JHR 95: 85-94 (2023) Fam JOURNAL OF | *0eerrtievedopencoss ural
doi: 10.3897/jhr.95.95646 RESEARCH ARTICLE () Hymenopter a

The International Society of Hymenopterists RESEARCH

https://jhr.pensoft.net

First record of the genus Sathon Mason, 1981
(Hymenoptera, Braconidae, Microgastrinae) in China

Zhen Liu'?, Jia-Jun Liu’, Jun-Hua He’, Xue-Xin Chen?

| Zoology Key Laboratory of Hunan Higher Education College of life and environmental sciences, Hunan
University of Arts and Science, Changde 415000, China 2. Institute of Insect Sciences, Zhejiang University,
Hangzhou 310058, China 3 Hunan Applied Technology University, Changde 415000, China

Corresponding author: Zhen Liu (qingniao8.27@163.com)

Academiceditor: Jose Fernandez- Triana | Received 28 September2022 | Accepted 13 December2022 | Published 17 February 2023
Attps://zoobank. org/64EBC59C-DCAB-41FA-B34A-6E432820F4BF

Citation: Liu Z, Liu J-J, He J-H, Chen X-X (2023) First record of the genus Sathon Mason, 1981 (Hymenoptera,
Braconidae, Microgastrinae) in China. Journal of Hymenoptera Research 95: 85-94. https://doi.org/10.3897/jhr.95.95646

Abstract
Sathon Mason, 1981 is reported for the first time from China through providing a diagnosis, description,
and images of Sathon falcatus (Nees, 1834). The mitochondrial genome of S. falcatus was sequenced, an-

notated and analysed.

Keywords

China, Microgastrinae, mitogenomics, Sathon

Introduction

The genus Sathon was erected in the tribe Microgastrini by Mason (1981) based on
some species from the vitripennis- and falcatus-groups of Apanteles s.l. (Nixon, 1965).
Williams (1985) separated three species from Sathon Mason and erected a new genus,
Lathrapanteles Williams, from the New World sooner after its determination. And later,
Williams (1988) revised Sathon while reporting five new species from the New World.
Austin & Dangerfield (1992) added two new species and three new combinations to
this genus when reviewing species from the Australasian region. Recently, Fagan-Jef-
fries et al. (2019) reported one new species from Australia and Fernandez-Triana et al.

Copyright Zhen Liu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0),
which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

86 Zhen Liu et al. / Journal of Hymenoptera Research 95: 85-94 (2023)

(2020) transferred six species from Ethiopian Microgaster Latreille to Sathon in sorting
the world checklist of Microgastrinae parasitoid wasps.

So far, 23 species (Fernandez-Triana et al. 2020) have been described under this
genus worldwide. It was strange that none had ever been reported from China before
this study, not to speak of Sathon falcatus (Nees, 1834), typical representative of Wil-
liams’s (1988) S. falcatus-group in the Old World which is distributed in 42 countries,
including some neighboring countries of China, e.g., Japan, Korea, Mongolia, and
Russia. We luckily found this species which represents a new genus record of China in
Inner Mongolia during our ongoing revision of the Chinese Microgastrinae.

The status of the genus Sathon has been discussed by some taxonomists since it was
established. Whitfield et al. (2002, 2009) and Arias-Penna et al. (2019) suggested that
Sathon should likely be subsumed within Glyptapanteles Ashmead because they shared
many characters. Plus, van Achterberg (2003) and Fernandez-Triana (2010) suggested
that Sathon and Glyptapanteles should be part of an expanded Protapanteles Ashmead.
It also has complicated relationships with the genera Choeras Mason and Lathrapanteles
(Fagan-Jeffries et al, 2019; Austin and Dangerfield 1992; Fernandez-Triana et al. 2020).

Microgastrine is considered as the most species-rich subfamily of animals on Earth
and has become a key group of organisms for studying parasitism, parasitoid genomics,
and mating biology (Whitfield et al. 2018). Nuclear genes (Banks et al. 2006), mito-
chondrial COI, 16S, and 28S genes, along with morphological characters (Mardulyn
et al. 1999; Whitfield et al. 2002) and anchored hybrid enrichment data (Parks et al.
2020) had been applied in earlier molecular studies. Here, we present the mitochon-
drial sequence of S. falcatus, which we hope it will be useful for subsequent phylogentic
studies in the subfamily.

