitripennis (hymenoptera) has recently become available, and analysis of this genome alongside apis mellifera allowed us to contribute to the phylogeny of this gene family in insects. nasonia, a parasitic wasp, has inde ...201020167022
the distribution of microsatellites in the nasonia parasitoid wasp genome.microsatellites are important molecular markers used in numerous genetic contexts. despite this widespread use, the evolutionary processes governing microsatellite distribution and diversity remain controversial. here, we present results on the distribution of microsatellites of three species in the parasitic wasp genus nasonia generated by an in silico data-mining approach. our results show that the overall microsatellite density in nasonia is comparable to that of the honey bee, but much highe ...201020167020
venom proteins of the parasitoid wasp nasonia vitripennis: recent discovery of an untapped pharmacopee.adult females of nasonia vitripennis inject a venomous mixture into its host flies prior to oviposition. recently, the entire genome of this ectoparasitoid wasp was sequenced, enabling the identification of 79 venom proteins. the next challenge will be to unravel their specific functions, but based on homolog studies, some predictions already can be made. parasitization has an enormous impact on hosts physiology of which five major effects are discussed in this review: the impact on immune respo ...201022069597
rearing sarcophaga bullata fly hosts for nasonia (parasitoid wasp).nasonia is a complex of four closely related species of wasps with several features that make it an excellent system for a variety of genetic studies. these include a short generation time, ease of rearing, interfertile species, visible and molecular markers, and a sequenced genome. it also can serve as a behavior model for studies of courtship, male aggression and territoriality, female dispersal, and sex ratio control. nasonia vitripennis is a parasitoid of a number of calliphorid flies, such ...200920147053
quercetin-metabolizing cyp6as enzymes of the pollinator apis mellifera (hymenoptera: apidae).although the honey bee (apis mellifera) genome contains far fewer cytochrome p450 genes associated with xenobiotic metabolism than other insect genomes sequenced to date, the cyp6as subfamily, apparently unique to hymenopterans, has undergone an expansion relative to the genome of the jewel wasp (nasonia vitripennis). the relative dominance of this family in the honey bee genome is suggestive of a role in processing phytochemicals encountered by honey bees in their relatively unusual diet of hon ...200919737624
evolution of the sugar receptors in insects.perception of sugars is an invaluable ability for insects which often derive quickly accessible energy from these molecules. a distinctive subfamily of eight proteins within the gustatory receptor (gr) family has been identified as sugar receptors (srs) in drosophila melanogaster (gr5a, gr61a, and gr64a-f). we examined the evolution of these srs within the 12 available drosophila genome sequences, as well as three mosquito, two moth, and beetle, bee, and wasp genome sequences.200919226470
the fruitless gene in nasonia displays complex sex-specific splicing and contains new zinc finger domains.the transcription factor fruitless exerts a broad range of functions during drosophila development, the most apparent of which is the determination of sexual behavior in males. although fruitless sequences are found in other insect orders, little is known about fruitless structure and function outside diptera. we have performed a thorough analysis of fruitless transcripts in the haplo-diploid wasp nasonia vitripennis and found both sex-specific and non-sex-specific transcripts similar to those f ...200919349644
hymenopteran parasitoids of forensic importance: host associations, seasonality, and prevalence of parasitoids of carrion flies in western australia.a 2-yr survey of hymenopteran parasitoids associated with carrion-breeding flies was conducted to establish the parasitoid species of potential forensic significance in western australia. host associations, seasonality, and rates of parasitism in the field were examined to assess the value of the identified parasitoids as forensic indicators of time since death. four species of parasitoid emerged from dipteran specimens collected from carcasses: tachinaephagus zealandicus ashmead (encryptidae), ...200919769056
durations of immature stage development period of nasonia vitripennis (walker) (hymenoptera: pteromalidae) under laboratory conditions: implications for forensic entomology.some microhymenopterans are parasitoids of flies of forensic importance. their parasitic habit can alter the duration of post-embryonic development of these flies, altering the postmortem interval. in order to analyze possible alterations occurring during the immature development period of nasonia vitripennis, this study tested different quantitative associations between female parasitoids and pupae of chrysomya megacephala, which were defined by: (a) one pupa was exposed to different numbers of ...200918972132
deciphering proteomic signatures of early diapause in nasonia.insect diapause is an alternative life-history strategy used to increase longevity and survival in harsh environmental conditions. even though some aspects of diapause are well investigated, broader scale studies that elucidate the global metabolic adjustments required for this remarkable trait, are rare. in order to better understand the metabolic changes during early insect diapause, we used a shotgun proteomics approach on early diapausing and non-diapausing larvae of the recently sequenced h ...200919636376
