Research Article |
Corresponding author: Rongjiao Zhang ( zhangrongjiao0922@163.com ) Corresponding author: Weian Deng ( dengweian5899@163.com ) Academic editor: Jun-Jie Gu
© 2024 Jieling Luo , Rongjiao Zhang, Weian Deng.
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.
Citation:
Luo J, Zhang R, Deng W (2024) First mitogenomic characterization of Macromotettixoides (Orthoptera, Tetrigidae), with the descriptions of two new species. ZooKeys 1195: 95-120. https://doi.org/10.3897/zookeys.1195.112623
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Classification of species is commonly based on morphological, molecular, and distribution depending on the taxa. Macromotettixoides Zheng, Wei & Jiang, 2005 and Formosatettix Tinkham, 1937 are both wingless types of Tetrigidae with extremely similar morphological characteristics, and in the current taxonomic system they are placed in two different subfamilies, Metrodorinae and Tetriginae, respectively. It is difficult to clearly identify the species of these two genera by morphological characteristics, and molecular data is often needed to assist identification. Here, the complete mitogenomes of two new species were sequenced and assembled, with that of Macromotettixoides orthomargina. Molecular data of species of Formosatettix were used to test the monophyly of Macromotettixoides and to re-assess the generic characters, and also to test whether Macromotettixoides belongs to the Asian Metrodorinae or Tetriginae. Furthermore, mitochondrial characteristics were analyzed and the phylogeny of the Tetrigidae reconstructed based on mitochondrial protein-coding genes (PCGs). The results indicated that the two new species were clustered with Macromotettixoides rather than Formosatettix, and the anterior margin of the fastigium and pronotum of the two new species usually had the humeral angle different from that of Formosatettix. Therefore, after integrating morphological and molecular data, the two new species were placed in the genus Macromotettixoides, M. maoershanensis sp. nov. and M. brachycorna sp. nov. Finally, a phylogenetic reconstruction supported Macromotettixoides being assigned to Tetriginae rather than Metrodorinae, in contrast to the previous classification of this genus.
China, Formosatettix, Metrodorinae, mitochondrial genome, phylogeny, taxonomy, Tetriginae
Tetrigidae is a family of Orthopteran insects in the superfamily Tetrigoidea. The pygmy grasshoppers are an ancient group of Orthoptera with a relatively uniform body structure (
Mitogenomes are stable in structure and composition; they have maternal inheritance and less recombination (
To date, among the Tetrigidae, only 35 species have their mitochondrial genomes published in GenBank. Additionally, many Tetrigidae have known COI sequences, but these are not adequate for deep phylogeny, only for species identification (
Macromotettixoides Zheng, Wei & Jiang, 2005 (
In this study, we collected two new species in Guangxi from China and discovered that they shared traits with both genera Macromotettixoides and Formosatettix. The two new species are similar to Formosatettix in that the anterior margin of the fastigium is angularly projecting and the posterior angles of pronotum turned downwards, and the apex of the posterior angles obtuse and rounded, while the pronotum is with humeral angles are similar to Macromotettixoides. Therefore, based solely on their morphology, it was difficult to classify them to any genus. The purposes of this study were to sequence the complete mitochondrial genomes of two new species and Macromotettixoides orthomargina Wei & Deng, 2023, to examine their phylogenetic positions and relationships within the genus Macromotettixoides and Formosatettix, and to describe and illustrate the two new species from China.
Specimens of M. orthomargina, M. maoershanensis sp. nov., and M. brachycorna sp. nov. were selected as representatives of the genus Macromotettixoides. (1) M. orthomargina, n = 3, collected at Lingshan, Mianning County, Sichuan Province, China; 23 June 2020; (2) M. brachycorna sp. nov., n = 3, collected at Jiuwanshan National Nature Reserve, Huanjiang Country, Guangxi, China; 25°11'41"N, 108°38'51'E; 29 July 2022; (3) M. maoershanensis sp. nov., n = 14, collected at Maoershan National Nature Reserve, Xing’an County, Guangxi, China; 25°51′35″N, 110°29′34″E; 12 July 2021. The specimens were preserved in 100% anhydrous ethanol (Xilong Scientific, Sichuan, MA, China) and stored in the refrigerator at -20 °C in the
Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection, Ministry of Education of Guangxi Normal University (
To clarify the taxonomic status of M. maoershanensis sp. nov. and M. brachycorna sp. nov., we combined the mitochondrial genome data assembled in the laboratory and the complete mitochondrial genome data of Tetrigidae from GenBank, representing one family, five subfamilies, 23 genera, and 36 species in total (Table
Accession numbers and references of the mitogenomes of Tetrigidae included in this study.
