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. 2025 Jan 11;10(2):108–113. doi: 10.1080/23802359.2025.2451201

The complete mitochondrial genome of Scambus vesicarius Ratzeburg (Hymenoptera: ichneumonidae: pimplinae)

Yu-Hao Nie a, Zi-Cong Li b, Hong-Ying Hu a,✉
PMCID: PMC11727046  PMID: 39810974

Abstract

The genomic-level characteristics play a pivotal role as genetic assets for the identification of species and phylogenetic analysis. Here, we sequenced and analyzed the mitochondrial genome of Scambus vesicarius (Ratzeburg), which was first morphologically described in “Die Ichneumonen der Forstinsecten in forstlicher und entomologischer Beziehung.” The motivation for this research arises from the necessity to comprehend the genetic composition and evolutionary history of S. vesicarius, a genus of parasitic wasps with potential agricultural significance, which. The circular genome is 26,103bp in length with an overall base composition of 42.02% for A, 43.71% for T, 8.64% for C, and 5.63% for G. The mitochondrial genome of S. vesicarius contained 13 protein-coding genes that initiated by the ATN codon, 22 transfer RNA genes, two ribosomal RNA genes (rRNAs), and a control region (CR). Phylogenetic analyses using Maximum-likelihood methods supported that S. vesicarius is closely related to Pimpla luctuosa, both of which belong to the subfamily Pimplinae, forming a clade that is sister to other subfamilies of Ichneumonidae. This study provides value not only into the genetic diversity and evolutionary history of S. vesicarius at the mitochondrial level but basic research on parasitic wasp biology and applied efforts in biological control.

Keywords: Scambus vesicarius, Ichneumonidae, mitogenome, phylogeny

Introduction

The study of mitochondrial genomes in insects is particularly significant for Hymenoptera, especially their mitochondrial genomes known for their high A＋T content (Cha et al. 2007), substantial base composition bias (Dowton and Austin 1997), and extensive gene rearrangements (Dowton et al. 2003). The base composition of Ichneumonidae is conserved, and their evolutionary rate is lower compared to other families of parasitic Hymenoptera (Zheng et al. 2022). Ichneumonidae, as known as Darwin wasps, is the largest Hymenopteran family, encompassing 42 extant subfamilies (Yu et al. 2016). The family includes approximately 25,000 described species, with many new species still being discovered (Yu et al. 2016). Scambus Hartig 1838 is a large genus with 149 described species (Yu et al. 2016), most of which are Holarctic in distribution. These species are idiobiont ectoparasitoids or facultative hyperparasitoids of holometabolous insects (Lasalle and Gauld 1991). The host range of Scambus is unusually wide, even for idiobiont parasitoids. Due to their parasitic nature on other insects, many members of this family serve as effective biological control agents against agricultural pests (Bennett 2008; Lotfalizadeh and Mohammadi-Khoramabadi 2021; Zheng et al. 2022), primarily attacking sawflies and parasitizing leaf and stem galls in willow, such as the bean gall caused by Pontania proxima (Kopelke 2003; Kasparyan and Kopelke 2009). This makes them crucial in agriculture and forestry (Shaw 2006). Consequently, the investigation of this group holds immense scientific and economic significance, as researchers aim to develop a well-supported phylogenetic tree to understand the ecology, evolution, and diversification patterns of the Ichneumonidae family (Zheng et al. 2022).

Pimplinae is a globally distributed subfamily of Ichneumonidae, known for its biological diversity and extensively studied (Fitton et al. 1988). This subfamily currently comprises approximately 79 genera (Yu et al. 2016). However, very few complete mitochondrial genomes have been sequenced, annotated, and published for Pimplinae (Tang et al. 2019). Additionally, the International Nucleotide Sequence Database Collaboration (INSDC) has only recorded four gene sequences of S. vesicarius, all from the CO1 gene of mitochondrial DNA (Nyman et al. 2015). Initially classified within the genus Pimpla Fabricius (Ratzeburg 1844), S. vesicarius was reclassified into the genus Scambus Hartig after a detailed morphological comparison with species of both Pimpla and Scambus. (Watanabe 2016). This reclassification, accepted in zoological taxonomy (Cabi 2019), was based solely on morphological features without considering genetic data, The morphological characteristics distinguishing this species from others in the same genus are as follows: In females, there is a somewhat depressed saddle-like area immediately distal to the nodus of the upper valve of the ovipositor, which is bordered laterally by weak carinae. The proximal teeth of the lower valve of the ovipositor are well developed and somewhat produced laterally. The hind tibia is reddish brown and may be slightly darkened subproximally and apically. In males, the fore femur is flattened ventrally. To better understand the mitochondrial genome characteristics and phylogenetic relationships, we sequenced the complete mitochondrial genome of S. vesicarius, the results will be valuable.