Material and methods

Collection, Identification and DNA extraction

This work is based on specimens in the collections of the Parasitic Hymenoptera Col-
lection of Zhejiang University, Hangzhou, China. Materials were all collected by hand
netting in Helan Mountain, Inner Mongolia (E105°49'—-106°41', N38°19'-39°22').
Each dried specimen was tagged with a unique number.

Descriptions and measurements were made using a stereomicroscope (Zeiss Stereo
Discovery V8). All photographs of the wasps were taken and processed using a digi-
tal camera KEYENCE VHX-2000C. The images were further processed using Adobe
Photoshop CS6. Morphological terms for body structures and measurements follow
Nixon (1965) and Mason (1981). The veins follow the modified Comstock-Needham
system (van Achterberg 1993). The terminology of the cuticular sculpture follows Har-
ris (1979).

Genomic DNA was extracted from the legs of a single specimen (No. 201006962)
using a Ezup Column Animal Genomic DNA Purification Kit (Sangon Biotech,

New record of Sathon Mason, 1981 in China 87

China) following the manufacturer's protocols. Extracted genomic DNA were quali-
fied by NanoPhotometer (IMPLEN, CA, USA) and Qubit 3.0 (Invitrogen, Life Tech-
nologies, Carlsbad, CA, USA) and a Nanodrop 2000c Spectrophotometer (Thermo
Scientific, Wilmington, DE, USA). All residual DNAs are archived (-30 °C) in the
molecular laboratory of Hunan University of Arts and Science, Changde, China, and
are available for further study upon request.

Genome sequencing, assembly and annotation

The extracted genomic DNA of the specimen was sheared into fragments of approxi-
mately 350 bp in length using the Ultrasonic Processor Covaris $220 (Covaris, Inc.
MS, USA). High-throughput sequencing libraries were constructed using the Illumina
TruSeq DNA PCR-Free HT Kit and sequenced using an Illumina Novaseq6000 with
the strategy of producing 150 bp paired-ends by the Annoroad Gene Tech. (Beijing)
Co., Ltd. Quality of raw sequencing reads was checked by FastQC version 0.11.3
(Andrews 2010), and low-quality reads and sites were filtered by Trimmomatic version
3.2.57 (Bolger et al. 2014).

The target mitochondrial reads were filtered out using BLAST (BLASTn with E
value: 1 x 10) against a reference data set containing Braconidae mitochondrial ge-
nomes via the FastqExtract script (Crampton Platt et al. 2015). The mitochondrial ge-
nome of Sathon falcatus was assembled by IDBA_UD version 1.1.3 (Peng et al. 2012)
and SPAdes version 3.15.2 (Bankevich et al. 2012) with default parameters.

Annotation of the assembled genome was performed by using MITOS Web Server
(Bernt et al. 2013). Start and stop codons of protein-coding genes (PCGs) were manu-
ally adjusted in Geneious Prime v11 by referencing to the published mito-genomes of
Microgastrinae. Gene rearrangements were analyzed by comparing with the putative
ancestral type of Drosophila melanogaster (Diptera: Drosophilidae).

Results

Taxonomy
Genus Sathon Mason, 1981

Sathon Mason, 1981: 78. Williams 1988: 540; Austin and Dangerfield 1992: 52;
Fagan-Jeffries et al. 2019: 427. Fernandez-Triana et al. 2020: 945.

Type species. Apanteles neomexicanus Muesebeck, 1920, by original designation.
Diagnosis. Areolet of fore wing present or absent; metanotum with sublateral
lobes slightly setose, exposing postero-lateral phragma of scutellum; propodeum with
median carina present over most of length or almost completely absent, but marked by
at least a trace of rugosity; tergite I somewhat narrow, length at least 3.0x longer than

88 Zhen Liu et al. / Journal of Hymenoptera Research 95: 85-94 (2023)

apical width; tergite Hf subtriangular; hypopygium evenly sclerotized, without striae
mid-ventrally; ovipositor sheaths at least half as long as hind tibia; often with large
external genitalia in male.