Subfamily | Species | Accession number | Reference |
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Tripetalocerinae | Tripetaloceroides tonkinensis | MW770353 |
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Batrachideinae | Saussurella borneensis | MZ169555 |
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Metrodorinae | Bolivaritettix lativertex | MN083173 |
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Bolivaritettix sikkinensis | MN083174 |
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Bolivaritettix yuanbaoshanensis | KY123121 |
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Mazarredia convexa | MN938924 |
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Criotettigini | Criotettix japonicus | MT162542 |
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Scelimeninae | Falconius longicornis | MT162543 |
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Paragavialidium hainanense | NC_071831 | ||
Paragavialidium sichuanese | MT162549 |
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Scelimena melli | MW722938 |
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Zhengitettix curvispinus | MT162544 |
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Thoradontini | Eucriotettix oculatus | MN083176 |
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Loxilobus prominenoculus | MT162545 |
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Thoradonta nodulosa | MT162547 |
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Thoradonta obtusilobata | KY798414 |
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Thoradonta yunnana | OP805341 | ||
Tetriginae | Alulatettix yunnanensis | NC_018542 |
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Coptotettix longjiangensis | KY798413 |
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Coptotettix longtanensis | OK540319 | ||
Ergatettix serrifemora | MN938923 |
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Ergatettix dorsifera | NC_046540 |
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Euparatettix bimaculatus | NC_046541 |
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Euparatettix variabilis | NC_046542 |
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Formosatettix qinlingensis | KY798412 |
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Macromotettixoides brachycorna sp. nov. | OR003899 | This study | |
Macromotettixoides maoershanensis sp. nov. | OR030790 | This study | |
Macromotettixoides orthomargina | OR030789 | This study | |
Systolederus anhuiensis | OP113951 | ||
Systolederus bashanensis | NC_063118 | Li et al. 2021 | |
Systolederus hainanensis | NC_063117 | Li et al. 2021 | |
Systolederus nigropennis | MN938922 |
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Systolederus spicupennis | MH791445 | ||
Tetrix japonica | NC_018543 |
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Tetrix ruyuanensis | NC_046412 |
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Outgroup | Mirhipipteryx andensis | NC_028065 |
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All muscle tissues of each sample were extracted using a TlANamp Genomic DNA Kit (Tiangen Biotech, Beijing, China), and the extracted samples were sent to Berry Genomics (Beijing, China) for genomic sequencing using Next Generation Sequencing (NGS). The remaining specimens were deposited as voucher specimens at the Guangxi Normal University. Separate 350-bp insert libraries were created from the whole genome DNA and sequenced using the Illumina HiSeq X Ten sequencing platform. A total of 5 Gb of 150-bp paired-end (PE) reads were generated in total for each sample. The mitogenome sequences were assembled using NOVOPlasty 4.2.1 and annotated using the MITOS Web Server (http://mitos2.bioinf.uni-leipzig.de/index.py, accessed on 17 March 2023;
The base compositions, G–C- and A–T-skews, and codon usages were calculated in PhyloSuite v. 1.2.3. The formulas used to calculate the skews of the composition were (A–T) / (A+T) for the A–T-skew and (G–C) / (G+C) for the G–C-skew.
To systematically understand the phylogenetic relationships of M. orthomargina and the two new species, the mitochondrial genomes of the three species obtained in the laboratory and the mitogenomes of 36 species taken from GenBank were used to construct a phylogeny of the Tetrigidae, and Mirhipipteryx andensis of the Tridactyloidea was selected as the outgroup. The analysis was performed using PhyloSuite 1.2.3. Redundant sequences were removed, and protein-coding genes in the mitochondrial genome were extracted and aligned in batches with MAFFT (
Best-fitting models used for phylogenetic analyses of the mitochondrial PCGs dataset.
