Abstract
We present a genome assembly from an individual female Acrocera orbiculus (the Top-horned Hunchback fly; Arthropoda; Insecta; Diptera; Acroceridae). The genome sequence is 221.0 megabases in span. Most of the assembly is scaffolded into 5 chromosomal pseudomolecules, including the X sex chromosome. The mitochondrial genome has also been assembled and is 18.67 kilobases in length. Gene annotation of this assembly on Ensembl identified 10,439 protein coding genes.
Keywords: Acrocera orbiculus, Top-horned Hunchback fly, genome sequence, chromosomal, Diptera
Species taxonomy
Eukaryota; Opisthokonta; Metazoa; Eumetazoa; Bilateria; Protostomia; Ecdysozoa; Panarthropoda; Arthropoda; Mandibulata; Pancrustacea; Hexapoda; Insecta; Dicondylia; Pterygota; Neoptera; Endopterygota; Diptera; Brachycera; Muscomorpha; Nemestrinoidea; Acroceridae; Acrocera; Acrocera orbiculus (Fabricius, 1787) (NCBI:txid210248).
Background
Acrocera orbiculus (Fabricius, 1787), the Top-horned Hunchback fly, is one of three species of Acroceridae found in the UK, but globally there are around 530 species placed within 55 genera ( Stubbs & Drake, 2014). Acrocera is a cosmopolitan genus spanning the Holarctic but most frequently sampled in western Palaearctic ( Kehlmaier & Almeida, 2014).
The adults are small (body length 3–6.56 mm, wing length 3.5–4.5 mm) and are globular, with a shape that is often described as ‘dumpy’. The head is very small and round with the diagnostic features of the genus being that the stylate antennae are positioned on top of the head, the eyes lack hair, and both mouthparts and wing venation are reduced ( Stubbs & Drake, 2014). They have well developed squamae (calypters) and are very good flyers, although not often seen due in some part to the very short emergence period (thought to be only a few days) ( Schlinger, 1987).
Acrocera orbiculus are commonly called hunchback flies, small-headed flies or spider-killing flies. The latter name indicates the host preference of their larvae: all Acrocera species have larvae which are parasitoids of spiders. The adults congregate for mating and oval eggs are laid on vegetation directly afterwards in clusters of several hundred ( Edwards, 1984).
After three to six weeks and usually at night, the first instar (stage) of the larva emerges. This is a specialised instar called a planidium. It is tiny (0.3–0.4 mm), and actively crawls to search out a host. Upon finding one it attaches itself by its mouthpart to the legs and stays there. Acrocerid larva then undergo hypermetamorphosis, changing into a functionally and morphologically different larval phase as an endoparasite ( Schlinger, 1987). Host records are few, but Kehlmaier and Almeida (2014) list three families within which rearing has been recorded (Amaurobiidae, Clubionidae and Lycosidae). The first instar cuts through the integument and is thought to feed directly on the haemolymph of its host ( Overgaard Nielsen et al., 1999). After a week the first moulting occurs, and it is during this period that the second, more flexible, instar injects itself into the host via the original oral cavity and host wound, leaving the original exuviae as a plug ( Overgaard Nielsen et al., 1999; Toft et al., 2012). The second instar, now an endoparasite, travels through the lymph up through to the abdomen where it resides near the booklungs of the spider, growing in size till the final (fourth) instar. The mature larvae leave the host at this stage to pupate, which results in the death of the spider. Waste material is evacuated from the body pre-pupation and from host to the adult fly emerging has been recorded as just over two weeks ( Kehlmaier & Almeida, 2014).
In the UK this species has a threat status of Least Concern and a rarity status of Nationally Scarce ( Drake, 2017). Data held by the national recording scheme for soldierflies and allies includes records from 42 vice-counties, widely scattered from South Devon northwards to Stirlingshire; it is more frequently seen in the southern parts of its range (and is also known from the Channel Islands) (Martin Harvey, pers. comm.).
Previous molecular analysis of the COI-dataset has been undertaken to help determine whether this species was in fact a complex, as suggested by the variable abdominal pattern found across the range. The findings of Kehlmaier and Almeida (2014) suggest that this is a single species, albeit with a high degree of variation in size, colouration, and some sexual dimorphism.
The genome of the Top-horned Hunchback fly, Acrocera orbiculus, was sequenced as part of the Darwin Tree of Life Project, a collaborative effort to sequence all named eukaryotic species in the Atlantic Archipelago of Britain and Ireland.
Genome sequence report
The genome was sequenced from one female Acrocera orbiculus ( Figure 1) collected from Wytham Woods, Oxfordshire, UK (51.77, –1.34). A total of 104-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 4 missing joins or mis-joins and removed one haplotypic duplication.
Figure 1.
Photographs of the Acrocera orbiculus (idAcrOrbc1) specimen used for genome sequencing a) Live specimen b) Specimen during preservation and processing.
