Research Article |
Corresponding author: Yun Bu ( buy@sstm.org.cn ) Academic editor: Bruce A. Snyder
© 2023 Ya-Li Jin, Nerivania Nunes Godeiro, Yun Bu.
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:
Jin Y-L, Nunes Godeiro N, Bu Y (2023) Description of the first species of Scutigerella (Symphyla, Scutigerellidae) from China, with mitogenomic and genetic divergence analysis. ZooKeys 1157: 145-161. https://doi.org/10.3897/zookeys.1157.99686
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Scutigerella sinensis Jin & Bu, sp. nov. from China is described and illustrated. It is characterized by a deeply emarginated posterior margin of tergite 2, less differentiated marginal setae on all tergites, absence of seta a3 around the antennal base, and 6–8 setae on the first tergite. The complete mitochondrial genome of the new species is also analyzed and compared with the mitogenome of Scutigerella causeyae. In the reconstructed Neighbor-Joining tree based on COI gene sequences, S. sinensis sp. nov. clusters with S. causeyae, however, with big distances. The genetic divergence among S. sinensis sp. nov. and congeners, species of Hanseniella and Scutigerella, and both families of Symphyla was analyzed using COI gene sequences.
DNA barcode, genetic distance, mitochondrial genome, Myriapoda, symphylans, taxonomy
The class Symphyla Ryder, 1880 is a monophyletic group of myriapods with worldwide distribution (
In recent years, many specimens of Scutigerellidae Bagnall, 1913 were obtained from Shanghai and Beijing and were carefully studied, and most of them belong to the genus Hanseniella Bagnall, 1913. Among those specimens, one species of Scutigerella was identified as new to science and is described in the present paper. It is also the first species of the genus from China. In order to provide further evidence for the new species and clarify its taxonomic position, its complete mitogenome was sequenced and analyzed. In addition, the phylogenetic relationship and genetic divergence of symphylans were analyzed based on DNA barcode sequences.
Soil and litter samples from broad-leaf and bamboo forests from Dajinshan Island, Shanghai were collected during several ecological surveys of soil fauna between 2015–2018, and specimens were extracted using Berlese-Tullgren funnels and preserved in 80% ethanol. Materials from Beijing were collected in Yuan-Ming Yuan Imperial Garden by Mr Rui-Qing Wang in 2021. They were mounted on slides using Hoyer’s solution and dried in an oven at 50 °C. Morphological observations were performed under a phase contrast microscope (Leica DM 2500). Photographs were taken with a digital camera installed on the microscope (Leica DMC 4500). Line drawings were done using a drawing tube. All specimens are deposited in the collections of the Shanghai Natural History Museum (SNHM), Shanghai, China.
The specimens used for the experiment were collected by Ya-Li Jin and Yun Bu from Dajinshan Island on 11 November, 2017. Samples were preserved in absolute ethanol at -20 °C for DNA extraction. Prior to DNA extraction, a single individual was mounted on a temporary slide using absolute ethanol to confirm the species identification. One specimen, preserved in alcohol, was sent to Shanghai Yaoen Biotechnology Co., Ltd, China, where all laboratory procedures, including DNA extraction and library construction were made following custom procedures. DNA was extracted from a single individual of the species using the TIANamp MicroDNA extraction kit (Tiangen Co., Ltd, China). Libraries were constructed using KAPA Hyper Prep Kit (Roche). An Illumina NovaSeq platform was used to produce paired-end reads with 150 bp length. Approximately 10 Gb of data from the species was generated and used to assemble the mitogenomes.
NovoPlasty v.3.8.3 (
Taxonomical and collection information of the species used in the analysis.