Information Criterion for model selection | Best model | Partition names |
---|---|---|
AICc | GTR+F+R4 | cox3_mafft, nad4L_mafft, nad4_mafft |
TIM+F+I+I+R5 | nad1_mafft | |
GTR+F+I+I+R5 | cox1_mafft, nad5_mafft | |
TIM2+F+I+I+R4 | cox2_mafft | |
TIM3+F+R5 | atp6_mafft, nad2_mafft | |
TIM2+F+R4 | cytb_mafft, nad3_mafft | |
TIM3+F+I+I+R4 | nad6_mafft | |
TN+F+I+I+R3 | atp8_mafft | |
BIC | GTR+F+I+G4 | atp6_mafft, cox2_mafft, cytb_mafft, cox1_mafft, cox3_mafft, nad1_mafft, nad4L_mafft, nad4_mafft, nad2_mafft, nad3_mafft, nad5_mafft, nad6_mafft, atp8_mafft |
Bayesian inference phylogenies were obtained using MrBayes v. 3.2.7a (
The maximum likelihood phylogenies were inferred using IQ-TREE v. 2.2.0 (
In this study, the mitochondrial genomes of M. orthomargina, M. brachycorna sp. nov., and M. maoershanensis sp. nov. were all circular molecules, with total lengths of 16,995 bp, 18,034 bp, and 16,999 bp, respectively (Fig.
The gene arrangements of the newly sequenced mitochondrial genomes were similar to those of other species of Tetrigidae (
Regions | A% | G% | AT% | AT-skew | GC-skew |
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Full genome | 41.4/44.1/43.9 | 10.4/9.2/9.5 | 71.4/73.7/73.2 | 0.158/ 0.198/0.200 | –0.274/–0.296/–0.293 |
PCGs | 31.0/ 31.9/31.2 | 14.1/13.2/13.6 | 69.4/72.3/71.2 | –0.108/–0.117/–0.124 | –0.079/–0.046/–0.051 |
1st codon position | 34.0/34.8/34.3 | 18.5/17.9/18.1 | 67.1/69.0/68.9 | 0.013/0.008/–0.004 | 0.128/0.152/0.163 |
2nd codon position | 20.3/20.3/20.4 | 14.8/14.7/14.7 | 65.6/ 65.9/66.2 | –0.382/–0.384/–0.384 | –0.140/–0.135/–0.130 |
3rd codon position | 38.6/40.5/38.9 | 9.0/7.1/8.1 | 75.4/81.7/78.6 | 0.023/–0.009/–0.01 | –0.270/–0.217/–0.240 |
rRNAs | 40.8/41.8/41.6 | 12.7/12.2/12.5 | 74.2/75.0/74.0 | 0.100/ 0.115/0.124 | –0.017/–0.026/–0.038 |
tRNAs | 28.8/27.3/27.6 | 16.1/15.9/16.4 | 75.2/76.9/76.1 | –0.234/–0.290/–0.274 | 0.296/0.374/0.372 |
CR | 36.2/46.3/48.1 | 13.1/9.6/8.0 | 69.4/79.2/80.0 | 0.040/0.170/0.203 | –0.140/–0.077/–0.200 |
As in most pygmy grasshoppers, ATN was the initiation codon of M. orthomargina, M. brachycorna sp. nov., and M. maoershanensis sp. nov., with ATG being the most frequently used (Table
Initiation and termination codons of PCGs of the newly sequenced complete mitogenomes.
PCGs | Initiation codons | Termination codons | ||||
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M. maoershanensis | M. brachycorna | M. orthomargina | M. maoershanensis | M. brachycorna | M. orthomargina | |
ATP6 | ATG | ATG | ATG | TAA | TAA | TAA |
ATP8 | ATG | ATG | ATG | TAA | TAA | TAA |
COX1 | ATC | ATC | ATC | TAA | TAA | TAA |
COX2 | ATG | ATG | ATG | TAA | TAA | TAA |
COX3 | ATG | ATG | ATG | T | T | T |
CYTB | ATG | ATG | ATG | TAA | TAA | TAA |
NAD1 | ATT | ATT | ATA | TAA | TAA | TAA |
NAD2 | ATT | ATA | ATT | TAA | TAA | TAA |
NAD3 | ATA | ATC | ATA | TAG | TAG | TAG |
NAD4 | ATG | ATG | ATG | TAG | TAA | TAG |
NAD4L | ATT | ATT | ATT | TAA | TAA | TAA |
NAD5 | ATG | ATG | ATG | T | TA | T |
NAD6 | ATA | ATG | ATA | TAA | TAA | TAA |
Comparing the AT content of the mitochondrial genomes’ PCGs, rRNAs, tRNAs, and the control regions of Tetrigidae (Suppl. material
Comparison of the codons of PCGs in Tetrigids (Suppl. material
There was little difference in the lengths of all tRNAs in the newly sequenced mitochondrial genomes of M. orthomargina and M. maoershanensis sp. nov. All secondary structures of the tRNAs of the three species could be folded into a typical clover structure (Fig.