The final assembly has a total length of 221.0 Mb in 73 sequence scaffolds with a scaffold N50 of 63.1 Mb ( Table 1). The snailplot 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 (99.99%) of the assembly sequence was assigned to 5 chromosomal-level scaffolds, representing 4 autosomes and the X sex chromosome. Chromosome-scale scaffolds confirmed by the Hi-C data are named in order of size ( Figure 5; Table 2). The size of the rRNA clusters on chromosome X is not exact and additional rRNA sequences are in the unlocalised sequences for X. The observed genotype is 4+XX, but the coverage on the repetitive allosome is very unequal. While not fully phased, the assembly deposited is of one haplotype. Contigs corresponding to the second haplotype have also been deposited. The mitochondrial genome was also assembled and can be found as a contig within the multifasta file of the genome submission.
Figure 2. Genome assembly of Acrocera orbiculus, idAcrOrbc1.1: metrics.
The BlobToolKit Snailplot 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 221,032,551 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 (70,384,342 bp, shown in red). Orange and pale-orange arcs show the N50 and N90 scaffold lengths (63,123,693 and 29,288,000 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 diptera_odb10 set is shown in the top right. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CANAHR01/dataset/CANAHR01/snail.
Figure 3. Genome assembly of Acrocera orbiculus, idAcrOrbc1.1: BlobToolKit GC-coverage plot.
Scaffolds are coloured by phylum. Circles are sized in proportion to scaffold length. Histograms show the distribution of scaffold length sum along each axis. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CANAHR01/dataset/CANAHR01/blob.
Figure 4. Genome assembly of Acrocera orbiculus, idAcrOrbc1.1: BlobToolKit cumulative sequence plot.
The grey line shows cumulative length for all scaffolds. Coloured lines show cumulative lengths of scaffolds assigned to each phylum using the buscogenes taxrule. An interactive version of this figure is available at https://blobtoolkit.genomehubs.org/view/CANAHR01/dataset/CANAHR01/cumulative.
Figure 5. Genome assembly of Acrocera orbiculus, idAcrOrbc1.1: Hi-C contact map of the idAcrOrbc1.1 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=LcDi2s4OSM-GkorzPMxP3w.
Table 1. Genome data for Acrocera orbiculus, idAcrOrbc1.1.
| Project accession data | ||
|---|---|---|
| Assembly identifier | idAcrOrbc1.1 | |
| Species | Acrocera orbiculus | |
| Specimen | idAcrOrbc1 | |
| NCBI taxonomy ID | 210248 | |
| BioProject | PRJEB55974 | |
| BioSample ID | SAMEA7701562 | |
| Isolate information | idAcrOrbc1 | |
| Assembly metrics * | Benchmark | |
| Consensus quality (QV) | 65.8 | ≥ 50 |
| k-mer completeness | 100.0% | ≥ 95% |
| BUSCO ** | C:91.6%[S:90.7%,D:1.0%],
F:1.9%,M:6.5%,n:3,285 |
C ≥ 95% |
| Percentage of assembly mapped to
chromosomes |
99.99% | ≥ 95% |
| Sex chromosomes | X | localised homologous pairs |
| Organelles | Mitochondrial genome: 18.67 kb | complete single alleles |
| Raw data accessions | ||
| PacificBiosciences SEQUEL II | ERR10224913 | |
| Hi-C Illumina | ERR10297810 | |
| PolyA RNA-Seq Illumina | ERR10378032 | |
| Genome assembly | ||
| Assembly accession | GCA_947359355.1 | |
| Accession of alternate haplotype | GCA_947359395.1 | |
| Span (Mb) | 221.0 | |
| Number of contigs | 76 | |
| Contig N50 length (Mb) | 63.1 | |
| Number of scaffolds | 73 | |
| Scaffold N50 length (Mb) | 63.1 | |
| Longest scaffold (Mb) | 70.38 | |
| Genome annotation | ||
| Number of protein-coding genes | 10,439 | |
| Number of non-coding genes | 1,292 | |
| Number of gene transcripts | 19,199 | |
* 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 diptera_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/CANAHR01/dataset/CANAHR01/busco.
Table 2. Chromosomal pseudomolecules in the genome assembly of Acrocera orbiculus, idAcrOrbc1.
| INSDC
accession |
Chromosome | Length
(Mb) |
GC% |
|---|---|---|---|
| OX375756.1 | 1 | 70.38 | 27.5 |
| OX375757.1 | 2 | 63.12 | 27.5 |
| OX375758.1 | 3 | 47.32 | 28.0 |
| OX375759.1 | 4 | 29.29 | 26.0 |
| OX375760.1 | X | 4.76 | 22.0 |
| OX375761.1 | MT | 0.02 | 18.5 |
The estimated Quality Value (QV) of the final assembly is 65.8 with k-mer completeness of 100.0%, and the assembly has a BUSCO v5.3.2 completeness of 91.6% (single = 90.7%, duplicated = 1.0%), using the diptera_odb10 reference set ( n = 3,285).
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/210248.
Genome annotation report
The Acrocera orbiculus genome assembly (GCA_947359355.1) was annotated using the Ensembl rapid annotation pipeline ( Table 1; https://rapid.ensembl.org/Acrocera_orbiculus_GCA_947359355.1/Info/Index). The resulting annotation includes 19,199 transcribed mRNAs from 10,439 protein-coding and 1,292 non-coding genes.