the parasitoid wasp nasonia: an emerging model system with haploid male genetics.nasonia is a complex of four closely related species of wasps that is rapidly emerging as a model for evolutionary and developmental genetics. it has several features that make it an excellent genetic system, including a short generation time, ease of rearing, interfertile species, visible and molecular markers, and a sequenced genome. the form of sex determination, called "haplodiploidy," makes nasonia particularly suitable as a genetic tool. females are diploid and develop from fertilized eggs ...200920147035
strain maintenance of nasonia vitripennis (parasitoid wasp).nasonia is a complex of four closely related species of wasps with several features that make it an excellent system for a variety of genetic studies. these include a short generation time, ease of rearing, interfertile species, visible and molecular markers, and a sequenced genome. furthermore, its parasitoid lifestyle allows investigations of questions relating to parasitoid/host dynamics, host preference, and specialist versus generalist biology. it also can serve as a behavior model for stud ...200920147052
a case for sequencing the genome of musca domestica (diptera: muscidae).house flies are carriers of >100 devastating diseases that have severe consequences for human and animal health. despite the fact that it is a passive vector, a key bottleneck to progress in controlling the human diseases transmitted by house flies is lack of knowledge of the basic molecular biology of this species. sequencing of the house fly genome will provide important inroads to the discovery of novel target sites for house fly control, understanding of the house fly immune response, rapid ...200919351068
reconstructing the phylogeny of 21 completely sequenced arthropod species based on their motor proteins.motor proteins have extensively been studied in the past and consist of large superfamilies. they are involved in diverse processes like cell division, cellular transport, neuronal transport processes, or muscle contraction, to name a few. vertebrates contain up to 60 myosins and about the same number of kinesins that are spread over more than a dozen distinct classes.200919383156
evolutionary conservation and changes in insect trp channels.trp (transient receptor potential) channels respond to diverse stimuli and thus function as the primary integrators of varied sensory information. they are also activated by various compounds and secondary messengers to mediate cell-cell interactions as well as to detect changes in the local environment. their physiological roles have been primarily characterized only in mice and fruit flies, and evolutionary studies are limited. to understand the evolution of insect trp channels and the mechani ...200919740447
rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp nasonia (hymenoptera: pteromalidae).we sequenced the nearly complete mtdna of 3 species of parasitic wasps, nasonia vitripennis (2 strains), nasonia giraulti, and nasonia longicornis, including all 13 protein-coding genes and the 2 rrnas, and found unusual patterns of mitochondrial evolution. the nasonia mtdna has a unique gene order compared with other insect mtdnas due to multiple rearrangements. the mtdnas of these wasps also show nucleotide substitution rates over 30 times faster than nuclear protein-coding genes, indicating a ...200818653734
wolbachia modification of sperm does not always require residence within developing sperm.wolbachia are maternally inherited intracellular bacteria known to manipulate the reproduction of their arthropod hosts. wolbachia commonly affect the sperm of infected arthropods. wolbachia-modified sperm cannot successfully fertilize unless the female is infected with the same wolbachia type. a study of spermatogenesis in the parasitic wasp nasonia vitripennis reveals that wolbachia are not required in individual spermatocytes or spermatids to modify sperm. in n. vitripennis, wolbachia modify ...200818648384
cloning and identification of an oxytocin/vasopressin-like receptor and its ligand from insects.more than 20 years ago, an oxytocin/vasopressin-like peptide, clitncprgamide, was isolated from the locust, locusta migratoria [proux jp, et al. (1987) identification of an arginine vasopressin-like diuretic hormone from locusta migratoria. biochem biophys res commun 149:180-186]. however, no similar peptide could be identified in other insects, nor could its prohormone be cloned, or its physiological actions be established. here, we report that the recently sequenced genome from the red flour b ...200818316733
plasticity in mrna expression and localization of orthodenticle within higher diptera.orthodenticle (otd) genes are found throughout the animal kingdom and encode well-studied homeodomain transcription factors that share conserved functions in cephalization, head segmentation, brain patterning, and the differentiation of photoreceptors. otd proteins have been proposed as ancestral key players in anterior determination despite a high level of variation in gene expression at early developmental stages: otd is expressed strictly zygotically in the dipteran drosophila melanogaster, w ...200819021740
the evolution of developmental gene networks: lessons from comparative studies on holometabolous insects.recent comparative studies have revealed significant differences in the developmental gene networks operating in three holometabolous insects: the beetle tribolium castaneum, the parasitic wasp nasonia vitripennis and the fruitfly drosophila melanogaster. i discuss these differences in relation to divergent and convergent changes in cellular embryology. i speculate on how segmentation gene networks have evolved to operate in divergent embryological contexts, and highlight the role that co-option ...200818192180