Total numbers of different types of base mismatches in tRNAs of the three newly sequenced mitogenomes.
Species | A–A | A–G | A–C | G–U | C–U | U–U |
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M. orthomargina | 1 (trnW) | 1 (trnG) | 1 (trnS2) | 34 | 2 (trnY, trnE) | |
M. brachycorna sp. nov. | 2 (trnW, trnG) | 1 (trnF) | 2 (trnG) | 35 | 1 (trnM) | 4 (trnY, trnR, trnE, trnF) |
M. maoershanensis sp. nov. | 2 (trnW, trnG) | 35 | 2 (trnY, trnE) |
Distribution of G–U base mismatches in tRNAs of M. orthomargina, M. brachycorna sp. nov., and M. maoershanensis sp. nov.
Transfer RNA | M. orthomargina | M. brachycorna | M. maoershanensis | Transfer RNA | M. orthomargina | M. brachycorna | M. maoershanensis |
---|---|---|---|---|---|---|---|
trnI | 0 | 0 | 0 | trnR | 0 | 0 | 0 |
trnQ | 5 | 4 | 4 | trnN | 1 | 1 | 0 |
trnM | 0 | 1 | 0 | trnS1 | 0 | 0 | 2 |
trnW | 0 | 0 | 0 | trnE | 0 | 0 | 0 |
trnC | 3 | 3 | 3 | trnF | 5 | 3 | 5 |
trnY | 3 | 3 | 2 | trnH | 3 | 3 | 5 |
trnL2 | 1 | 1 | 0 | trnT | 0 | 0 | 0 |
trnD | 1 | 1 | 1 | trnP | 5 | 4 | 6 |
trnK | 0 | 1 | 0 | trnS2 | 0 | 1 | 0 |
trnG | 1 | 1 | 1 | trnL1 | 3 | 3 | 2 |
trnA | 1 | 2 | 1 | trnV | 2 | 3 | 3 |
This study supported the non-monophyly of Metrodorinae and Scelimeninae (Figs
In this study (Figs
Previous studies on the classification of Metrodorinae or Tetriginae were based on the morphology of the posterior angles of lateral lobes of pronotum (turned downwards, rounded, or produced forward, truncated), but some investigations suggested that distinguishing between Metrodorinae and Tetriginae based on the shape of the lateral lobes of the pronotum was unreliable (
Holotype : China ♀; Guangxi, Guilin, Xing’an Country, Gaozhai; 25°51'35"N, 110°29'34"E; alt. 652.7 m; 12.VII.2021; Wei’an Deng, Chaomei Huang leg. Paratypes: China 5♀, 1♂; Guangxi, Guilin, Xing’an Country, Gaozhai; 25°51'35"N, 110°29'34"E; alt. 652.7 m; 20.VII.2022, Jieling Luo, Chaomei Huang leg. 6♀, 2♂; Guangxi prov., Guilin, Longsheng Country, Hongtan; 25°36'34"N, 109°57'55"E; alt. 818 m; 04–9.VII.2022; Jieling Luo, Chaomei Huang leg.
Macromotettixoides maoershanensis sp. nov., holotype female A left fore femur, lateral view B left mid femur, lateral view C left hind femur, lateral view D left hind tibia, lateral view E left posterior tarsus, lateral view F subgenital plate of female, lateral view G subgenital plate of female, ventral view. male, paratype H body in dorsal view I body in lateral view.