Methods
Sample acquisition and nucleic acid extraction
A female Acrocera orbiculus (specimen ID Ox000701, ToLID idAcrOrbc1), which was used for genome sequencing, was collected from Wytham Woods, Oxfordshire (biological vice-county Berkshire), UK (latitude 51.77, longitude –1.34) on 2020-07-24 by potting. The specimen used for Hi-C sequencing (specimen ID Ox001583, ToLID idAcrOrbc2) was collected from the same location on 2021-07-14. The specimens were collected and identified by Liam Crowley (University of Oxford) and preserved on dry ice.
The specimen used for RNA sequencing (specimen ID NHMUK014561630, ToLID idAcrOrbc3) was collected from South Ockendon, UK (latitude 51.51, longitude 0.29) on 2021-07-25. The specimen was collected by Neil Phillips (Dipterists Forum) and identified by Ed Hardy (Dipterists Forum).
Protocols developed by the Wellcome Sanger Institute (WSI) Tree of Life core laboratory have been deposited on protocols.io ( Denton et al., 2023b). The workflow for high molecular weight (HMW) DNA extraction at the WSI includes a sequence of core procedures: sample preparation; sample homogenisation, DNA extraction, fragmentation, and clean-up. In sample preparation, the idAcrOrbc1 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 using the Automated MagAttract v1 protocol ( Sheerin et al., 2023). HMW DNA was sheared into an average fragment size of 12–20 kb in a Megaruptor 3 system with speed setting 30 ( Todorovic 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.
RNA was extracted from whole organism tissue of idAcrOrbc3 in the Tree of Life Laboratory at the WSI using the RNA Extraction: Automated MagMax™ mirVana protocol ( do Amaral et al., 2023). The RNA concentration was assessed using a Nanodrop spectrophotometer and a Qubit Fluorometer using the Qubit RNA Broad-Range Assay kit. Analysis of the integrity of the RNA was done using the Agilent RNA 6000 Pico Kit and Eukaryotic Total RNA assay.
Sequencing
Pacific Biosciences HiFi circular consensus DNA sequencing libraries were constructed according to the manufacturers’ instructions. Poly(A) RNA-Seq libraries were constructed using the NEB Ultra II RNA Library Prep kit. DNA and RNA sequencing was performed by the Scientific Operations core at the WSI on Pacific Biosciences SEQUEL II (HiFi) and Illumina NovaSeq 6000 (RNA-Seq) instruments. Hi-C data were also generated from whole organism tissue of idAcrOrbc2 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) and haplotypic duplication was identified and removed with purge_dups ( Guan et al., 2020). 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 using the gEVAL system ( Chow et al., 2016) as described previously ( Howe et al., 2021). Manual curation was performed using gEVAL, HiGlass ( Kerpedjiev et al., 2018) and Pretext ( Harry, 2022). The mitochondrial genome was assembled using MitoHiFi ( Uliano-Silva et al., 2023), which runs MitoFinder ( Allio et al., 2020) or MITOS ( Bernt et al., 2013) and uses these annotations to select the final mitochondrial contig and to ensure the general quality of the sequence.
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 | 4.1.7 | https://github.com/blobtoolkit/blobtoolkit |
| BUSCO | 5.3.2 | https://gitlab.com/ezlab/busco |
| gEVAL | N/A | https://geval.org.uk/ |
| Hifiasm | 0.16.1-r375 | https://github.com/chhylp123/hifiasm |
| HiGlass | 1.11.6 | https://github.com/higlass/higlass |
| Merqury | MerquryFK | https://github.com/thegenemyers/MERQURY.FK |
| MitoHiFi | 2 | https://github.com/marcelauliano/MitoHiFi |
| PretextView | 0.2 | https://github.com/wtsi-hpag/PretextView |
| purge_dups | 1.2.3 | https://github.com/dfguan/purge_dups |
| 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 | yahs-1.1.91eebc2 | https://github.com/c-zhou/yahs |
Genome annotation
The Ensembl gene annotation system ( Aken et al., 2016) was used to generate annotation for the Acrocera orbiculus assembly (GCA_947359355.1). Annotation was created primarily through alignment of transcriptomic data to the genome, with gap filling via protein-to-genome alignments of a select set of proteins from UniProt ( UniProt Consortium, 2019).
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.
Acknowledgements
EM would like to thank Martin Harvey from the Soldierflies and Allies Recording Scheme for helpful input.
Funding Statement
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.
[version 1; peer review: 2 approved]
Data availability
European Nucleotide Archive: Acrocera orbiculus (top-horned hunchback). Accession number PRJEB55974; https://identifiers.org/ena.embl/PRJEB55974 ( Wellcome Sanger Institute, 2022). The genome sequence is released openly for reuse. The Acrocera orbiculus 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. Raw data and assembly accession identifiers are reported in Table 1.
Author information
Members of the University of Oxford and Wytham Woods Genome Acquisition Lab are listed here: https://doi.org/10.5281/zenodo.7125292.
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.
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