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Wellcome Open Res
Wellcome Open Res
Wellcome Open Research
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10.12688/wellcomeopenres.21215.1
Data Note
Articles
The genome sequence of an ichneumonid wasp, Oxytorus armatus Thomson, 1883
[version 1; peer review: 2 approved]

Broad Gavin R. Investigation Resources Writing – Original Draft Preparation Writing – Review & Editing https://orcid.org/0000-0001-7223-5333
1
Fletcher Chris Investigation Resources https://orcid.org/0000-0002-1944-5048
1
Januszczak Inez Investigation Resources https://orcid.org/0000-0003-3857-9989
1
Natural History Museum Genome Acquisition Lab
Darwin Tree of Life Barcoding collective
Wellcome Sanger Institute Tree of Life Management, Samples and Laboratory team
Wellcome Sanger Institute Scientific Operations: Sequencing Operations
Wellcome Sanger Institute Tree of Life Core Informatics team
Tree of Life Core Informatics collective
Darwin Tree of Life Consortiuma
1 Natural History Museum, London, England, UK
a mark.blaxter@sanger.ac.uk
No competing interests were disclosed.

12 4 2024
2024
9 19015 3 2024
Copyright: © 2024 Broad GR et al.
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

We present a genome assembly from an individual male Oxytorus armatus (an ichneumonid wasp; Arthropoda; Insecta; Hymenoptera; Ichneumonidae). The genome sequence is 367.8 megabases in span. Most of the assembly is scaffolded into 13 chromosomal pseudomolecules. The mitochondrial genome has also been assembled and is 56.22 kilobases in length.

Oxytorus armatus
ichneumonid wasp
genome sequence
chromosomal
Hymenoptera
Wellcome Trust218328 206194 This work was supported by Wellcome through core funding to the Wellcome Sanger Institute (206194) and the Darwin Tree of Life Discretionary Award (218328). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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pmcSpecies taxonomy

Eukaryota; Opisthokonta; Metazoa; Eumetazoa; Bilateria; Protostomia; Ecdysozoa; Panarthropoda; Arthropoda; Mandibulata; Pancrustacea; Hexapoda; Insecta; Dicondylia; Pterygota; Neoptera; Endopterygota; Hymenoptera; Apocrita; Ichneumonoidea; Ichneumonidae; Oxytorinae; Oxytorus; Oxytorus armatus Thomson, 1883 (NCBI:txid495374).

Background

Oxytorus armatus is a widespread ichneumonid wasp. Females are rather distinctive as they have white-striped antennae, small projections on the propodeum (apophyses), a long and posteriorly compressed metasoma (the abdomen beyond the first segment), and short, wide ovipositor sheaths. The only other European (including British) species of Oxytorus, O. luridator, can be separated most easily by its much smaller apophyses, closed areolet in the fore wing, and shorter metasoma. Males are very similar but can usually be separated by the absence of the areolet in O. armatus and the rougher, more ‘leathery’ sculpture on the second metasomal tergite. Kerrich (1939) and van Rossem (1987) provide some notes on identification. The main problem in identifying males of Oxytorus is in recognising that they are oxytorines. The subfamily Oxytorinae comprises the single genus Oxytorus, which is defined by some distinctive features such as the female metasoma shape, the flattened clypeus and the exceptionally long maxillary palps. Males, however, look rather indistinct and are often passed over as specimens of Ctenopelmatinae, Cryptinae or Phygadeuontinae.

Based on specimens in museum collections, especially light-trapped individuals identified by GRB, adults are active from June to early September, most commonly in June and July. Oxytorus armatus has a wide range across Europe, as does O. luridator, although O. luridator is perhaps the more commonly collected of the two. Usually found in deciduous woodland, we know very little about the ecology of O. armatus. As with O. luridator, males are frequently attracted to light so are presumably at least partly nocturnal or crepuscular. In fact, the small subfamily Oxytorinae is one of only three ichneumonid subfamilies entirely lacking host records. Oxytorinae is the most species-rich of those three, with 25 described species and several undescribed species found across both temperate and tropical areas of Asia, Europe and the Americas ( Broad et al., 2018; Riedel et al., 2021). As pointed out by Wahl (1990), when classifying Oxytorus in their own subfamily, the short ovipositor of Oxytorus has a subapical notch, which means they will be endoparasitoids of larvae.