Host. Bombycidae: Bombyx mori (L., 1758); Limacodidae: Cheromettia lo-
hor (Moore, 1859), C. sumatrensis (Heylaerts, 1884); Noctuidae: Actinotia polyodon
(Clerck, 1759), Apamea lateritia (Hufnagel, 1766), Apamea monoglypha (Hufnagel,
1766); Papilionidae: Papilio zelicaon Lucas, 1858; Pterophoridae: Adaina microdac-
tyla (Hiibner, 1813), Emmelina monodactyla (L., 1758); Psychidae: Hyalarcta huebneri
(Westwood, 1854); H. nigresens (Doubleday, 1845), Narycia Stephens, 1836; Sesiidae:
Synanthedon tipuliformis Clerck, 1759, Zeiraphera griseana (Hiibner, 1799); Tortrici-
dae: Rhyacionia buoliana (Denis & Schiffermiiller, 1775) (Yu et al. 2016; Fernandez-
Triana et al. 2020). This list of hosts records was compiled in a non-critical way by Yu
et al. (2016) from the literature and it is very likely that several (perhaps many) records
are inaccurate or erroneous.

Distribution. Worldwide.

Sathon falcatus (Nees, 1834)

Microgaster falcatus Nees von Esenbeck 1834: 175; type lost, Neotype designated by
Wilkinson 1945: 113, 2 — Germany: Zoologisches Museum, Hamburg University.

Microgaster equestris Haliday, 1834. Synonymized by Curtis 1837: 116.

Apanteles equestris; Hincks, 1944: 20.

Apanteles priapus Gautier & Cleu, 1927. Syn. by Wilkinson 1945: 133.

Apanteles gladiator Szepligeti, 1901. Syn. by Tobias 1971: 246.

Sathon falcatus: Mason 1981: 78; Williams 1988: 560.

Diagnosis. Body length 3.3—-3.5 mm, fore wing length 3.6—-3.8 mm. Antenna nearly
1.1x longer than body length, preapical segment of antenna 1.3x longer than wide.
Scutellar sulcus curved, narrow with spare carinae in between. Propodeum 1.8x wider
than long, not shiny, densely longitudinally rugose medially, with punctate-rugose
aside, largely polished on anterior-medial part and posterior corners. Pterostigma 2.3x
as long as its widest part. Tergite I slightly narrowing towards posterior margin, 2.2
longer than hind width, turned-over part as long as wide, shallowly and independently
punctate, weakly rugulose-punctate laterally. Tergite Hl weakly striate laterally, polished
medially, strongly curved apically. Ovipositor sheath 0.8x length of hind tibia, falcate.

Head. Transverse in dorsal view, 1.9x as wide as long, 1.1x wider than mesoscu-
tum. Eyes 1.6x longer than temple dorsally. Gena slightly dull with poorly defined,
shallow punctures, constricted behind eyes from dorsal view (Fig. le). Face (Fig. 1f) a
little shiny with fine, sparse punctures with intervals 2—4 times of a puncture diameter,
transverse, 0.8x as high as wide, sparsely pubescent. Ocelli big, posterior tangent to
anterior ocellus just touching posterior pair of ocelli, distance between fore and a hind
ocelli shorter than diameter of an hind ocellus, hind ocelli separated from one another

New record of Sathon Mason, 1981 in China 89

Figure |. Sathon falcatus (Nees, 1834) (new record to China) a 9, habitus, lateral view b 3, habitus,
lateral view € fore wing d hind wing e head, dorsal view f head, frontal view g antenna h metanotum
i propodeum and terga I-III j mesosoma, dorsal view k male external genitalia | mesopleuron, lateral view.
Scale line: 0.5 mm.

by 1.5x their own diameter and from eye by 1.4x their own diameter. Antenna nearly
1.1x longer than body length, preapical segment of antenna 1.3x longer than wide
(Fig. 1g).

Mesosoma. Length:width:height = 29.0:17.5:20. Mesoscutum (Fig. 1j) shiny, no
notaulic courses, punctures fine, intervals 2-3x of a puncture diameter, a little sparser
posteriorly. Scutellar sulcus curved, narrow with spare carinae in between. Scutel-
lum shiny, with sparse punctures, intervals 2-4x of a puncture diameter. Propodeum
(Fig. 1i) 1.8x wider than long, not shiny, densely longitudinally rugose medially, with
punctate-rugose aside, largely polished on anterior-medial part and posterior corners.
Mesopleuron (Fig. 11) highly shiny, largely polished, except anterior part shallowly
punctate, intervals 2-3x of a puncture diameter.