Species and voucher | Family | Genus | Country | GenBank number | Reference |
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Scutigerella sinensis sp. nov. JYL-DJS2017011 | Scutigerellidae | Scutigerella | China | OQ165321 | Present study |
Scutigerella causeyae | Scutigerellidae | Scutigerella | Germany | NC008453 |
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Scutigerella sp. WAMT144261 | Scutigerellidae | Scutigerella | Australia | MW021294 | Cullen and Harvey 2020 (unpublished) |
Scutigerella sp. WAMT144298 | Scutigerellidae | Scutigerella | Australia | MW021295 | Cullen and Harvey 2020 (unpublished) |
Scutigerella sp. WAMT145461 | Scutigerellidae | Scutigerella | Australia | MW021296 | Cullen and Harvey 2020 (unpublished) |
Scutigerella sp. WAMT145462 | Scutigerellidae | Scutigerella | Australia | MW021297 | Cullen and Harvey 2020 (unpublished) |
Scutigerella sp. WAMT145463 | Scutigerellidae | Scutigerella | Australia | MW021298 | Cullen and Harvey 2020 (unpublished) |
Scutigerella sp. PU234 | Scutigerellidae | Scutigerella | Australia | MT457863 | Cullen and Harvey 2020 (unpublished) |
Hanseniella sp. BMR00202 | Scutigerellidae | Hanseniella | Australia | MT902530 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00229 | Scutigerellidae | Hanseniella | Australia | MT902546 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00230 | Scutigerellidae | Hanseniella | Australia | MT902547 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00231 | Scutigerellidae | Hanseniella | Australia | MT902548 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00232 | Scutigerellidae | Hanseniella | Australia | MT902549 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00243 | Scutigerellidae | Hanseniella | Australia | MT902557 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR00364 | Scutigerellidae | Hanseniella | Australia | MT902595 | Gunawardene et al. 2020 (unpublished) |
Hanseniella sp. BMR01208 | Scutigerellidae | Hanseniella | Australia | MT902776 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. FRL-2015 | Scutigerellidae | undetermined | Colombia | KP696390 |
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Scutigerellidae sp. BMR00070 | Scutigerellidae | undetermined | Australia | MT902426 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR00071 | Scutigerellidae | undetermined | Australia | MT902427 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR00241 | Scutigerellidae | undetermined | Australia | MT902555 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR00242 | Scutigerellidae | undetermined | Australia | MT902556 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR00244 | Scutigerellidae | undetermined | Australia | MT902558 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR00641 | Scutigerellidae | undetermined | Australia | MT902704 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR01199 | Scutigerellidae | undetermined | Australia | MT902772 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR01576 | Scutigerellidae | undetermined | Australia | MT621062 | Gunawardene et al. 2020 (unpublished) |
Scutigerellidae sp. BMR01578 | Scutigerellidae | undetermined | Australia | MT621064 | Huey and Floeckner 2020 (unpublished) |
Scutigerellidae sp. BMR01587 | Scutigerellidae | undetermined | Australia | MT621072 | Huey and Floeckner 2020 (unpublished) |
Symphylella sp. YG-2006 | Scolopendrellidae | Symphylella | China | NC011572 |
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In order to make a comprehensive analysis of genetic divergences among symphylans, DNA barcode sequences (COI gene, 658 base pairs) of 26 sequences of the family Scutigerellidae and one sequence of the family Scolopendrellidae Newport, 1844 (outgroup) were downloaded from GenBank and analyzed. The detailed information and accession numbers of the 28 sequences analyzed in this study are listed in Table
After publication, mitogenome sequence and raw sequencing data will be available in GenBank (NCBI) at https://www.ncbi.nlm.nih.gov/ under the accession numbers OQ165321/PRJNA900014.
Class Symphyla Ryder, 1880
Family Scutigerellidae Bagnall, 1913
Scolopendrella immaculata Newport, 1845. Valid name: Scutigerella immaculata (Newport, 1845).
Trunk with 15 tergites. Four macrosetae (a1–a4) around the antennal base, rarely seta a3 absent. Posterior margins of tergites emarginated. Last tergite with a deep cavity between cerci. First pair of legs with 4 segments, others with 5 segments. Styli present at the base of legs 3–12. Coxal sacs present at the base of legs 3–10.
Sub-cosmopolitan (
Scutigerella sinensis sp. nov. is characterized by absence of a3 seta around the antennal base, 6–8 setae on the first tergite, deeply emarginated posterior margin of tergite 2, 28–37 marginal and 41–57 inner setae on tergite 2, less differentiated marginal setae on all tergites, femur of first pair of legs without a conspicuous ventral process, posterior styli without a lateral seta, cavity of fifteenth tergite V-shaped, tarsus of last pair of legs moderately set with setae, cerci 2.7–3.4 times as long as width, cerci densely covered with subequal setae, cerci without expansion in terminal area.
