Research Article |
Corresponding author: Yun-Xia Luan ( yxluan@sibs.ac.cn ) Academic editor: Wanda M. Weiner
© 2016 Yun Bu, Yao Ma, Yun-Xia Luan.
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:
Bu Y, Ma Y, Luan Y-X (2016) Paracerella Imadaté in China: the description of a new species and the analysis of genetic differences between populations (Protura, Acerentomata, Nipponentomidae). ZooKeys 604: 1-11. https://doi.org/10.3897/zookeys.604.8737
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The genus Paracerella Imadaté, 1980 is recorded from China for the first time, with the description of a new species, Paracerella sinensis sp. n. Paracerella sinensis is characterized by four pairs of A-setae on tergite I, the presence of setae Pc and P3a on tergite VII, eight A-setae on tergite VIII, the presence of seta Pc on both sternites VI and VII, and 4/2 setae on sternite VIII, which are different from all other members of the genus. The key to the four species of the genus is updated. In addition, DNA barcodes of four populations are sequenced and their genetic differences are analyzed.
DNA barcodes, genetic divergences, identification key, sensillum, taxonomy
The genus Paracerella Imadaté, 1980 is separated from Verrucoentomon Rusek, 1974 by the parallel position of the foretarsal sensilla d and a’ to t2. It is characterized by having a distinct calyx with racemose appendices on its surface, three pairs of A-setae on meso- and metanota, filiform foretarsal sensillum t1, three A-setae on sternites I–VII, posterior position of setae P3 on tergites II–VI, well-developed labial palps, two subequal setae on abdominal legs II and III and well-developed striate band on segment VIII.
As a small genus in Protura, Paracerella has only three known species: P. shiratki (Imadaté, 1964) recorded from Japan (
During field work in Inner Mongolia and Heilongjiang Provinces, northeast China, plenty of proturan specimens of Paracerella were found. They were identified as a new species and are described in the present paper, and an updated key to the genus was also provided. In addition, the DNA barcodes of the new species from four localities were sequenced and analyzed, the morphological identification was confirmed, and the genetic differences between different populations were revealed.
Specimens were collected by Tullgren funnels. All specimens were mounted on slides in Hoyer’s medium and dried at 60 °C. Specimens were identified and drawn with the aid of a NIKON E600 phase contrast microscope. The photos were taken by digital camera Nikon DXM1200. Type specimens are deposited in the Shanghai Entomological Museum (SEM), Institute of Plant Physiology & Ecology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, and Shanghai Natural History Museum (SNHM).
Abbreviations used in the text follow the paper of
For the analysis of genetic differences, genomic DNA was extracted from each individual separately by means of a non-destructive method (
Holotype, female (No. LM6-12D) (SEM), China, Inner Mongolia Province, Balin town, Lama Hill, extracted from the soil samples under some small pine trees, 48°19.969'N, 122°19.160'E, elev. 562 m, 12-VIII-2014, coll. W.J. Chen, C.W. Huang, Y. Ma, Y.X. Luan, and M. Potapov. Paratypes, 4 females (nos. LM6-10, LM6-11, LM6-13D, LM6-14D) (SEM), same data as holotype; 3 females (nos. HH1-1D, HH1-3D, HH1-4D) (SEM), CHINA, Heilongjiang Province, Heihe City, from the soil samples under some black birches of Tree Farm 727, 50°15.491'N, 126°48.434'E, elev. 410 m, 15-VIII-2014; 11 females (nos. WHS4-2D, WHS5-2D, WHS6-2D, WHS4-6-1, WHS4-6-2, WHS5-3-2, WHS5-4-1, WHS5-4-3 in SEM, nos. WHS4-5-1, WHS4-5-2, WHS4-5-3 in SNHM), China, Heilongjiang Province, Wudalianchi City, from three soil samples of Wohu Hill, 48°39.252'N, 126°02.281'E, elev. 480 m, 17-VIII-2014; 5 females (nos. DZH2-1D, DZH2-2D, DZH2-3, DZH2-12D, DZH2-16) (SEM), China, Heilongjiang Province, Wudalianchi City, from the soil sample under some larches in Dazhanhe National Forest Park, 48°41.726'N, 127°40.556'E, elev. 327 m, 18-VIII-2014. Other materials,1 maturus junior (no. HH7-1) (SEM), China, Heilongjiang Province, Heihe City, from the soil samples under some black oaks of Tree Farm 733, 50°13.909'N, 126°51.887'E, elev. 517 m, 15-VIII-2014; 1 maturus junior (no. WHS6-3-2) (SEM), China, Heilongjiang Province, Wudalianchi City, from three soil samples of Wohu Hill, 48°39.252'N, 126°02.281'E, elev. 480 m, 17-VIII-2014; 3 maturi juniores (nos. DZH2-18, DZH 2-19, DZH2- 20) (SEM), 2 larvae II (nos. DZH2-4, DZH2-17) (SEM), China, Heilongjiang Province, Wudalianchi City, from the soil sample under some larches in Dazhanhe National Forest Park, 48°41.726'N, 127°40.556'E, elev. 327 m, 18-VIII-2014. All specimens are collected by W. J. Chen, C.W. Huang, Y. Ma, Y.X. Luan, and M. Potapov. Twelve specimens (nos. LM6-12D, LM6-13D, LM6-14D, HH1-1D, HH1-3D, HH1-4D, WHS4-2D, WHS5-2D, WHS6-2D, DZH2-1D, DZH2-2D and DZH2-12D) are voucher specimens retrieved after DNA extraction.