90 Zhen Liu et al. / Journal of Hymenoptera Research 95: 85-94 (2023)

Legs. Hind coxa shallowly punctate dorsally. Inner spurs of hind tibia half-length
of hind basitarsus, outer spur 2/5. Basitarsus of hind leg as long as tarsomeres 2—4.

Wings. Pterostigma 2.3x as long as its widest part (Fig. 1c). Vein 1-R1 1.4x length
of pterostigma, nearly 4.0x longer than its distance from apex of marginal cell. Vein r
arising from apex of pterostigma, nearly perpendicular to and 0.8x as long as width of
latter, r 1.2x longer than 2-SR, distinctly angled at meeting, 2-M 4/5 length of 2-SR.
First discal cell of fore wing nearly 1.2x wider than high. Second submarginal cell of
hind wing 1.5x wider than high, vein cu-a of hind wing a little incurved (Fig. 1d).

Metasoma. 1.4x longer than mesosoma. Tergite I (Fig. 1i) slightly narrowing to-
wards posterior margin, 2.2x longer than hind width, basal width 1.4x longer than
apical width, basal 2/5 concave, turned-over part as long as wide, shallowly and in-
dependently punctate, weakly rugulose-punctate laterally, no longitudinal channel.
Tergite II weakly striate laterally, polished medially, 1.9x wider than long in middle,
strongly curved apically. Tergite II 1.6x longer than tergite II. Tergites posterior to
tergite II polished, shiny, and sparsely pubescent. Hypopygium a little shorter than
apex of metasoma. Ovipositor sheath 0.8x length of hind tibia, falcate.

Colour. Black (Fig. 1a). Tegula brown. Palpi blackish brown and spurs pale yellow.
Flagellum of antenna dark brown. Mandible yellowish brown. Legs mainly reddish yel-
low, except sometimes hind femur, apical fourth and all tarsi fulvous. Wing membrane
hyaline, vein and pterostigma brown.

Male. Similar to female, except preapical segment of antenna much longer, 2.5x
longer, colouration of legs lighter (Fig. 1b).

Hosts. Noctuidae: Actinotia polyodon (Clerck, 1759), Apamea lateritia (Hufnagel,
1766), Apamea monoglypha (Hufnagel, 1766); Pterophoridae: Adaina microdactyla
(Hiibner, 1813); Sesiidae: Synanthedon tipuliformis Clerck, 1759; Zeiraphera griseana
(Hiibner, 1799); Tortricidae: Rhyacionia buoliana (Denis & Schiffermiiller, 1775) (Yu
et al. 2016; Fernandez-Triana et al. 2020, see comments above).

Material examined. (ZJUH). 1599504, Luanchaigou, Helan Mountain, In-
ner Mongolia, 26.VII.2010, Jie Zeng, Nos. 201006962, 201007079, 201006956,
201006892, 201006933, 201007110, 201006901, 201006900, 201007014,
201007015, 201007019, 201007020, 201007022, 201007013, 201007113,
201006895, 201006946, 201006913, 201007100, 201006910; 1089 9293'3,
Dayanggou, Helan Mountain, Inner Mongolia, 27.VII.2010, Hongfei Chai, Nos.
201007246, 201007253, 201007262, 201007316, 201007391, 201007216,
201007397, 201007399, 201007404, 201007401, 201007396, 201007395,
201007394, 201007380, 201007388, 201007402, 201007406, 201007400,
201007389, 201007390, 201007418, 201007414, 201007332, 201007331,
201007430, 201007429, 201007431, 201007433, 201007435, 201007255,
201007282, 201007434, 201007387, 201007386, 201007385, 201007341,
201007343, 201007359, 201007357, 201007377, 201007344, 201007345,
201007333, 201007348, 201007360, 201007371, 201007378, 201007213,
201007265, 201007252, 201007312, 201007314, 201007315, 201007352,
201007330, 201007327, 201007326, 201007325, 201007324, 201007322,