In the few large-scale phylogenetic studies which have included Oxytorus ( Bennett et al., 2019; Quicke et al., 2009; Sharanowski et al., 2021), they have been found to be part of a grouping called the ‘ophioniformes’, and part of a very large clade which are invariably koinobiont endoparasitoids of holometabolous insect larvae, i.e., the host develops further following oviposition, with the wasp larva feeding internally. Oxytorus might be closely related to some of the groups of sawfly parasitoids currently classified as Ctenopelmatinae, which are not monophyletic Oxytorus ( Bennett et al., 2019; Quicke et al., 2009; Sharanowski et al., 2021), but are all parasitoids of sawfly (Hymenoptera) larvae. It is conceivable that Oxytorus will be found to be parasitoids of sawfly larvae, but it is striking that while the larvae of many northern European sawfly species have been reared, Oxytorus never has. The metasoma adaptations, and the fact that females seem to stay near ground level ( Broad et al., 2018) suggests that the hosts will be concealed in loose, or easily penetrated substrate. The availability of a genome will help to pin down the affinities of this enigmatic group of Darwin Wasps, and hopefully spur efforts to rear these wasps.

Genome sequence report

The genome was sequenced from one male Oxytorus armatus ( Figure 1) collected from Bert’s Pheasant Pen, Wytham Woods, Oxfordshire, UK (51.77, –1.31). A total of 62-fold coverage in Pacific Biosciences single-molecule HiFi long reads was generated. Primary assembly contigs were scaffolded with chromosome conformation Hi-C data. Manual assembly curation corrected 35 missing joins or mis-joins, reducing the scaffold number by 26.42%, and increasing the scaffold N50 by 0.66%.

Figure 1. Photographs of the Oxytorus armatus (iyOxyArmt1) specimen used for genome sequencing.

The final assembly has a total length of 367.8 Mb in 38 sequence scaffolds with a scaffold N50 of 31.2 Mb ( Table 1). The snail plot in Figure 2 provides a summary of the assembly statistics, while the distribution of assembly scaffolds on GC proportion and coverage is shown in Figure 3. The cumulative assembly plot in Figure 4 shows curves for subsets of scaffolds assigned to different phyla. Most (99.98%) of the assembly sequence was assigned to 13 chromosomal-level scaffolds. The genome is of a haploid male specimen. Chromosome-scale scaffolds confirmed by the Hi-C data are named in order of size ( Figure 5; Table 2). The mitochondrial genome was also assembled and can be found as a contig within the multifasta file of the genome submission.

Table 1. Genome data for Oxytorus armatus, iyOxyArmt1.1.

Project accession data	
Assembly identifier	iyOxyArmt1.1	
Species	Oxytorus armatus	
Specimen	iyOxyArmt1	
NCBI taxonomy ID	495374	
BioProject	PRJEB61495	
BioSample ID	SAMEA14448319	
Isolate information	iyOxyArmt1, male (DNA and Hi-C sequencing)	
Assembly metrics *	Benchmark	
Consensus quality (QV)	67.8	≥ 50	
k-mer completeness	100.0%	≥ 95%	
BUSCO **	C:95.3%[S:94.9%,D:0.4%],
F:1.3%,M:3.4%,n:5,991	C ≥ 95%	
Percentage of assembly
mapped to chromosomes	99.98%	≥ 95%	
Sex chromosomes	None	localised homologous pairs	
Organelles	Mitochondrial genome:
56.22 kb	complete single alleles	
Raw data accessions	
PacificBiosciences SEQUEL II	ERR11263498	
Hi-C Illumina	ERR11271517	
Genome assembly	
Assembly accession	GCA_958009045.1	
Span (Mb)	367.8	
Number of contigs	357	
Contig N50 length (Mb)	2.0	
Number of scaffolds	38	
Scaffold N50 length (Mb)	31.2	
Longest scaffold (Mb)	43.48	
* Assembly metric benchmarks are adapted from column VGP-2020 of “Table 1: Proposed standards and metrics for defining genome assembly quality” from Rhie et al. (2021).

** BUSCO scores based on the hymenoptera_odb10 BUSCO set using version 5.3.2. C = complete [S = single copy, D = duplicated], F = fragmented, M = missing, n = number of orthologues in comparison. A full set of BUSCO scores is available at https://blobtoolkit.genomehubs.org/view/iyOxyArmt1_1/dataset/iyOxyArmt1_1/busco.