Paracerella sinensis sp. n. is characterized by four pairs of A-setae on tergite I, the presence of seta Pc and P3a on tergite VII, 8 A-setae on tergite VIII, the presence of seta Pc on sternites VI and VII, 4/2 setae on sternite VIII, which are different to any other members of the genus, foretarsal sensillum a extremely long, surpassing base of sensillum e, sensilla d and a’ located in subequal level with t2, acrostyli of female squama genitalis each with two fine flaps.
Adult body length 1150–1450 μm (n = 24), body yellow-brown color (Fig.
Head (Fig.
Paracerella sinensis sp. n. holotype. A Head, dorsal view (cp = clypeal pore, fp = frontal pore) B pseudoculus C canal of maxillary gland D labial palpus E maxillary palpus (d = dorsal sensillum, v = ventral sensillum) F foretarsus, exterior view G foretarsus, interior view H foretarsus, interolateral view (paratype No. LM6-14D) I comb J female quama genitalis. Scale bars: (A, F–H) 50 μm; others, 20 μm.
Foretarsus (Fig.
Thorax. Thoracic chaetotaxy given in Table
Segment | Dorsal | Ventral | |||
---|---|---|---|---|---|
Formula | Setae | Formula | Setae | ||
Th. | I | 4 | 1, 2 | 4 + 4 6 |
A1, 2, M1, 2 P1, 2, 3 |
II | 8 16 |
A2, 3, 4, M P1, 1a, 2, 2a, 3, 3a, 4, 5 |
5 + 2 4 |
Ac, 2, 3, M P1, 2 |
|
III | 8 16 |
A2, 3, 4, M P1, 1a, 2, 2a, 3, 3a, 4, 5 |
7 + 2 4 |
Ac, 1, 2, 3, M P1, 2 |
|
Abd. | I | 8 12 |
A1, 2, 3, 5 P1, 1a, 2, 2a, 3, 4 |
3 4 |
Ac, 2 P1, 1a |
II–III | 10 16 |
A1, 2, 3, 4, 5 P1, 1a, 2, 2a, 3, 4, 4a, 5 |
3 5 |
Ac, 2 Pc, 1a, 2 |
|
IV–V | 10 16 |
A1, 2, 3, 4, 5 P1, 1a, 2, 2a, 3, 4, 4a, 5 |
3 8 |
Ac, 2 P1, 1a, 2, 3 |
|
VI | 10 16 |
A1, 2, 3, 4, 5 P1, 1a, 2, 2a, 3, 4, 4a, 5 |
3 9 |
Ac, 2 Pc, 1, 1a, 2, 3 |
|
VII | 10 19 |
A1, 2, 3, 4, 5 Pc,1, 1a, 2, 2a, 3,3a, 4, 4a, 5 |
3 9 |
Ac, 2 Pc, 1, 1a, 2, 3 |
|
VIII | 8 15 |
A1, 2, 4, 5 Mc, 2, 3, 4, P2, 3, 4, 5 |
4 2 |
1, 2 1a |
|
IX | 12 | 1, 1a, 2, 2a, 3, 4 | 4 | 1, 2 | |
X | 10 | 1, 2, 2a, 3, 4 | 4 | 1, 2 |
Abdomen. Abdominal chaetotaxy given in Table
Paracerella sinensis sp. n. holotype. A Tergite VII (psm= posterosubmedial) B tergite VIII C sternite I D sternite II E sternite IV F sternite VI (spm= sternal posteromedial) G sternite VII H striate band of abdominal VIII I Tergite VIII–XII J sternites VIII–XII. Arrows indicate pores. Scale bars: 20 μm.
Tergites I–III and VII with pores psm and al, IV–VI with pores psm, al and psl, VIII with pores psm only, IX–XI without pores, XII with single medial pore. Pores psm on tergite VII close to seta P1 (Fig.