New record of Sathon Mason, 1981 in China 91

201007321, 201007318, 201007363, 201007317, 201007335, 201007307,
201007306, 201007303, 201007302, 201007301, 201007299, 201007297,
201007296, 201007293, 201007287, 201007283, 201007284, 201007278,
201007275, 201007272, 201007271, 201007270, 201007267, 201007264,
201007261, 201007257, 201007251, 201007249, 201007245, 201007244,
201007243, 201007242, 201007239, 201007235, 201007234, 201007229,
201007228, 201007227, 201007208, 201007205, 201007206, 201007209,
201007211, 201007212, 201007215, 201007392, 201007222, 201007204,
201007202, 201007201, 201007198, 201007200, 201007199, 201007196,
201007195, 201007194, 201007192, 201007191, 201007187, 201007186,
201007184, 201007185, 201007156, 201007160, 201007164, 201007162,
201007166, 201007169, 201007172, 201007176, 201007173, 201007174,
201007177, 201007179, 201007183, 201007420, 201007419; 12, Qianggangling,
Helan Mountain, Inner Mongolia, 3.VIII.2010, Dingjie Zhang, No. 201006771; 19,
Ganshuwan, Helan Mountain, Inner Mongolia, 9.VHI.2010, Yan Li, No. 201006663.

Distribution. China: Inner Mongolia; Afghanistan, Austria, Armenia, Azerbaijan,
Belarus, Bosnia and Herzegovina, Croatia, Czech Republic, Denmark, Egypt, Estonia,
Finland, France, Georgia, Germany, Hungary, Indonesia, Ireland, Italy, Japan, Ka-
zakhstan, Kyrgyzstan, Korea, Latvia, Lithuania, Luxembourg, Macedonia, Mongolia,
Montenegro, Netherlands, Poland, Romania, Russia, Serbia, Slovenia, Spain, Sweden,
Switzerland, Tajikistan, Turkey, United Kingdom and Uzbekistan.

Notes. Characters of the examined specimens from China are mostly in agreement
with the description in William (1988), except the legs are lighter (mainly reddish-yellow
in female or yellow in male) than what he described (mainly rufo-fulvous in female). Char-
acters combining large inflexible hypopygium, the length of ovipositor with its sheath and
the typical large external genitalia in males (Fig. 1k, 1.5x wider than width of hind femur),
could be a useful way to distinguish S. falcatus from other related genera in China. We
treated Sathon provisionally as a valid genus for the Chinese fauna, with only one distin-
guishable representative for now, though the size of genitalia varies in other Sathon species.

Genome characteristic analyses

A total of 5.76 Gb filtered clean data were produced. The imcomplete mitochondrial
genome of S. falcatus is 14,492 bp in length (GenBank accession OP432054), contain-
ing 11 PCGs, 17 tRNA genes. The entire A+T content in the S. falcatus mitochondrial
genome was 88%, which ranged from 75.60% (cox1) to 91.7% (atp8) with 39.7% of
A, 7.1% of G, 48.3% of T, and 4.9% of C. It is common to find such relative high
A+T proportion in the mitochondrial genome of Hymenoptera (Oliveira et al. 2008).
The sequence of CO/ gene obtained closest match with a Sathon sp. sequence (Sample
ID: CGTURK-1557, BIN ID: BOLD:ACE9685) by 99.07% and Sathon falcatus se-
quence (Sample ID: CGTURK-1532, BIN ID: BOLD:AAB3882) by 98.45% when
blasted in the BOLD (Barcode of Life Database, http://www.boldsystems.org/), which

confirmed the conspecificity of Chinese material with other S. falcatus specimens.

92 Zhen Liu et al. / Journal of Hymenoptera Research 95: 85—94 (2023)

Ancestral type of insect DINED DES DS ss ee

Sathon falcatus P naaz Pwo] ¥ [cost [ta] cox [| | x [atos]anos) sas | oats [st] aD EDN] sas [cf cos] R[F soast] TL Py ands]

Figure 2. Gene rearrangement in the mitochondrial genome of Sathon falcatus (Nees, 1834).

Gene rearrangements were evident when compared with the ancestral type of Dros-
ophila melanogaster: remote and local inversion occurred in trnH and trnY respectively,
trnK and trnD were translocated, cox3—nad4 were shuffled (Fig. 2). The rearrange-
ments showed on mitogenomes evidenced the rapid evolution of this group compared
to other lineages of Hymenoptera.

