Sight of parasitoid wasps accelerates sexual behavior and upregulates a micropeptide gene in Drosophila.
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ABSTRACT:
SUBMITTER: Ebrahim SAM
PROVIDER: S-EPMC8079388 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BackgroundNatural selection has resulted in a complex and fascinating repertoire of innate behaviors that are produced by insects. One puzzling example occurs in fruit fly larvae that have been subjected to a noxious mechanical or thermal sensory input. In response, the larvae "roll" with a motor pattern that is completely distinct from the style of locomotion that is used for foraging.ResultsWe have precisely mapped the sensory neurons that are used by the Drosophila larvae to detect nociceptive stimuli. By using complementary optogenetic activation and targeted silencing of sensory neurons, we have demonstrated that a single class of neuron (class IV multidendritic neuron) is sufficient and necessary for triggering the unusual rolling behavior. In addition, we find that larvae have an innately encoded preference in the directionality of rolling. Surprisingly, the initial direction of rolling locomotion is toward the side of the body that has been stimulated. We propose that directional rolling might provide a selective advantage in escape from parasitoid wasps that are ubiquitously present in the natural environment of Drosophila. Consistent with this hypothesis, we have documented that larvae can escape the attack of Leptopilina boulardi parasitoid wasps by rolling, occasionally flipping the attacker onto its back.ConclusionsThe class IV multidendritic neurons of Drosophila larvae are nociceptive. The nociception behavior of Drosophila melanagaster larvae includes an innately encoded directional preference. Nociception behavior is elicited by the ecologically relevant sensory stimulus of parasitoid wasp attack.
| S-EPMC2225350 | biostudies-literature
Project description:Maternally transmitted associations between endosymbiotic bacteria and insects are diverse and widespread in nature. Owing to imperfect vertical transmission, many heritable microbes have evolved compensational mechanisms to enhance their persistence in host lineages, such as manipulating host reproduction and conferring fitness benefits to host. Symbiont-mediated defense against natural enemies of hosts is increasingly recognized as an important mechanism by which endosymbionts enhance host fitness. Members of the genus Spiroplasma associated with distantly related Drosophila hosts are known to engage in either reproductive parasitism (i.e., male killing) or defense against natural enemies (the parasitic wasp Leptopilina heterotoma and a nematode). A male-killing strain of Spiroplasma (strain Melanogaster Sex Ratio Organism (MSRO)) co-occurs with Wolbachia (strain wMel) in certain wild populations of the model organism Drosophila melanogaster. We examined the effects of Spiroplasma MSRO and Wolbachia wMel on Drosophila survival against parasitism by two common wasps, Leptopilina heterotoma and Leptopilina boulardi, that differ in their host ranges and host evasion strategies. The results indicate that Spiroplasma MSRO prevents successful development of both wasps, and confers a small, albeit significant, increase in larva-to-adult survival of flies subjected to wasp attacks. We modeled the conditions under which defense can contribute to Spiroplasma persistence. Wolbachia also confers a weak, but significant, survival advantage to flies attacked by L. heterotoma. The host protective effects exhibited by Spiroplasma and Wolbachia are additive and may provide the conditions for such cotransmitted symbionts to become mutualists. Occurrence of Spiroplasma-mediated protection against distinct parasitoids in divergent Drosophila hosts suggests a general protection mechanism.
| S-EPMC3966124 | biostudies-literature
Project description:Oak galls form when gall wasps lay their eggs into part of the tree; in some galls, this attachment point to the host consists of only a few cells. The gall itself comprises entirely of host tissue; however, the initiation, development, and physical appearance are controlled by the inducer. This raises the intriguing question of the molecular mechanisms underlying gall formation, by which one or a small number of cells are reprogrammed and commit to a novel developmental path. Gall wasps undergo two generations each year, and the galls formed by these two generations exhibit markedly different appearances. We sequenced the transcriptomes of both the sexual and asexual generations of Neuropterus quercusbaccarum and Neuroterus numismalis. The transcriptomes of the generations that occur at the same time of year are more similar to each other than they are to the opposite generation of their respective species.