New species is generally similar to M. orthomargina (Figs
M. orthomargina, female A left fore femur, lateral view B left mid femur, lateral view C left hind femur, lateral view D left hind tibia, lateral view E left posterior tarsus, lateral view F subgenital plate of female, lateral view G subgenital plate of female, ventral view. male, paratype.
Female. short and small size. Body length 7–8 mm, pronotum length 6–7 mm, hind femur length 4–5 mm.
Head. Head and eyes not exserted above pronotal surface (Fig.
Thorax. Pronotum not smooth and has irregular tuberculate (Fig.
Legs. Upper margin of fore and middle femora finely serrated, with carinated, ventral margins undulated (Fig.
Abdomen. Ovipositor narrow and short; upper and lower valvulae with slender saw-like teeth; length of upper valvulae 2.0× its width. Length of subgenital plate 2.5× its width, middle of posterior margin of subgenital plate slightly triangular and projecting (Fig.
Coloration. Body dark brown. Hind tibia yellowish brown, with two light rings in the middle.
Male. Similar to female, but smaller and narrower (Fig.
The new species was named after the type locality, Maoershan, Guangxi, China.
China: Guangxi.
Holotype : China ♀; Guangxi Province, Hechi, Huanjiang, Yangmei’ao; 25°11'41"N, 108°38'51"E; alt. 1169.13 m; 03.IX.2021; Chaomei Huang leg. Paratypes: China 1♂1♀; Guangxi, Hechi, Huanjiang, Yangmei’ao; 25°11'41"N, 108°38'51"E; alt. 1169.13 m; 29.VII.2022; Chaomei Huang and Jieling Luo leg.
The new species is similar to Macromotettixoides maoershanensis sp. nov. from which it differs in width of vertex between eyes 1.3× width of a compound eye (width of vertex between eyes 2.0× width of a compound eye in M. maoershanensis); anterior margin of fastigium not surpassing anterior margin of eye (anterior margin of fastigium surpassing anterior margin of eye in M. maoershanensis); median carina of pronotum slightly elevated and undulated in profile (median carina of pronotum slightly arc-like in profile in M. maoershanensis); ventral margin of middle femora slightly undulate (ventral margin of middle femora distinctly undulate in M. maoershanensis). It is also similar to Macromotettixoides tuberculata Mao, Li & Han, 2020 but differs from the latter by width of vertex between eyes 1.3× width of compound eye (width of vertex between eyes 1.7× width of compound eye in M. tuberculata); antennal grooves inserted far below inferior margin of compound eyes (antennal grooves inserted between inferior margin of compound eyes); hind pronotal process narrowly rounded (hind pronotal process broad in M. tuberculata); lower margin of hind process bend upwards at 1/4 and then tilt straight up, lateral carinae of metazona curved (lower margin of hind process and lateral carinae of metazona slightly straight in M. tuberculata).
Female. Body size small. Body length 8 mm, pronotum length 6–7 mm, hind femur length 4 mm.
Head. Head and eyes exserted above pronotal surface (Fig.
Thorax. The dorsal surface of the pronotum is coarse dorsum with dense granules, anterior margin of pronotum straight; median carina entire and wavy in profile; lateral carinae of prozona slightly parallel; humeral angle obtuse; hind pronotal process narrow and its apex rounded, reaching pregenicular knee (Fig.
Legs. Fore femora and middle femora with slightly undulated ventral margins (Fig.
Macromotettixoides brachycorna sp. nov., holotype female A left hind femur, lateral view B left hind tibia, lateral view C left posterior tarsus, lateral view D subgenital plate of female, lateral view E subgenital plate of female, ventral view. male, paratype F body in dorsal view G body in lateral view.
Abdomen. Ovipositor narrow and long (Fig.
Coloration. Body dark brown or brown; antennae tawny; hind femur yellowish brown in the middle and dark brown around the sides; hind tibia yellowish brown, with two light rings in the middle.
Male. Similar to female, but smaller and narrower (Fig.
The specific epithet is derived from brachycorna, meaning the antennae are shorter and the number of segments is less.
China: Guangxi.