Acknowledgements

We thank the reviewers who critically reviewed the manuscript. Funding for this study
was provided by the National Natural Science Foundation of China (32100351), Sci-
entific Research Fund of Hunan Provincial Education Department (20K089) and Hu-
nan Provincial Natural Science Foundation of China (2020JJ5392).

References

Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. http://
www.bioinformatics.babraham.ac.uk/projects/fastqc/

Arias-Penna DC, Whitfield JB, Janzen DH, Hallwachs W, Dyer LA, Smith MA, Fernandez-Tri-
ana JL (2019) A species-level taxonomic review and host associations of Glyptapanteles (Hy-
menoptera, Braconidae, Microgastrinae) with an emphasis on 136 new reared species from
Costa Rica and Ecuador. ZooKeys 890: 1-685. https://doi.org/10.3897/zookeys.890.35786

Austin AD, Dangerfield PC (1992) Synopsis of Australasian Microgastrinae (Hymenoptera:
Braconidae), with a key to genera and description of new taxa. Invertebrate Systematics
6(1): 1-76. https://doi.org/10.1071/IT9920001

Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Niko-
lenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev
MA, Pevzner PA (2012) SPAdes: A new genome assembly algorithm and its applications
to single-cell sequencing. Journal of Computational Biology 19(5): 455-477. https://doi.
org/10.1089/cmb.2012.0021

Banks JC, Whitfifield JB (2006) Dissecting the ancient rapid radiation of microgastrine wasp
genera using additional nuclear genes. Molecular Phylogenetics and Evolution 41: 690-
703. https://doi.org/10.1016/j.ympev.2006.06.001

Bernt M, Donath A, Jiihling FE Externbrink F, Florentz C, Fritzsch G, Pitz J, Middendorf M,
Stadler PF (2013) MITOS: Improved de novo metazoan mitochondrial genome annota-
tion. Molecular Phylogenetics and Evolution 69(2): 313-319. https://doi.org/10.1016/j.
ympev.2012.08.023

New record of Sathon Mason, 1981 in China 93

Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence
data. Bioinformatics 30: 2114-2120. https://doi.org/10.1093/bioinformatics/btul70
Crampton-Platt A, Timmermans MJ, Gimmel ML, Kutty SN, Cockerill TD, Vun Khen C,
Vogler AP (2015) Soup to Tree: The Phylogeny of Beetles Inferred by Mitochondrial
Metagenomics of a Bornean Rainforest Sample. Molecular Biology and Evolution 32:

2302-2316. https://doi.org/10.1093/molbev/msv111

Fagan-Jeftries EP, Cooper SJ, Austin AD (2019) New species of Australian microgastrine parasitoid
wasps (Hymenoptera: Braconidae: Microgastrinae) documented through the “Bush Blitz’ surveys
of national reserves. Zootaxa 4560(3): 401-440. https://doi.org/10.11646/zootaxa.4560.3.1

Fernandez-Triana J (2010) Eight new species and an annotated checklist of Microgastrinae
(Hymenoptera: Braconidae) from Canada and Alaska. ZooKeys 63: 1-53. https://doi.
org/10.3897/zookeys.63.565

Fernandez-Triana J, Shaw MR, Boudreault C, Beaudin M, Broad GR (2020) Annotated and
illustrated world checklist of Microgastrinae parasitoid wasps (Hymenoptera, Braconidae).
ZooKeys 920: 1-1089. https://doi.org/10.3897/zookeys.920.39128

Harris RA (1979) Glossary of surface sculpturing. Occasional Papers in Entomology of the
California Department of Food and Agriculture 28: 1-31.