2024-06-18 | GSE244168 | GEO
Project description:BackgroundThe majority of Eukaryotic genomes are composed of a small portion of stable (non-mobile) genes and a large fraction of parasitic mobile elements such as transposable elements and endogenous viruses: the Mobilome. Such important component of many genomes are normally underscored in genomic analysis and detailed characterized mobilomes only exists for model species. In this study, we used a combination of de novo and homology approaches to characterize the Mobilome of two non-model parasitoid wasp species.ResultsThe different methodologies employed for TE characterization recovered TEs with different features as TE consensus number and size. Moreover, some TEs were detected only by one or few methodologies. RepeatExplorer and dnaPipeTE estimated a low TE content of 5.86 and 4.57% for Braconidae wasp and 5.22% and 7.42% for L. boulardi species, respectively. Both mobilomes are composed by a miscellaneous of ancient and recent elements. Braconidae wasps presented a large diversity of Maverick/Polintons Class II TEs while other TE superfamilies were more equally diverse in both species. Phylogenetic analysis of reconstructed elements showed that vertical transfer is the main mode of transmission.ConclusionDifferent methodologies should be used complementarity in order to achieve better mobilome characterization. Both wasps genomes have one of the lower mobilome estimates among all Hymenoptera genomes studied so far and presented a higher proportion of Class II than Class I TEs. The large majority of superfamilies analyzed phylogenetically showed that the elements are being inherited by vertical transfer. Overall, we achieved a deep characterization of the mobilome in two non-model parasitoid wasps improving our understanding of their evolution.
| S-EPMC6035795 | biostudies-literature
Project description:Host-parasitoid interactions are among the most studied interactions between invertebrates because of their fundamental interest - the evolution of original traits in parasitoids - and applied, parasitoids being widely used in biological control. Immunity, and in particular cellular immunity, is central in these interactions, the host encapsulation response being specific for large foreign bodies such as parasitoid eggs. Although already well studied in this species, recent data on Drosophila melanogaster have unquestionably improved knowledge of invertebrate cellular immunity. At the same time, the venomics of parasitoids has expanded, notably those of Drosophila. Here, we summarize and discuss these advances, with a focus on an emerging "time-dependent" view of interactions outcome at the intra- and interspecific level. We also present issues still in debate and prospects for study. Data on the Drosophila-parasitoid model paves the way to new concepts in insect immunity as well as parasitoid wasp strategies to overcome it.
| S-EPMC6529592 | biostudies-literature
Project description:Parasitoid wasps use venom to manipulate the immunity and metabolism of their host insects in a variety of ways to provide resources for their offspring. Yet, how genes are recruited and evolve to perform venom functions remain open questions. A recently recognized source of eukaryotic genome innovation is lateral gene transfer (LGT). Glycoside hydrolase family 19 (GH19) chitinases are widespread in bacteria, microsporidia, and plants where they are used in nutrient acquisition or defense, but have previously not been known in metazoans. In this study, a GH19 chitinase LGT is described from the unicellular microsporidia/Rozella clade into parasitoid wasps of the superfamily Chalcidoidea, where it has become recruited as a venom protein. The GH19 chitinase is present in 15 species of chalcidoid wasps representing four families, and phylogenetic analysis indicates that it was laterally transferred near or before the origin of Chalcidoidea (∼95 Ma). The GH19 chitinase gene is highly expressed in the venom gland of at least seven species, indicating a role in the complex host manipulations performed by parasitoid wasp venom. RNAi knockdown in the model parasitoid Nasonia vitripennis reveals that-following envenomation-the GH19 chitinase induces fly hosts to upregulate genes involved in an immune response to fungi. A second, independent LGT of GH19 chitinase from microsporidia into mosquitoes was also found, also supported by phylogenetic reconstructions. Besides these two LGT events, GH19 chitinase is not found in any other sequenced animal genome, or in any fungi outside the microsporidia/Rozella clade.
| S-EPMC5013869 | biostudies-literature
Project description:BackgroundCoexistence of sexual and asexual populations remains a key question in evolutionary ecology. We address the question how an asexual and a sexual form of the parasitoid Venturia canescens can coexist in southern Europe. We test the hypothesis that both forms are adapted to different habitats within their area of distribution. Sexuals inhabit natural environments that are highly unpredictable, and where density of wasps and their hosts is low and patchily distributed. Asexuals instead are common in anthropic environments (e.g., grain stores) where host outbreaks offer periods when egg-load is the main constraint on reproductive output.MethodsWe present a meta-analysis of known adaptations to these habitats. Differences in behavior, physiology and life-history traits between sexual and asexual wasps were standardized in term of effect size (Cohen's d value; Cohen, 1988).ResultsSeeking consilience from the differences between multiple traits, we found that sexuals invest more in longevity at the expense of egg-load, are more mobile, and display higher plasticity in response to thermal variability than asexual counterparts.DiscussionThus, each form has consistent multiple adaptations to the ecological circumstances in the contrasting environments.