Holotype : male (slide no. SH-DJS-SY2015009) (SNHM), China, Shanghai, Dajinshan Island, extracted from soil samples of bamboo forest, alt. 103 m, 30°41'N, 121°26'E, 30-VI-2015, coll. Y. Bu & Y. L. Jin. Paratypes: 1 female (slide no. SH-DJS-SY2017001), ibidem, 11-XI-2017; 1 female (slide no. SH-DJS-SY2017002), ibidem, extracted from soil samples of broad-leaf forest, 11-XI-2017, coll. Y. Bu & Y. L. Jin; 1 female (slide no. SH-DJS-SY2018003), ibidem, 24-IV-2018, coll. Y. Bu & J. Y. Li; 1 male (slide no. SH-DJS-SY2018001), ibidem, extracted from soil samples of broad-leaf forest, 24-X-2018, coll. Y. Bu & J. Y. Li; 1 female (slide no. BJ-YMY-SY2021001), China, Beijing, Yuan-Ming Yuan Imperial Garden, extracted from soil samples of a deserted field with herbaceous plants, alt. 60 m, 40°1'N, 116°17'E, 15-IV-2021, coll. R. Q. Wang. Non-type specimens: 1 juvenile with 8 pairs of legs (slide no. SH-DJS-SY2015002), same data as holotype; 1 juvenile with 9 pairs of legs (slide no. SH-DJS-SY2015111), ibidem, 22-IX-2015, coll. Y. Bu & Y. L. Jin; 1 juvenile with 11 pairs of legs (slide no. SH-DJS-SY2018002), ibidem, 24-IV-2018, coll. Y. Bu.
Adult body 3.4 mm long on average (3.0–4.3 mm, N = 6), holotype 3.2 mm (Fig.
Scutigerella sinensis Jin & Bu, sp. nov. A habitus, dorsal view in alcohol B head, dorsal view (a1, a2 and a4–macrosetae around antennal base) C tergites 1–2 D tergite 3 E first maxilla and the right part of second maxilla (arrows indicate spined organs) F head, ventral view G male genitalia H right 10–11 antennomeres, dorsal view (arrows indicate spiniform sensory organs) I right 13–14 antennomeres, ventral view (arrows indicate sensory setae) J stylus and coxal sac on base of leg 5 (arrow indicates stylus). Scale bars: 500 μm (A); 20 μm (B–J).
Head
length 300–350 μm, width 320–420 μm, broadest part just posterior of midlength, dorsally covered with straight setae of varying lengths (Fig.
Tömösváry organ
subspherical, length 20–22 μm, width 15–20 μm, 0.3–0.4 times as wide as greatest diameter of third antennomere (Fig.
Mouthparts. Mandible similar to Hanseniella. Pars incisivus with four distinct thick teeth, pars molaris with four smaller teeth and one proximal spine, lacinia mobilis with 2 pubescent processes observed from lateral view under light microscope (Fig.
Scutigerella sinensis Jin & Bu, sp. nov. A mandible, lateral view (pi–pars incisivus, pm–pars molaris, lm–lacinia mobilis) B first maxilla C right 6–7 antennomeres, dorsal view (co–conical sensory organ, spo–spiniform sensory organs, so–spined sensory organs) D right 13–14 antennomeres, ventral view (S–sensory setae) E terminal two antennomeres, dorsal view F femur and tibia of leg 1, ventral view. Scale bars: 20 μm.
Antennae
with 19–29 antennomeres (holotype with 29), about 0.4 of body length. First antennomere cylindrical, 1.3–2.5 times wider than long (length 30–45 μm, width 50–75μm), with 5–6 setae in one whorl, longest seta 28–30 μm, about half of antennomere width. Second antennomere 1.3–1.9 times wider than long (width 48–65 μm, length 33–40 μm), with 7–9 setae evenly inserted, longest seta inserted outer-dorsally, about 0.5–0.7 times as long as antennomere width. Third antennomere 1.3–1.9 times wider than long (length 25–40 μm, width 45–65μm), with primary whorl of 7–10 setae, longest seta 0.5–0.7 times as long as antennomere width. Setae on proximal antennomeres longer and on distal antennomeres shorter. Proximal antennomeres each with only primary whorl of setae. Secondary whorl setae appear from antennomeres 6–8 to penultimate antennomere (Figs
Numbers of normal setae and sensory organs on antennae of Scutigerella sinensis Jin & Bu sp. nov. (holotype).