Figure 2. Genome assembly of Oxytorus armatus, iyOxyArmt1.1: metrics.

The BlobToolKit snail plot shows N50 metrics and BUSCO gene completeness. The main plot is divided into 1,000 size-ordered bins around the circumference with each bin representing 0.1% of the 367,853,913 bp assembly. The distribution of scaffold lengths is shown in dark grey with the plot radius scaled to the longest scaffold present in the assembly (43,478,420 bp, shown in red). Orange and pale-orange arcs show the N50 and N90 scaffold lengths (31,210,731 and 19,609,202 bp), respectively. The pale grey spiral shows the cumulative scaffold count on a log scale with white scale lines showing successive orders of magnitude. The blue and pale-blue area around the outside of the plot shows the distribution of GC, AT and N percentages in the same bins as the inner plot. A summary of complete, fragmented, duplicated and missing BUSCO genes in the hymenoptera_odb10 set is shown in the top right. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/iyOxyArmt1_1/dataset/iyOxyArmt1_1/snail.

Figure 3. Genome assembly of Oxytorus armatus, iyOxyArmt1.1: BlobToolKit GC-coverage plot.

Sequences are coloured by phylum. Circles are sized in proportion to sequence length. Histograms show the distribution of sequence length sum along each axis. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/iyOxyArmt1_1/dataset/iyOxyArmt1_1/blob.

Figure 4. Genome assembly of Oxytorus armatus, iyOxyArmt1.1: BlobToolKit cumulative sequence plot.

The grey line shows cumulative length for all sequences. Coloured lines show cumulative lengths of sequences assigned to each phylum using the buscogenes taxrule. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/iyOxyArmt1_1/dataset/iyOxyArmt1_1/cumulative.

Figure 5. Genome assembly of Oxytorus armatus, iyOxyArmt1.1: Hi-C contact map of the iyOxyArmt1.1 assembly, visualised using HiGlass.

Chromosomes are shown in order of size from left to right and top to bottom. An interactive version of this figure may be viewed at https://genome-note-higlass.tol.sanger.ac.uk/l/?d=QG7ssJ0OSkGxmzq4ZBVN8A.

Table 2. Chromosomal pseudomolecules in the genome assembly of Oxytorus armatus, iyOxyArmt1.

INSDC
accession	Chromosome	Length
(Mb)	GC%	
OY253744.1	1	43.48	37.5	
OY253745.1	2	39.08	38.0	
OY253746.1	3	36.46	37.5	
OY253747.1	4	34.94	37.0	
OY253748.1	5	31.21	38.0	
OY253749.1	6	27.47	38.0	
OY253750.1	7	28.59	37.5	
OY253751.1	8	27.05	38.0	
OY253752.1	9	25.44	37.0	
OY253753.1	10	19.94	37.5	
OY253754.1	11	19.61	37.5	
OY253755.1	12	17.39	37.0	
OY253756.1	13	15.67	37.5	
OY253757.1	MT	0.06	11.5	

The estimated Quality Value (QV) of the final assembly is 67.8 with k-mer completeness of 100.0%, and the assembly has a BUSCO v5.3.2 completeness of 95.3% (single = 94.9%, duplicated = 0.4%), using the hymenoptera_odb10 reference set ( n = 5,991).

Metadata for specimens, barcode results, spectra estimates, sequencing runs, contaminants and pre-curation assembly statistics are given at https://links.tol.sanger.ac.uk/species/495374.

Methods

Sample acquisition and nucleic acid extraction

A male Oxytorus armatus (specimen ID NHMUK014451573, ToLID iyOxyArmt1) was collected from Wytham Woods, Bert's Pheasant Pen, Wytham Woods, Oxfordshire (biological vice-county Berkshire), UK (latitude 51.77, longitude –1.31) on 2021-09-02, using an aerial net. The specimen was collected by Gavin Broad, Chris Fletcher and Inez Januszczak (Natural History Museum) and identified by Gavin Broad, and then preserved by dry freezing at –80 °C.

The workflow for high molecular weight (HMW) DNA extraction at the Wellcome Sanger Institute (WSI) includes a sequence of core procedures: sample preparation; sample homogenisation, DNA extraction, fragmentation, and clean-up. The sample was prepared for DNA extraction at the WSI Tree of Life Core Laboratory: the iyOxyArmt1 sample was weighed and dissected on dry ice ( Jay et al., 2023). Tissue from the whole organism was homogenised using a PowerMasher II tissue disruptor ( Denton et al., 2023a).