Materials and methods

Sample collection and DNA extraction

Specimens of S. vesicarius were collected from the Tajik Autonomous County of Taxkorgan, Xinjiang, China (75°13’41.65"N, 37°46’46.04"E, H: 3094 m) using a sweeping net and malaise trap. Additionally, they emerged from the parasitized host Euura bridgmanii in an artificial climate chamber. Selected specimens were examined and identified under a Nikon SMZ745T stereomicroscope, based on morpho logical characters as described and later confirmed by comparing the DNA barcodes with the GenBank database. The specimens were immediately preserved in 100% alcohol and stored at −20 °C and have been deposited in the Insect Collection of the College of Life Science and Technology at Xinjiang University in Urumqi, Xinjiang, China (ICXU) under voucher number XTS-J2401. For further information, please contact Hong-Ying Hu via email at huhongying@xju.edu.cn. Digital habitus photographs of the specimens were taken with a NIKON D7000 digital camera connected to a Nikon SMZ25 stereomicroscope. Whole genomic DNA was extracted from the female using a DNA extraction kit (TIANamp Genomic DNA Kit, China) following the manufacturer’s protocol (Figure 1).

Figure 1.

Figure 1.

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Adult image of the Scambus vesicarius (Ratzeburg 1844), the main distinguishing morphological characters including: Antennae are approximately 0.75 times the length of the forewings, and the propodeum are short and elevated. In females, the basal claws have large teeth. The ovipositor is covered in dense hairs and is slightly compressed laterally. The most proximal teeth on the lower valve apex typically form an angle of around 30° with its longitudinal axis. The photo of species was taken by the first author Yu-hao Nie in Xinjiang University, Xinjiang, China.

Genome sequencing, assembly and annotation

The DNA sample was sent to Genepioneer Biotechnologies, Ltd. (Nanjing, China) for library construction and sequenced on the Illumina Novaseq 6000 platform. The raw reads were filtered using Fastp v0.23.0 (Chen et al. 2018). The assembly was performed with SPAdes v3.14.1 (Bankevich et al. 2012). The near-source sequence and second-generation assembly results are used as references. Minimap2 (version 2.15-r905) was employed to align third-generation sequencing data to the assembled mitochondrial sequence, resulting in BAM and SAM files. To verify the accuracy of the assembly, Samtools (version 1.16.1) software (Ni et al. 2023), along with Perl language, was utilized to filter out third-generation sequencing data larger than 5000 bp from the SAM file. Canu (master-snapshot) (Koren et al. 2017) was then used for error correction on the filtered third-generation data, obtaining high-quality third-generation sequences. Mummer (v4.0.0beta2) was employed to determine the positional relationship between contigs and fill any gaps. The alignment of second-generation assembly results with third-generation data was used to identify collinearity relationships, based on which third-generation reads were extracted and manually extended.The assembly is completed by utilizing the overlap relationships of third-generation data. The selected third-generation data and the result of assembly were compared by nucmer software, and the plot function was utilized for visualizing collinearity. The structural display confirmed that there were read connections from both ends of the third-generation reads, validating their circular structure. Additionally, Minimap2 (2.15-r905) was also used to calculate coverage depth statistics for the BAM file (minimum depth: 153x; maximum depth: 1544x; average depth: 1277.3x; Supplementary Figure S1).

Pilon v1.23 (Salmela and Rivals 2014) was then applied for polishing, resulting in the final sequence. Additionally, the assembled genome was aligned with the mitochondrial genome of Coelichneumon bivittatus Matsumura, 1912 (MT302534.1.gbk), The mitogenomes were annotated using MITOS (Bernt et al. 2013).