evolution of the insect sox genes.the sox gene family of transcriptional regulators have essential roles during development and have been extensively studied in vertebrates. the mouse, human and fugu genomes contain at least 20 sox genes, which are subdivided into groups based on sequence similarity of the highly conserved hmg domain. in the well-studied insect drosophila melanogaster, eight sox genes have been identified and are involved in processes such as neurogenesis, dorsal-ventral patterning and segmentation.200818439299
an epoxide hydrolase involved in the biosynthesis of an insect sex attractant and its use to localize the production site.epoxide hydrolases (ehs) are enzymes occurring in virtually any living organism. they catalyze the hydrolysis of epoxide containing lipids and are involved in crucial mechanisms, such as the detoxification of xenobiotics or the regulation of inflammation and blood pressure. here, we describe a function of a putative eh gene in the biosynthesis of a sex attractant in the jewel wasp nasonia vitripennis and use this gene to localize the site of pheromone production. males of this parasitic wasp rel ...200818579785
a bacterium targets maternally inherited centrosomes to kill males in nasonia.male killing is caused by diverse microbial taxa in a wide range of arthropods. this phenomenon poses important challenges to understanding the dynamics of sex ratios and host-pathogen interactions. however, the mechanisms of male killing are largely unknown. evidence from one case in drosophila suggests that bacteria can target components of the male-specific sex-determination pathway. here, we investigated male killing by the bacterium arsenophonus nasoniae in the haplo-diploid wasp nasonia vi ...200818804376
sex determination in the hymenoptera.the dominant and ancestral mode of sex determination in the hymenoptera is arrhenotokous parthenogenesis, in which diploid females develop from fertilized eggs and haploid males develop from unfertilized eggs. we discuss recent progress in the understanding of the genetic and cytoplasmic mechanisms that make arrhenotoky possible. the best-understood mode of sex determination in the hymenoptera is complementary sex determination (csd), in which diploid males are produced under conditions of inbre ...200817803453
[parasitoids of muscoids diptera collected at alvorada slaughterhouse in itumbiara, south of goiás, brazil].species of parasitoids associated with synanthropic flies were trapped by using chopped bovine liver as bites at slaughterhouse itumbiara in the state of goiás, from march to december 2005. pupae were obtained by removing them from sand, after using liver baits as substract to atract flies. they were individually placed in gelatin capsules until the emergency of the adult flies or their parasitoids. the overall prevalence of parasitism was 15.3%. the frequency, percentage and species of parasito ...200718373902
characterization of phenoloxidase activity in venom from the ectoparasitoid nasonia vitripennis (walker) (hymenoptera: pteromalidae).crude venom isolated from the ectoparasitic wasp nasonia vitripennis was found to possess phenoloxidase (po) activity. enzyme activity was detected by using a modified dot blot analysis approach in which venom samples were applied to nylon membranes and incubated with either l-dopa or dopamine. dot formation was most intense with dopamine as the substrate and no activators appeared to be necessary to evoke a melanization reaction. no melanization occurred when venom was incubated in schneider's ...200717054979
haploid females in the parasitic wasp nasonia vitripennis.the insect order of hymenoptera (ants, bees, sawflies, and wasps) consists almost entirely of haplodiploid species. under haplodiploidy, males develop from unfertilized eggs and are haploid, whereas females develop from fertilized eggs and are diploid. although diploid males commonly occur, haploid females have never been reported. in analyzing the phenomenon of gynandromorphism in the parasitoid wasp nasonia vitripennis, we found a line that generates complete phenotypic females from unfertiliz ...200717218519
wasps, beetles and the beginning of the ends.recent papers investigating the genes regulating early embryogenesis in the wasp nasonia vitripennis and the beetle tribolium castaneum have provided us with important clues as to how early development is controlled in insects other than higher dipterans such as drosophila melanogaster. the results of these studies demonstrate that in insects that do not have bicoid, anterior patterning is regulated by a combination of maternal orthodenticle and hunchback. furthermore, during the evolution of lo ...200616850399
[synanthropic flies (diptera: cyclorrapha) and their microhymenoptera parasitoids (insecta: hymenoptera) at monte mor poultry production system, são paulo, brazil].a survey of synanthropic flies and their microhymenopteran parasitoids was conducted at the capuavinha poultry farm, municipality of monte mor, state of são paulo, brazil, from 1991 to 1992. bird manure samples were collected biweekly for examined and selected by the following methods: flotation in water, dissected pupae, and sentinel pupae. the species of flies more abundant were: chrysomya putoria (wiedeman) (41.2% - calliphoridae), muscidae: muscina stabulans( fallén) (27.3%), musca domestica ...200616834896
the tripartite associations between bacteriophage, wolbachia, and arthropods.by manipulating arthropod reproduction worldwide, the heritable endosymbiont wolbachia has spread to pandemic levels. little is known about the microbial basis of cytoplasmic incompatibility (ci) except that bacterial densities and percentages of infected sperm cysts associate with incompatibility strength. the recent discovery of a temperate bacteriophage (wo-b) of wolbachia containing ankyrin-encoding genes and virulence factors has led to intensifying debate that bacteriophage wo-b induces ci ...200616710453
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