Mardulyn P, Whitfifield JB (1999) Phylogenetic siugnal in the COI, 16S, and 28S genes for
inferring relationships among genera of Microgastrinae (Hymenoptera: Braconidae).
Evidence of a high diversifification rate in this group of parasitoids. Molecular Phylogenet-
ics and Evolution 12: 282-294. https://doi.org/10.1006/mpev.1999.0618

Mason WRM (1981) ‘The polyphyletic nature of Apanteles Foerster (Hymenoptera: Braconi-
dae): A phylogeny and reclassification of Microgastrinae. Memoirs of the Entomological
Society of Canada No. 115. 147 pp. https://doi.org/10.4039/entm113115fv

Nixon GEJ (1965) A reclassification of the tribe Microgasterini (Hymenoptera: Braconidae).
Bulletin of the British Museum (Natural History), Entomology series Supplement 2:
1-284. https://doi.org/10.5962/p.144036

Nees von Esenbeck CG (1834) Hymenopterorum Ichneumonibus affnium monographiae,
genera Europaea et species illustrantes, 1. Stuttgartiae et Tubingae. 320 pp. https://doi.
org/10.5962/bhl.title.26555

Oliveira D, Raychoudhury R, Lavrov DV, Werren JH (2008) Rapidly evolving mitochondrial
genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia
(Hymenoptera: Pteromalidae). Molecular Biology and Evolution 25: 2167—2180. https://
doi.org/10.1093/molbev/msn159

Parks KS, Janzen DH, Hallwachs W, Fernandez-Triana J, Dyer LA, Rodriguez JJ, Arias-Penna
DC, Whitfield JB (2020) A five-gene molecular phylogeny reveals Parapanteles Ashmead
(Hymenoptera: Braconidae) to be polyphyletic as currently composed. Molecular Phyloge-
netics and Evolution 150: e106859. https://doi:10.1016/j.ympev.2020.106859

Peng Y, Leung HCM, Yiu SM, Chin FYL (2012) IDBA-UD: A de novo assembler for single-
cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 28(11):
1420-1428. https://doi.org/10.1093/bioinformatics/bts174

Tobias V (1971) Review of the Braconidae (Hymenoptera) of the USSR. Trudy Vsesoyuznogo
Entomologicheskogo Obshchestva 54: 156-268.

94 Zhen Liu et al. / Journal of Hymenoptera Research 95: 85-94 (2023)

Whitfield JB, Benzing A, Ponce F (2002) Review of the Glyptapanteles species (Hymenoptera:
Braconidae, Microgastrinae) attacking noctuids in field crops in the Neotropical Region,
with description of two new species from the Ecuadorian Andes. Journal of Hymenoptera
Research 11: 152-165.

Whitfield JB, Rodriguez JJ, Masonick PK (2009) Reared microgastrine wasps (Hymenop-
tera: Braconidae) from Yanayacu Biological Station and environs (Napo Province, Ec-
uador): diversity and host specialization. Journal of Insect Science 9(1): 31. https://doi.
org/10.1673/031.009.3101

Whitfield JB, Austin AD, Fernandez-Triana J (2018) Systematics, Biology, and Evolution of
Microgastrine Parasitoid Wasps. Annual Review of Entomology 63: 389-406. https://doi.
org/10.1146/annurev-ento-020117-043405

Wilkinson DS (1945) Description of palearctic species of Apanteles (Hymen., Braconidae).
Transactions of the Royal Entomological Society of London 95(3): 35-226. https://doi.
org/10.1111/j.1365-2311.1945.tb00436.x

Williams DJM (1985) The New World genus Lathrapanteles n. gen.: phylogeny and placement
in the Microgastrinae (Hymenoptera: Braconidae: Cotesiini). Canadian Journal of Zool-
ogy 63(8): 1962-1981. https://doi.org/10.1139/z85-289

Williams DJM (1988) Classification, phylogeny and zoogeographic studies of species of Sathon
Mason (Hymenoptera: Braconidae). Quaestiones Entomologicae 24(4): 529-639.

van Achterberg C (1993) Illustrated key to the subfamilies of the Braconidae (Hymenoptera:
Ichneumonoidea). Zoologische Verhandelingen (Leiden) 283: 1-189.

van Achterberg C (2003) Western Palaearctic genera of the subfamily Microgastrinae: A re-
appraisal of the generic and tribal division (Hymenoptera: Braconidae). In: Melika G,
Thurdéczy C (Eds) Parasitic wasps. Evolution, systematics, biodiversity and biological con-
trol (Agroinform Budapest): 19-35.

Yu DSK, van Achterberg C, Horstmann K (2016) Taxapad 2016, Ichneumonoidea 2015.

Database on flash-drive. Nepean, Ontario. http://www.taxapad.com