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Evidence of capacitation in the parasitoid wasp, Nasonia vitripennis, and its potential role in sex allocation.

ABSTRACT: The allocation of resources to the production of one sex or another has been observed in a large variety of animals. Its theoretical basis allows accurate predictions of offspring sex ratios in many species, but the mechanisms by which sex allocation is controlled are poorly understood. Using previously published data, we investigated whether alternative splicing, combined with differential gene expression, was involved with sex allocation in the parasitoid wasp, Nasonia vitripennis. We found that sex allocation is not controlled by alternative splicing but changes in gene and transcript-specific expression, which were identified to be involved with oviposition, were shown to be similar to those involved in sperm motility and capacitation. Genes involved in cholesterol efflux, a key component of capacitation, along with calcium transport, neurotransmission, trypsin, and MAPKinase activity were regulated in ovipositing wasps. The results show evidence for regulation of sperm motility and of capacitation in an insect which, in the context of the physiology of the N. vitripennis spermatheca, could be important for sex allocation.

SUBMITTER: Jones ARC

PROVIDER: S-EPMC7391552 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Evidence of capacitation in the parasitoid wasp, <i>Nasonia vitripennis,</i> and its potential role in sex allocation.

Jones Alun R C ARC Jones Alun R C ARC Mallon Eamonn B EB

Ecology and evolution 20200601 14

The allocation of resources to the production of one sex or another has been observed in a large variety of animals. Its theoretical basis allows accurate predictions of offspring sex ratios in many species, but the mechanisms by which sex allocation is controlled are poorly understood. Using previously published data, we investigated whether alternative splicing, combined with differential gene expression, was involved with sex allocation in the parasitoid wasp, <i>Nasonia vitripennis</i>. We f ...[more]

PMID: 32760522

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Project description:Linking behavioural phenotypes to their underlying genotypes is crucial for uncovering the mechanisms that underpin behaviour and for understanding the origins and maintenance of genetic variation in behaviour. Recently, interest has begun to focus on the transcriptome as a route for identifying genes and gene pathways associated with behaviour. For many behavioural traits studied at the phenotypic level, we have little or no idea of where to start searching for "candidate" genes: the transcriptome provides such a starting point. Here we consider transcriptomic changes associated with oviposition in the parasitoid wasp Nasonia vitripennis. Oviposition is a key behaviour for parasitoids, as females are faced with a variety of decisions that will impact offspring fitness. These include choosing between hosts of differing quality, as well as making decisions regarding clutch size and offspring sex ratio. We compared the whole-body transcriptomes of resting or ovipositing female Nasonia using a "DeepSAGE" gene expression approach on the Illumina sequencing platform. We identified 332 tags that were significantly differentially expressed between the two treatments, with 77% of the changes associated with greater expression in resting females. Oviposition therefore appears to focus gene expression away from a number of physiological processes, with gene ontologies suggesting that aspects of metabolism may be down-regulated during egg-laying. Nine of the most abundant differentially expressed tags showed greater expression in ovipositing females though, including the genes purity-of-essence (associated with behavioural phenotypes in Drosophila) and glucose dehydrogenase (GLD). The GLD protein has been implicated in sperm storage and release in Drosophila and so provides a possible candidate for the control of sex allocation by female Nasonia during oviposition. Oviposition in Nasonia therefore clearly modifies the transcriptome, providing a starting point for the genetic dissection of oviposition.

Project description:Background The generalist dipteran pupal parasitoid Nasonia vitripennis injects 79 venom peptides into the host before egg laying. This venom induces several important changes in the host, including developmental arrest, immunosuppression, and alterations to normal metabolism. It is hoped that diverse and potent bioactivities of N. vitripennis venom provide an opportunity for the design of novel acting drugs. However, currently very little is known about the individual functions of N. vitripennis venom peptides and less than half can be bioinformatically annotated. The paucity of annotation information complicates the design of studies that seek to better understand the potential mechanisms underlying the envenomation response. Although the RNA interference system of N. vitripennis provides an opportunity to functionally characterise venom encoding genes, with 79 candidates this represents a daunting task. For this reason we were interested in determining the expression levels of venom encoding genes in the venom gland, such that this information could be used to rank candidate venoms. To do this we carried out deep sequencing of the transcriptome of the venom gland and neighbouring ovary tissue and used RNA-seq to measure expression from the 79 venom encoding genes. The generation of a specific venom gland transcriptome dataset also provides further opportunities to investigate novel features of this highly specialised organ. Results High throughput sequencing and RNA-seq revealed that the highest expressed venom encoding gene in the venom gland was a serine protease called Nasvi2EG007167, which has previously been implicated in the apoptotic activity of N. vitripennis venom. As expected the RNA-seq confirmed that the N. vitripennis venom encoding genes are almost exclusively expressed in the venom gland relative to the neighbouring ovary tissue. Novel peptides appear to perform key roles in N. vitripennis venom function as only four of the highest 15 expressed venom encoding genes are bioinformatically annotationed. The high throughput sequencing data also provided evidence for the existence of an additional 471 novel genes in the Nasonia genome that are expressed in the venom gland and ovary. Finally, metagenomic analysis of venom gland transcripts identified viral transcripts that may play an important part in the N. vitripennis venom function. Conclusions The expression level information provided here for the 79 venom encoding genes provides an unbiased dataset that can be used by the N. vitripennis community to identify high value candidates for further functional characterisation. These candidates represent bioactive peptides that have value in drug development pipelines.

Project description:For many behaviours studied at the phenotypic level, we have little or no idea of where to start searching for “candidate” genes: the transcriptome provides such a starting point. Here we consider transcriptomic changes associated with oviposition in the parasitoid wasp Nasonia vitripennis. Oviposition is a key behaviour, as females are faced with a variety of decisions that will impact offspring fitness. These include choosing between hosts of differing quality, as well as deciding on clutch size and offspring sex ratio. We compared the whole-body transcriptomes of resting or ovipositing female Nasonia using a “DEEP-Sage” gene expression approach on the Illumina sequencing platform. Single 2-day old mated Nasonia vitripennis females (ASymC strain) were isolated in a glass vial and provided with a single host to produce F1 daughters. Eight 2-day old mated F1 females were subsequently provided with three hosts to produce the F2 test females. We randomly selected one host from each F1 female, and isolated 16 2-day old mated F2 test females in glass tubes, of which eight were randomly allocated to the oviposition treatment and eight to the resting treatment. We provided the test females with a single host for 24 hours as pre-treatment to facilitate egg development. We then discarded the pre-treatment hosts and gave each female a piece of chromatography paper soaked in honey solution for a further 24 hours. For the experiment, we transferred the females to 1.5 mL Eppendorf tubes that contained a single host for the oviposition experiment, or were empty for the resting treatment. After 60 mins, females were flash-frozen in liquid nitrogen and stored on dry-ice until the addition of RNAlater-ICE (Ambion, Austin, TX, USA) after which they were transferred to -20C. All females in the oviposition treatment were observed to have commenced ovipositing. We pooled the F2 test females from each F1 mother according to treatment, generating a total of eight pooled samples per treatment (consisting of 8 females per pool) for RNA isolation and sequencing.

Dataset Information

Evidence of capacitation in the parasitoid wasp, Nasonia vitripennis, and its potential role in sex allocation.

Publications

Evidence of capacitation in the parasitoid wasp, <i>Nasonia vitripennis,</i> and its potential role in sex allocation.

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