Unfortunately, we do not have access to the species of the South American Tetriginae and Metrodorinae, which makes it impossible to evaluate whether Systolederus + Macromotettixoides truly belong to the subfamily Metrodorinae. As a result, we cannot provide any conclusive evidence to support their classification within this subfamily. Therefore, further research is needed to clarify their taxonomic status and evolutionary relationships with other Southern American species. But the problematics of the Metrodorinae definition in Asia, especially when differentiated from very diverse Tetriginae, it is often seen that some species of Metrodornae are moved to Tetriginae (
Macromotettixoides is an apterous genus, but the non-flying Tetrigidae in the Oriental regions have multiple origins. For example, the genus Hainantettix Deng, 2020 (
Morphological comparison of Macromotettixoides, Epitettix, Hainantettix, Formosatettix, Alulatettix, and Skejotettix.
Characteristics | Macromotettixoides | Epitettix | Hainantettix | Formosatettix | Alulatettix | Skejotettix |
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Wing type | apterous | apterous | apterous | apterous | brachypterous | brachypterous |
Head | not exserted above the pronotum | not exserted above the pronotum | not exserted above the pronotum | not exserted above the pronotum | not exserted above the pronotum | not exserted above the pronotum |
Fastigium of vertex in dorsal view | not surpassing the anterior margin of eyes | distinctly surpassing the anterior margin of eyes | not surpassing the anterior margin of eyes | distinctly surpassing the anterior margin of eyes | not surpassing the anterior margin of eyes | not surpassing the anterior margin of eyes |
Fastigium of vertex | vertex not narrowed toward the front | vertex not narrowed toward the front | vertex very strongly narrowed toward the front drawing the eyes together | vertex not narrowed toward the front | vertex not narrowed toward the front | vertex not narrowed toward the front |
Width of longitudinal furrow of frontal ridge | narrower than antennal groove diameter | 1.3–3.0× antennal groove diameter | 1.6–1.8× antennal groove diameter | narrower than antennal groove diameter | narrower than antennal groove diameter | narrower than antennal groove diameter |
Tegminal sinus | absent | absent | absent | absent | present | present |
Posterior angles of lateral lobes | produced outwards and with truncated apex | produced outwards and with truncated apex | produced outwards and with truncated apex | turned downwards and with rounded apex | turned downwards and with rounded apex | turned downwards and with rounded apex |
Since the genus Macromotettixoides was erected in 2005, a total of 22 species has been described, another six species transferred to this genus (
Although the phylogenetic tree in this study supports the genus Macromotettixoides being assigned to Tetriginae rather than Metrodorinae, it is limited by the available data and cannot fully confirm its taxonomic placement and monophyletic. Therefore, more comprehensive molecular and morphological data are needed to further investigate the evolutionary relationships and taxonomic status of Macromotettixoides.
Thanks to Professor Feng Zhang (Nanjing Agricultural University), Dong Zhang (Lanzhou University), Fangluan Gao (Fujian Agricultural and Forestry University) for their help. Thanks to Professor Josip Skejo (University of Zagreb, Croatia) and an anonymous reviewer for comments and suggestions.
The authors have declared that no competing interests exist.
No ethical statement was reported.
This study was supported by the National Natural Science Foundation of China (32360124, 31960111), the Science & Technology Fundamental Resources Investigation Program of China (2023FY100200) and the Guangxi Natural Science Foundation under Grant No. 2023GXNSFDA026037 and 2020GXNSFBA159032.
Conceptualization, J.-L.L. and W.-A.D. R.-J.Z.; methodology, J.-L.L. and W.-A.D..; software, J.-L.L.; validation, all authors; formal analysis, J.-L.L. and W.-A.D.; investigation, J.-L.L.; resources, W.-A.D. and R.-J.Z.; writing—original draft preparation, J.-L.L.; writing—review and editing, W.-A.D.; visualization, J.-L.L.; supervision, W.-A.D.; project administration, W.-A.D.; funding acquisition, W.-A.D.
Jieling Luo https://orcid.org/0000-0002-5657-3436
Rongjiao Zhang https://orcid.org/0000-0001-5545-856X
Weian Deng https://orcid.org/0000-0002-8023-2498
All of the data that support the findings of this study are available in the main text or Supplementary Information.
Mitochondrial genome comparison of 37 species in Tetrigidae, the initiation and termination codons of PCGs of mitogenomes in Tetrigidae
Data type: docx