HMW DNA was extracted in the WSI Scientific Operations core using the Automated MagAttract v2 protocol ( Oatley et al., 2023). The DNA was sheared into an average fragment size of 12–20 kb in a Megaruptor 3 system with speed setting 31 ( Bates et al., 2023). Sheared DNA was purified by solid-phase reversible immobilisation ( Strickland et al., 2023): in brief, the method employs a 1.8X ratio of AMPure PB beads to sample to eliminate shorter fragments and concentrate the DNA. The concentration of the sheared and purified DNA was assessed using a Nanodrop spectrophotometer and Qubit Fluorometer and Qubit dsDNA High Sensitivity Assay kit. Fragment size distribution was evaluated by running the sample on the FemtoPulse system.

Protocols developed by the WSI Tree of Life laboratory are publicly available on protocols.io ( Denton et al., 2023b).

Sequencing

Pacific Biosciences HiFi circular consensus DNA sequencing libraries were constructed according to the manufacturers’ instructions. DNA sequencing was performed by the Scientific Operations core at the WSI on a Pacific Biosciences SEQUEL II instrument. Hi-C data were also generated from remaining tissue of iyOxyArmt1 using the Arima2 kit and sequenced on the Illumina NovaSeq 6000 instrument.

Genome assembly, curation and evaluation

Assembly was carried out with Hifiasm ( Cheng et al., 2021). The assembly was then scaffolded with Hi-C data ( Rao et al., 2014) using YaHS ( Zhou et al., 2023). The assembly was checked for contamination and corrected as described previously ( Howe et al., 2021). Manual curation was performed using HiGlass ( Kerpedjiev et al., 2018) and PretextView ( Harry, 2022). The mitochondrial genome was assembled using MitoHiFi ( Uliano-Silva et al., 2023) and OATK ( Zhou, 2023).

A Hi-C map for the final assembly was produced using bwa-mem2 ( Vasimuddin et al., 2019) in the Cooler file format ( Abdennur & Mirny, 2020). To assess the assembly metrics, the k-mer completeness and QV consensus quality values were calculated in Merqury ( Rhie et al., 2020). This work was done using Nextflow ( Di Tommaso et al., 2017) DSL2 pipelines “sanger-tol/readmapping” ( Surana et al., 2023a) and “sanger-tol/genomenote” ( Surana et al., 2023b). The genome was analysed within the BlobToolKit environment ( Challis et al., 2020) and BUSCO scores ( Manni et al., 2021; Simão et al., 2015) were calculated.

Table 3 contains a list of relevant software tool versions and sources.

Table 3. Software tools: versions and sources.

Software tool	Version	Source	
BlobToolKit	4.2.1	https://github.com/blobtoolkit/blobtoolkit	
BUSCO	5.3.2	https://gitlab.com/ezlab/busco	
Hifiasm	0.16.1	https://github.com/chhylp123/hifiasm	
HiGlass	1.11.6	https://github.com/higlass/higlass	
Merqury	MerquryFK	https://github.com/thegenemyers/MERQURY.FK	
MitoHiFi	3.01	https://github.com/marcelauliano/MitoHiFi	
OATK	-	https://github.com/c-zhou/oatk	
PretextView	0.2	https://github.com/wtsi-hpag/PretextView	
sanger-tol/genomenote	v1.0	https://github.com/sanger-tol/genomenote	
sanger-tol/readmapping	1.1.0	https://github.com/sanger-tol/readmapping/tree/1.1.0	
YaHS	1.1a.2	https://github.com/c-zhou/yahs	

Wellcome Sanger Institute – Legal and Governance

The materials that have contributed to this genome note have been supplied by a Darwin Tree of Life Partner. The submission of materials by a Darwin Tree of Life Partner is subject to the ‘Darwin Tree of Life Project Sampling Code of Practice’, which can be found in full on the Darwin Tree of Life website here. By agreeing with and signing up to the Sampling Code of Practice, the Darwin Tree of Life Partner agrees they will meet the legal and ethical requirements and standards set out within this document in respect of all samples acquired for, and supplied to, the Darwin Tree of Life Project.