| S-EPMC5600175 | biostudies-literature
Project description:UnlabelledInsects commonly harbor facultative bacterial endosymbionts, such as Wolbachia and Spiroplasma species, that are vertically transmitted from mothers to their offspring. These endosymbiontic bacteria increase their propagation by manipulating host reproduction or by protecting their hosts against natural enemies. While an increasing number of studies have reported endosymbiont-mediated protection, little is known about the mechanisms underlying this protection. Here, we analyze the mechanisms underlying protection from parasitoid wasps in Drosophila melanogaster mediated by its facultative endosymbiont Spiroplasma poulsonii Our results indicate that S. poulsonii exerts protection against two distantly related wasp species, Leptopilina boulardi and Asobara tabida S. poulsonii-mediated protection against parasitoid wasps takes place at the pupal stage and is not associated with an increased cellular immune response. In this work, we provide three important observations that support the notion that S. poulsonii bacteria and wasp larvae compete for host lipids and that this competition underlies symbiont-mediated protection. First, lipid quantification shows that both S. poulsonii and parasitoid wasps deplete D. melanogaster hemolymph lipids. Second, the depletion of hemolymphatic lipids using the Lpp RNA interference (Lpp RNAi) construct reduces wasp success in larvae that are not infected with S. poulsonii and blocks S. poulsonii growth. Third, we show that the growth of S. poulsonii bacteria is not affected by the presence of the wasps, indicating that when S. poulsonii is present, larval wasps will develop in a lipid-depleted environment. We propose that competition for host lipids may be relevant to endosymbiont-mediated protection in other systems and could explain the broad spectrum of protection provided.ImportanceVirtually all insects, including crop pests and disease vectors, harbor facultative bacterial endosymbionts. They are vertically transmitted from mothers to their offspring, and some protect their host against pathogens. Here, we studied the mechanism of protection against parasitoid wasps mediated by the Drosophila melanogaster endosymbiont Spiroplasma poulsonii Using genetic manipulation of the host, we provide strong evidence supporting the hypothesis that competition for host lipids underlies S. poulsonii-mediated protection against parasitoid wasps. We propose that lipid competition-based protection may not be restricted to Spiroplasma bacteria but could also apply other endosymbionts, notably Wolbachia bacteria, which can suppress human disease-causing viruses in insect hosts.
| S-EPMC4958261 | biostudies-literature
Project description:Background:Cuticular hydrocarbons (CHC) have been documented to play crucial roles as species- and sex-specific cues in the chemical communication systems of a wide variety of insects. However, whether they are sufficient by themselves as the sole cue triggering sexual behavior as well as preference of con- over heterospecific mating partners is rarely assessed. We conducted behavioral assays in three representative species of parasitoid wasps (Hymenoptera: Pteromalidae) to determine their reliance on CHC as species-specific sexual signaling cues. Results:We found a surprising degree of either unspecific or insufficient sexual signaling when CHC are singled out as recognition cues. Most strikingly, the cosmopolitan species Nasonia vitripennis, expected to experience enhanced selection pressure to discriminate against other co-occurring parasitoids, did not discriminate against CHC of a partially sympatric species from another genus, Trichomalopsis sarcophagae. Focusing on the latter species, in turn, it became apparent that CHC are even insufficient as the sole cue triggering conspecific sexual behavior, hinting at the requirement of additional, synergistic sexual cues particularly important in this species. Finally, in the phylogenetically and chemically most divergent species Muscidifurax uniraptor, we intriguingly found both CHC-based sexual signaling as well as species discrimination behavior intact although this species is naturally parthenogenetic with sexual reproduction only occurring under laboratory conditions. Conclusions:Our findings implicate a discrepancy in the reliance on and specificity of CHC as sexual cues in our tested parasitioid wasps. CHC profiles were not sufficient for unambiguous discrimination and preference behavior, as demonstrated by clear cross-attraction between some of our tested wasp genera. Moreover, we could show that only in T. sarcophagae, additional behavioral cues need to be present for triggering natural mating behavior, hinting at an interesting shift in signaling hierarchy in this particular species. This demonstrates the importance of integrating multiple, potentially complementary signaling modalities in future studies for a better understanding of their individual contributions to natural sexual communication behavior.
| S-EPMC5946414 | biostudies-literature
Project description:Metabolomics studies of low-biomass organisms, such as small insects, have previously relied on the pooling of biological samples to overcome detection limits, particularly using NMR. We show that the differentiation of metabolite profiles of individual 1?mg parasitoid wasps of different ages is possible when using a modified sample preparation and a combination of untargeted NMR and LC-MS based metabolomics. Changes were observed between newly emerged and older wasps in glycerolipids, amino acids and circulatory sugars. This advance in chemical profiling has important implications for the study of the behaviour and ecology of parasitoids and many other species of small organisms because predictions and observations are typically made at the level of the individual. Thus, the metabolomic state of low-biomass individuals can now be related to their behaviour and ecological performance. We discuss specifically the utility of age-related metabolomic profiling but our new approach can be applied to a wide range of biological research.
| S-EPMC5054366 | biostudies-literature