Abdominal appendages I, II, III with 2, 1, 1 segments and 4, 2, 2 setae respectively (Fig.
The species is named after the Latin name of China, the place where the species was found.
Inner Mongolia and Heilongjiang, China.
The new species is placed in the genus Paracerella because of the three pairs of A-setae on both meso- and metanota, filiform sensillum t1 on foretarsus, sensilla d and a’ located in subequal level with t2, and well-developed striate band. Paracerella sinensis sp. n. can be easily distinguished from the other three species of the genus by the chaetotaxy of tergites I, IV and VIII, sternites VI–VIII, as well as the length of foretarsal sensillum a.
Among 24 adults of P. sinensis observed, the length of sensillum a is variable between individuals: in most specimens it can surpass base of e (holotype and most of paratypes) (Fig.
1 | Tergites I–VI with seta P1a, sternite I with 4 posterior setae | 2 |
– | Tergites I–VI without seta P1a, sternite I with 2 posterior setae | P. monterey Shrubovych, 2012; USA (California) |
2 | Tergite VII without Pc and P3a setae, sternite VI without Pc seta | 3 |
– | Tergite VII with Pc and P3a setae, sternite VI with Pc seta | P. sinensis sp. n.; China (Inner Mongolia, Heilongjiang) |
3 | Tergite VII with 8 A-setae and without seta P1a, tergite VIII with 6 A-setae | P. americana Imadaté, 1980; USA (California) |
– | Tergite VII with 6 A-setae and with P1a seta, tergite VIII with 4 A-setae | P. shiratki (Imadaté, 1964); Japan (Hokkaido) |
The standard DNA barcoding sequences (COI genes) of eight individuals (voucher species nos. LM6-12D, LM6-14D, HH1-2D, WHS4-2D, WHS5-2D, WHS6-2D, DZH2-1D and DZH2-2D) from one locations in Inner Mongolia (LM) and three locations in Heilongjiang (HH, WHS and DZH) were sequenced and deposited in GenBank (accession numbers KU983757-KU983764). Each sequence contains 658 base pairs of nucleotides that encoding 219 amino acids. The average nucleotide composition is A = 25.2%, T = 41.5%, C = 15.9%, and G = 17.4%.
The K2P genetic divergences of nucleotides for barcode sequences are 0-3.78% between individuals within the same population, and 0.46%-12.54% between individuals from different populations. The numbers of different coded amino acids for this sequence are 0-3 between individuals within the same populations, and 1-4 between individuals from different populations. Except that the COI gene sequence of WHS4-2D is more similar to COI of HH1-2D than to COI of WHS5-2D and WHS6-2D, our data show low genetic variation within populations (LM, WHS, and DZH), but reveal high genetic differentiation among four geographic populations (Table
The K2P genetic distances of DNA barcodes (COI gene) in Paracerella sinensis sp. n.
LM6-12D | LM6-14D | HH1-2D | WHS4-2D | WHS5-2D | WHS6-2D | DZH2-1D | DZH2-2D | |
---|---|---|---|---|---|---|---|---|
LM6-12D | ||||||||
LM6-14D | 0.0000 | |||||||
HH1-2D | 0.1211 | 0.1211 | ||||||
WHS4-2D | 0.1173 | 0.1173 | 0.0046 | |||||
WHS5-2D | 0.1251 | 0.1251 | 0.0346 | 0.0362 | ||||
WHS6-2D | 0.1193 | 0.1193 | 0.0362 | 0.0378 | 0.0046 | |||
DZH2-1D | 0.1235 | 0.1235 | 0.1214 | 0.1214 | 0.1197 | 0.1178 | ||
DZH2-2D | 0.1254 | 0.1254 | 0.1233 | 0.1233 | 0.1216 | 0.1197 | 0.0015 |
The intraspecific distances of most insects are very low.
We offer our cordial gratitude to Dr. W. J. Chen, Mr. C. W. Huang and Dr. M. B. Potapov (Russia) for their help during the collection of specimens, and Mr. R. D. Xie for his instructive advice. We would like to thank Dr. Nikolaus Szucsich (Austria), Dr. Julia Shrubovych (Ukraine), and one anonymous reviewer who helped to improve our manuscript. This study was supported by the National Natural Sciences Foundation of China (nos: 31471958, 31201706, 31272298), the Youth Innovation Promotion Association of the CAS (no. 2013183), NSFC-RFBR Cooperative Research Project (31411130193 / 11-04-91179-GFENa, RFBR 14-04-91169M), and Open Project (no. 2009DP17321409) of Key Laboratory of Insect Developmental and Evolutionary Biology, CAS.