Further, the Wellcome Sanger Institute employs a process whereby due diligence is carried out proportionate to the nature of the materials themselves, and the circumstances under which they have been/are to be collected and provided for use. The purpose of this is to address and mitigate any potential legal and/or ethical implications of receipt and use of the materials as part of the research project, and to ensure that in doing so we align with best practice wherever possible. The overarching areas of consideration are:

•     Ethical review of provenance and sourcing of the material

•     Legality of collection, transfer and use (national and international)

Each transfer of samples is further undertaken according to a Research Collaboration Agreement or Material Transfer Agreement entered into by the Darwin Tree of Life Partner, Genome Research Limited (operating as the Wellcome Sanger Institute), and in some circumstances other Darwin Tree of Life collaborators.

Data availability

European Nucleotide Archive: Oxytorus armatus. Accession number PRJEB61495; https://identifiers.org/ena.embl/PRJEB61495 ( Wellcome Sanger Institute, 2023). The genome sequence is released openly for reuse. The Oxytorus armatus genome sequencing initiative is part of the Darwin Tree of Life (DToL) project. All raw sequence data and the assembly have been deposited in INSDC databases. The genome will be annotated using available RNA-Seq data and presented through the Ensembl pipeline at the European Bioinformatics Institute. Raw data and assembly accession identifiers are reported in Table 1.

Author information

Members of the Natural History Museum Genome Acquisition Lab are listed here: https://doi.org/10.5281/zenodo.7139035.

Members of the Darwin Tree of Life Barcoding collective are listed here: https://doi.org/10.5281/zenodo.4893703.

Members of the Wellcome Sanger Institute Tree of Life Management, Samples and Laboratory team are listed here: https://doi.org/10.5281/zenodo.10066175.

Members of Wellcome Sanger Institute Scientific Operations: Sequencing Operations are listed here: https://doi.org/10.5281/zenodo.10043364.

Members of the Wellcome Sanger Institute Tree of Life Core Informatics team are listed here: https://doi.org/10.5281/zenodo.10066637.

Members of the Tree of Life Core Informatics collective are listed here: https://doi.org/10.5281/zenodo.5013541.

Members of the Darwin Tree of Life Consortium are listed here: https://doi.org/10.5281/zenodo.4783558.

10.21956/wellcomeopenres.23462.r94872
Reviewer response for version 1
Sun Cheng 1Referee
1 Capital Normal University, Beijing, Beijing, China
7 9 2024 Copyright: © 2024 Sun C
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove
The study presented a chromosome-level genome assembly for a widespread ichneumonid wasp, Oxytorus armatus, using genomic DNAs obtained from one single male. The genome sequence is 367.8 Mb in length, with 13 chromosomal pseudomolecules. The Method of this paper was clear and the Result was reliable. This reference genome will be useful in understanding the evolution and rearing of this wasp.

Are sufficient details of methods and materials provided to allow replication by others?

Yes

Is the rationale for creating the dataset(s) clearly described?

Yes

Are the datasets clearly presented in a useable and accessible format?

Yes

Are the protocols appropriate and is the work technically sound?

Yes

Reviewer Expertise:

insect genome evolution

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

10.21956/wellcomeopenres.23462.r94871
Reviewer response for version 1
Wulff Juan 1Referee https://orcid.org/0000-0002-5773-4684

1 Department of Entomology and Plant Pathology, North Carolina State University, Raleigh, USA
1 9 2024 Copyright: © 2024 Wulff J
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove
The work in general is very good and the method used for sequencing is quite robust. The manuscript is short, but I understand that it is more of a report or short communication than a research paper. This is my fourth time reviewing this type of work for this journal and I always mention the same thing, especially since they are all almost identical, the main weakness of these studies is that the annotation was done using a database without transcriptomes to support gene annotation. However, I must say that given the large scale of this project, obtaining the genomes of closely related species will improve gene annotation. Likewise, the absence of species-specific isoforms will always be a weakness of this study and other similar ones that I have reviewed. Finally, I think that the quality of the genome assembly is very good.

Are sufficient details of methods and materials provided to allow replication by others?

Yes

Is the rationale for creating the dataset(s) clearly described?

Yes

Are the datasets clearly presented in a useable and accessible format?

Yes

Are the protocols appropriate and is the work technically sound?

Yes

Reviewer Expertise:

Biology, Entomology, Molecular biology and Genetics.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.
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