Antennomere | Normal setae | Spiniform sensory organs | Spined sensory organs | Conical sensory organs | Ventral sensory setae |
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1 | 5 | ||||
2 | 9 | 1 | |||
3 | 10 | 1 | |||
4 | 10 | 1 | 1 | 1 | |
5 | 11 | 3 | 1 | 1 | |
6 | 14 | 4 | 1 | 1 | |
7 | 17 | 4 | 1 | 1 | 1 |
8 | 18 | 4 | 1 | 1 | |
9 | 19 | 4 | 1 | 1 | 1 |
10 | 19 | 4 | 1 | 1 | |
11 | 20 | 4 | 1 | 1 | 1 |
12 | 20 | 4 | 1 | 1 | |
13 | 20 | 5 | 1 | 1 | |
14 | 20 | 4 | 1 | 1 | |
15 | 19 | 6 | 1 | 1 | 1 |
16 | 18 | 6 | 1 | 1 | |
17 | 17 | 5 | 1 | 1 | |
18 | 17 | 5 | 1 | 1 | |
19 | 17 | 5 | 1 | 1 | 1 |
20 | 18 | 5 | 1 | 1 | |
21 | 17 | 6 | 1 | 1 | 1 |
22 | 16 | 5 | 0 | 1 | |
23 | 17 | 6 | 1 | 1 | |
24 | 17 | 6 | 1 | 1 | |
25 | 18 | 6 | 1 | 1 | 1 |
26 | 18 | 6 | 0 | 1 | |
27 | 14 | 8 | 1 | 1 | 1 |
28 | 16 | 5 | 1 | 1 | |
29 | 22 | 7 | 3 |
Tergites. Tergite 1 rudimentary, with 6–8 subequal setae in one row (Fig.
Legs. First pair of legs with 4 segments, trochanter absent; femur 1.8–2.0 times longer than wide (length 38–85 μm, width 28–43 μm), with cuticular reticulation (Fig.
Coxal sacs
present at bases of legs 3–10, fully developed, each with 5 or 6 setae on surface (Fig.
Styli
present at base of legs 3–12, 2.6–4.3 times as long as wide (33–58 μm, 10–20 μm), pubescent, with two distal setae, subapical seta (15–23 μm) 0.3–0.5 times as long as stylus, apical seta (8–10 μm) 0.2–0.3 times as long as stylus, both with pointed apex (Fig.
Sense calicles located on two ventral protuberances of last tergite, posterior to base of leg 12, with smooth margin around pit. Sensory seta inserted in cup center, extremely long (235–275 μm).
Cerci
about 0.7–0.9 of head length, distinctly shorter than leg 12, 2.7–3.4 times as long as its greatest width (240–300 μm, 80–110 μm), moderately covered with subequal setae (Fig.
Male genitalia
with 30 setae in total in holotype, without specialized setae (Fig.
This new species is named after the country of origin, from the Latin adjective sinensis, meaning Chinese.
China (Shanghai, Beijing).
Our current investigation indicates that Scutigerella sinensis sp. nov. is a rare species in natural habitats with very low density. We found about ten individuals among several hundred symphylans from plots of different vegetation. This Scutigerella is often coexisting with other dominant species of Hanseniella and Symphylella in the upper soil layer (0–10 cm) or humus.
The head chaetotaxy was briefly described in the previous studies of Scutigerella, usually with only shapes and numbers mentioned. The macrosetae around the base of the antenna of Scutigerella have been noticed and named by former researchers, and all species examined until now have a complete set of four macrosetae (a1–a4), which was deemed as a good diagnostic character in the taxonomy of Scutigerella (
The mitochondrial genome of Symphyla until now was only known from two species: Scutigerella causeyae and one undetermined species of Symphylella (
Start | End | Length (bp) | Direction | Start/Stop codons | Gene name | Gene product |
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181 | 1303 | 1122 | + | ATG/TAA | CYTB | Cytochrome C Oxidase 1 |
1307 | 1368 | 62 | + | trnS2 (uga) | tRNA-Ser | |
1386 | 2286 | 901 | - | ATA/TAA | ND1 | NADH Dehydrogenase 1 |
2298 | 2360 | 63 | - | trnL1 (uag) | tRNA-Leu | |
2360 | 2425 | 66 | - | trnL2 (uaa) | tRNA-Leu | |
2371 | 3656 | 1286 | - | l-rRNA | 16S ribosomal RNA | |
3604 | 3665 | 62 | - | trnV (uac) | tRNA-Val | |
3659 | 4408 | 750 | - | s-rRNA | 12S ribosomal RNA | |
4369 | 4425 | 57 | - | trnQ (uug) | tRNA-Gln | |
4425 | 4722 | 297 | CR | Control Region | ||
4723 | 4786 | 64 | + | trnM (cau) | tRNA-Met | |