Phylogenetic analysis

To reveal the phylogenetic position of S. vesicarius, we downloaded 15 sequences of the mitochondrial genome from NCBI, including 13 Ichneumonidae species and 2 outgroup species. A total of 16 species, including S. vesicarius (accession number PP971122) were aligned and concatenated using MAFFT software (v7.427 - auto mode) for multiple sequence alignment (Edgar 2004) to infer the phylogenetic relationships among subfamilies. The alignment was then used to construct a maximum-likelihood phylogenetic tree using IQ-Tree (Minh et al. 2020).

Results

Characteristics of S. vesicarius mitogenome

The new mitochondrial genome is circular with a total length of 26,103 bp (Figure 2). It contains 13 protein-coding genes (PCGs), all starting with typical ATN initiation codons: four with ATT (ND1, ND2, ND3, ND5); one with ATA (COX1); one with ATC (ATP8); and seven with ATG (COX2, COX3, ND4, ND6, ND4L, ATP6, CYTB). Eight of the PCGs end with the typical stop codons TAA (ATP6, ATP8, COX3, ND1, ND4, ND5, ND6, ND4L), while five use T as an incomplete termination codon (ND2, ND3, COX1, COX2,CYTB). Among the 22 tRNAs (∼65 bp), tRNA-Ala lacks the dihydrouridine (DHU) arm and cannot form a cloverleaf structure, however, the remaining tRNAs have approximate cloverleaf structures (Supplementary Table S2). This is consistent with the secondary structure of tRNA genes found in other insect mitochondrial genomes (Eimanifar et al. 2017; Zhao et al. 2019; Wang et al. 2020). The two ribosomal RNA genes, 16S ribosomal RNA (l-rRNA) and 12S ribosomal RNA (s-rRNA), are 1,359 bp and 887 bp in size, respectively. Additionally, there is a putative control region rich in A and T, as well as other non-coding regions. Of the 37 genes, 23 are located on the J- strand, including 9 PCGs (COX1, COX2, COX3, ATP6, ATP8, CYTB, ND2, ND3, ND6) and 14 tRNAs (trnI, trnM, trnW, trnL trnD, trnK, trnG, trnA, trnR, trnN, trnSAGN, trnE, trnT, trnSUCN) while the remaining 14 are located on the N-strand. The composition is AT biased (85.73%), comprising 42.02% A, 43.71% T, 8.64% C, and 5.63% G. Strand asymmetry was calculated using the formulae: AT-skew = (A − T)/(A + T) = −0.020; GC-skew = (G − C)/(G + C) = −0.211 (Perna and Kocher 1995).

Figure 2.

Figure 2.

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Circular map of the Scambus vesicarius mitochondrial genome. Different colors indicate different types of genes and regions.

Phylogenetic relationships

Phylogenetic relationships among subfamilies of Ichneumonidae were inferred using maximum-likelihood methods, with the best-fitting model determined by ModelFinder (Kalyaanamoorthy et al. 2017) as GTR+F + R5. The values on the nodes represent maximum-likelihood bootstrap support. * represents the newly sequenced mitochondrial genome in this study. Mitochondrial gene sequences obtained from NCBI were used to construct the phylogenetic tree (Supplementary Table S1). The results showed that all the mitochondrial gene sequences used for tree construction, except for the outgroup, clustered into five groups. Maximum-likelihood analyses supported the close relationships among Pimpliformes, Xoridiformes, and Ichneumoniformes. These results are consistent with previous studies based on both morphological classification and molecular phylogenetics (Watanabe 2016; Zheng et al. 2022). The widely accepted topology of ((Pimpliformes + Ichneumoniformes) + Ophioniformes) is supported by study as well as others (Belshaw and Quicke 2002; Bennett et al. 2019; Klopfstein et al. 2019; Sharanowski et al. 2021). Brachycyrtiformes was found to be sister to the rest of the ichneumonids (Zheng et al. 2022), and Xoridiformes was sister to Pimpliformes according to our results (Figure 3).

Figure 3.

