Morphological Re-Description and 18 S rDNA Sequence Confirmation of the Pinworm Aspiculuris tetraptera (Nematoda, Heteroxynematidae) Infecting the Laboratory Mice Mus musculus

Abdel-Gaber, Rewaida; Abdel-Ghaffar, Fathy; Al Quraishy, Saleh; Morsy, Kareem; Saleh, Rehab; Mehlhorn, Heinz

doi:10.21307/jofnem-2018-026

Figures & Tables

A–G, Line drawings of different body parts of Aspiculuris tetraptera. A, Lateral view of female worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN) and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system characterized with a uterus filled with numerous eggs (EG), ovijector apparatus (OA), vagina (VA) and vulval opening (VU) surrounded by two fleshy vulval lips (VL). B, Lateral view of male worm with mouth opening surrounded by three lips with cephalic papillae (CP) and amphids (AM), followed by muscular esophagus (E), esophageal bulb region (EOB), intestine (IN), rectum (R) with rectal gland (RG), anal opening (AN), and ending with a long tapered tail (T). Note, transverse annulated (TA) cuticle, and the genital system with testes (TE), cloacal opening (CO) surrounded by precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). C–G, High magnifications of: C, Face view of anterior extremity of female worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). D, Face view of anterior extremity of male worm mouth opening (MO) surrounded by three lips (L) with cephalic papillae (CP) and amphids (AM) with cervical alae (CA). E, Ovejector region (OA) of female showing vulva opening (VU), two fleshy vulval lips (VL), muscular vagina (VA), and eggs collected (EG) from uterus. F, Posterior end of male worm showing the cloacal opening (CO) with caudal papillae of precloacal papillae (PCP), adcloacal papillae (ACP), postadcloacal papillae (PACP), median postadcloacal papillae (MPACP), and posterior papillae (PP). G, Morula (M) surrounded by egg shell (ES).

Phylogenetic tree generated by neighbor-joining analyses of the partial SSU rDNA sequence of Aspiculuris tetraptera and oxyurid species with the strongest BLAST matches and in part with some ascarid species. GenBank accession numbers are given after the species names. The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. Oxyurid parasite examined in the present study is bolded.

Nematoda species used in the phylogenetic analysis of Aspiculuris tetraptera in the present study_

Parasite species	Order/family	Host species	Source	Accession no.	Sequence length (bp)	Divergence	Percent identity (%)
Cosmocerca japonica	Ascaridida/Cosmocercidae	Rana ornativentris	GenBank	LC052782	749	5.2	89.0%
Parascaris equorum	Ascaridida/Ascarididae	Africa lion and wolf	GenBank	JN617987	814	5.2	89.0%
Cucullanus extraneus	Rhabditida/Cucullanidae	Pomacanthus maculosus	GenBank	KT192060	1,150	4.9	90.0%
Pseudanisakis rajae	Rhabditida/Acanthocheilidae	Elasmobranchs	GenBank	JN392470	903	4.9	90.0%
Enterobius vermicularis	Oxyurida/Oxyuroidae	Human children	GenBank	HQ646164	2,867	5.2	91.0%
Skrjabinema kamosika	Oxyurida/Oxyuroidae	Capricornis crispus	GenBank	AB699691	898	4.9	91.0%
Aspiculuris tianjinensis	Oxyurida/Heteroxynematidae	Mus musculus domesticus	GenBank	KT175733	967	3.2	92.0%
Aspiculuris tetraptera	Oxyurida/Heteroxynematidae	M. musculus domesticus	GenBank	KT175725	936	1.4	97.0%
Aspiculuris dinniki	Oxyurida/Heteroxynematidae	Myodes glareolus	GenBank	KT175736	995	0.6	98.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. glareolus	GenBank	KT175728	954	0.6	98.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. glareolus	GenBank	KT175729	964	0.6	98.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	KJ143615	419	0.1	99.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	KJ143618	419	0.1	99.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	KJ143617	419	0.1	99.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	KJ143616	419	0.1	99.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	EF464551	3,676	0.1	99.0%
A. tetraptera	Oxyurida/Heteroxynematidae	M. musculus musculus	GenBank	EU263107	1,032	0.1	99.0%

Main morphological features and measurements of female Aspiculuris tetraptera compared with previous studies_