4788 | 4851 | 64 | + | trnI (aau) | tRNA-Ile | |
4881 | 5871 | 991 | + | ATT/TAA | ND2 | NADH Dehydrogenase 2 |
5876 | 5939 | 64 | + | trnW (uca) | tRNA-Trp | |
5931 | 5986 | 56 | - | trnC (gca) | tRNA-Cys | |
5985 | 6046 | 62 | - | trnY (gua) | tRNA-Tyr | |
6038 | 7582 | 1545 | + | ATA/TAA | COX1 | Cytochrome C Oxidase I |
7581 | 8256 | 676 | + | ATG/TAA | COX2 | Cytochrome C Oxidase II |
8258 | 8321 | 64 | + | trnK (cuu) | tRNA-Lys | |
8321 | 8387 | 67 | + | trnD (guc) | tRNA-Asp | |
8387 | 8549 | 163 | + | ATT/TAA | ATP8 | ATP synthase F0 subunit 8 |
8542 | 9214 | 673 | + | ATG/TAA | ATP6 | ATP synthase F0 subunit 6 |
9213 | 10014 | 802 | + | ATG/TAA | COX3 | Cytochrome C Oxidase III |
9997 | 10052 | 56 | + | trnG (ucc) | tRNA-Gly | |
10052 | 10406 | 355 | + | ATT/TAA | ND3 | NADH Dehydrogenase 3 |
10412 | 10472 | 61 | + | trnA (ugc) | tRNA-Ala | |
10472 | 10534 | 63 | + | trnR (ucg) | tRNA-Arg | |
10537 | 10599 | 63 | + | trnN (guu) | tRNA-Asn | |
10599 | 10653 | 55 | + | trnS1 (gcu) | tRNA-Ser | |
10653 | 10715 | 63 | + | trnE (uuc) | tRNA-Glu | |
10713 | 10769 | 57 | - | trnF (gaa) | tRNA-Phe | |
10768 | 12436 | 1669 | - | ATT/TAG | ND5 | NADH Dehydrogenase 5 |
12445 | 12499 | 55 | - | trnH (gug) | tRNA-His | |
12498 | 13821 | 1324 | - | ATG/TAG | ND4 | NADH Dehydrogenase 4 |
13814 | 14093 | 280 | - | ATG/TAA | ND4L | NADH Dehydrogenase 4L |
14095 | 14157 | 63 | - | trnP (ugg) | tRNA-Pro | |
14158 | 14218 | 61 | + | trnT (ugu) | tRNA-Thr | |
14217 | 181 | 477 | + | ATT/TAA | ND6 | NADH Dehydrogenase 6 |
Compared to the mitogenome of the congeneric species S. causeyae, the new sequence is 125 bp smaller and differs in the relative position of three tRNA genes (Q, M, I) located next to the control region. Additionally, the tRNA-Valine is located between the rRNAs, like in the inferred arthropod ground pattern (
Mitochondrial gene arrangements of Scutigerella sinensis sp. nov. compared to S. causeyae and the arthropod ground pattern (adapted from
In the Neighbor-Joining tree constructed based on DNA barcoding sequences, S. sinensis sp. nov. clustered with S. causeyae (Fig.
The pairwise genetic distance of 28 sequences of symphylan species based on the K2P model is given in the Suppl. material
Genetic distances of Symphyla analyzed by mitochondrial COI gene (K2P model).
Level | Mean | Minimum | Maximum |
---|---|---|---|
Scutigerella sinensis sp. nov. vs congeners | 0.2747 | 0.2280 | 0.2946 |
Interspecific distances within the genus Scutigerella | 0.2638 | 0.1883 | 0.3248 |
Interspecific distances within the genus Hanseniella | 0.2084 | 0.1738 | 0.2343 |
Conspecific distances of the genus Hanseniella | 0.0550 | 0.0160 | 0.0961 |
Intergeneric distances between Scutigerella and Hanseniella | 0.2376 | 0.1700 | 0.3364 |
Interfamiliar distance between Scutigerellidae and Scolopendrellidae | 0.3170 | 0.2947 | 0.3636 |
We cordially thank Dr Bi-Cheng Li for his careful organization of the expedition to Dajinshan Island, and Dr Jing-Yang Li and Mrs Si-Qi Yang for their generous help in the collection. Special thanks are given to Mr Rui-Qing Wang for the collection of specimens from Yuan-Ming Yuan Imperial Garden in Beijing. We appreciate Prof. José G. Palacios-Vargas (Mexico) for the linguistic corrections of the manuscript and valuable advice. We sincerely thank Dr Nikolaus Szucsich (Austria) and Dr Carlos Alberto Martínez Muñoz (Finland) for their valuable comments in review of the manuscript. This research was supported by the National Natural Science Foundation of China (no: 32170471) and the Research Foundation of Shanghai Science and Technology Museum.
K2P distances between different speices of Symphyla analyzed by the mitochondrial COI gene
Data type: table (excel file)