Figure 3.

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The maximum-likelihood (ML) phylogenetic tree of Ichneumonidae based on concatenated 16 mitochondrial protein-coding genes. All species involved in the tree have scientific names with accession number on right side, * represents the newly sequenced mitochondrial genome in this study. The complete mitochondrial sequences and accession ID were used as follows: Aphidius gifuensis NC054223; Aphidius colemani OP661166; Xorides funiuensis MT252851 (Zheng et al. 2022); Odontocolon albotibiale MT252850 (Zheng et al. 2022); Megarhyssa sp. MT755629; Pimpla luctuosa MG923506 (Tang et al. 2019); Scambus vesicarius PP971122; Hidryta fusiventris MT302536; Gotra octocincta OP850580; Enclisis macilenta MT302538; Coelichneumon bivittatus MT302534; Diadromus collaris JX131613 (Li et al. 2015); Diadegma semiclausum EU871947; Venturia canescens FJ478176; Euceros serricornis MT252853 (Zheng et al. 2022); Euceros kiushuensis MT252852 (Zheng et al. 2022).

Discussion and conclusion

We have successfully sequenced the complete mitogenome of S. vesicarius for the first time, utilizing high-throughput and third-generation sequencing with Oxford Nanopore technology. The mitogenome, measuring 26,103 base pairs, retains the same gene orientation and order across all 37 genes as observed in other Ichneumonidae species (Cha et al. 2007; Eimanifar et al. 2017; Zhao et al. 2019). Chen validated the three primary high-level groupings proposed by early scholars based on morphological characteristics (Ichneumoniformes, Ophioniformes, Pimpliformes). Through comparative mitogenomics of 104 mitochondrial genomes of Ichneumonidae, five higher-level groupings of Ichneumonidae were proposed and confirmed: Brachycyrtiformes, Ichneumoniformes, Ophioniformes, Pimpliformes, and Xoridiformes (Zheng et al. 2022). The findings of this study also support this high-level grouping classification method.

The results of this study indicate a close phylogenetic relationship between Scambus and Pimpla genera. This finding also supports the reclassification of Scambus vesicarius from Pimpla to Scambus based on morphological classification (Watanabe 2016). Therefore, this study confirms previous morphological classifications within the context of animal taxonomy research.

Approximately 25,000 species have been described in the family Ichneumonidae (Yu et al. 2016), only a limited number of fewer than 150 complete mitochondrial genomes have been deposited in the GenBank database. In this study, we successfully assembled and annotated the entire mitochondrial genome of S. vesicarius, providing insights into its structural features and establishing its phylogenetic placement within Ichneumonidae. These findings substantially contribute to the mitochondrial genomic data available for this diverse family.

Supplementary Material

Supplemental Material.docx
TMDN_A_2451201_SM9791.docx (4.8MB, docx)

Funding Statement

This work was supported by the National Natural Science Foundation of China [32070472].

Author contributions

Both Yu-Hao Nie and Zi-Cong Li made significant contributions to the collection of S. vesicarius, data analysis, and drafting of the manuscript collaboratively. Zi-Cong Li critically reviewed and approved the manuscript, while also revising its final version. Hong-Ying Hu provided experimental conditions, designed the experiments, and acquired funding.

Ethical approval

The sampling site is located outside of any protected area, and ethical approval is not necessary.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

The data supporting the findings of this study are openly available in the GenBank of NCBI at https://www.ncbi.nlm.nih.gov/ under the accession number PP971122. The associated BioProject, BioSample and SRA numbers are PRJNA1128876, SAMN42109884, SRR29606238 (result of second-generation sequencing data), and SRR29606384 (result of third-generation sequencing Data), respectively.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplemental Material.docx
TMDN_A_2451201_SM9791.docx (4.8MB, docx)

Data Availability Statement

The data supporting the findings of this study are openly available in the GenBank of NCBI at https://www.ncbi.nlm.nih.gov/ under the accession number PP971122. The associated BioProject, BioSample and SRA numbers are PRJNA1128876, SAMN42109884, SRR29606238 (result of second-generation sequencing data), and SRR29606384 (result of third-generation sequencing Data), respectively.

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