Related species	Aspiculuris ackerti	Aspiculuris artigasi	Aspiculuris versterae	Aspiculuris tetraptera	Aspiculuris ackerti	A. tetraptera	A. tetraptera	A. tetraptera	Aspiculuris huascaensis	Aspiculuris tianjinensis	A. tetraptera	A. tetraptera	A. tetraptera
Parameters	Kruidenier and Mehra (1959)	Araujo (1965)	Hugot (1980)	Hugot (1980)	Miller and Schmidt (1982)	Kohn and Macedo (1984)	Pinto et al. (1994)	Landaeta-Aqueveque et al. (2007)	Falcón-Ordaz et al. (2010)	Liu et al. (2012)	Khalil et al. (2014)	Abdel-Gaber and Fol (2015)	(Present study)
Host species	Neotoma albigtda	Mus musculus	Mastomys natalensis	M. natalensis	Neotoma cinerea	Haemulon sciurus	M. musculus	M. musculus	M. musculus	Clethrionomys rufocanus	M. musculus	M. musculus	M. musculus
Host locality	Coconimo, Arizona	Sao Paulo, Brazil	Onderstepoort, South Africa	Maracay, Venezuela	Colorado, Idaho, USA	Rio de Janeiro, Brazil	Río de Janeiro, Brazil	Santiago, Chile	Hidalgo, Mexico	Tianjin, China	Cairo, Egypt	Cairo, Egypt	Cairo, Egypt
Site of infection	Intestine	Intestine	Caecum	Caecum	Caecum	Intestine	Intestine	Caecum and upper colon	Intestine	Intestine	Caecum	Caecum	Caecum and upper colon
Body length	5.5–6.8 (6.2)	3.534–5.394	1.95	1.2	5.46–8.97 (7.41)	3.60–4.61 (4.18)	3.1–3.6	3.53–4.51 (3.53–4.51)	3.024–3.528 (3.219 ± 0.150)	5.38–7.00 (6.46)	3.55–4.12 (3.83 ± 0.403)	3.2–3.6 (3.5 ± 0.1)	2.9–3.4 (3.1 ± 0.1)
Body width	0.197–0.232 (0.210)	0.153–0.234	0.15	0.08	0.225–0.391 (0.330)	0.20–0.30 (0.27)	0.175–0.245	0.230–0.270 (0.260 ± 0.01)	0.099–0.153 (0.120 ± 0.016)	0.282–0.447 (0.352)	0.199–0.288 (0.244 ± 0.062)	0.21–0.26 (0.24 ± 0.01)	0.19–0.23 (0.20 ± 0.01)
Esophageal length	0.290–0.348 (0.317)	0.252–0.336	0.49	0.43	0.305–0.465 (0.387)	0.25–0.29 (0.27)	0.331–0.433	0.400–0.450 (0.425 ± 0.01)	0.312–0.351 (0.322 ± 0.012)	0.417–0.480 (0.461)	0.328–0.382 (0.35 ± 0.038)	0.33–0.39 (0.27 ± 0.01)	0.30–0.34 (0.32 ± 0.01)
Esophageal width	0.042–0.052 (0.044)	0.048–0.057	–	–	0.045–0.080 (0.061)	–	–	–	–	–	–	0.17–0.19 (0.18 ± 0.01)	0.14–0.16 (0.15 ± 0.01)
Esophageal bulb length	0.145–0.171 (0.158)	0.129–0.159	0.14	0.16	0.150–0.225 (0.177)	0.12–0.15 (0.13)	–	0.140–0.160 (0.152 ± 0.006)	0.090–0.111 (0.103 ± 0.005)	0.123–0.167 (0.152)	0.108 (0.108 ± 0)	0.12–0.15 (0.140 ± 0.01)	0.10–0.13 (0.11 ± 0.01)
Esophageal bulb width	0.068–0–0.087 (0.080)	0.087–0.111	0.095	0.13	0.080–0.150 (0.107)	0.08–0.12 (0.10)	–	–	0.054–0.087 (0.063 ± 0.008)	0.088–0.137 (0.118)	0.081 (0.081 ± 0)	0.07–0.11 (0.09 ± 0.01)	0.05–0.09 (0.07 ± 0.01)
Distance from anterior extremity Nerve ring	0.155–0.185 (0.168)	0.120–0.168	0.14	0.13	0.162–0.238 (0.202)	0.15	0.158–0.216	0.12–0.162 (0.140 ± 0.013)	0.081–0.0105 (0.093 ± 0.007)	0.121–0.157 (0.134)	0.144–0.147 (0.145 ± 0.002)	–	0.078–0.090 (0.085 ± 0.002)
Excretory pore	–	0.756–1.056	0.53	0.9	0.82–1.67 (1.10)	0.81–0.89 (0.86)	0.734–0.936	0.860–0.950 (0.888 ± 0.032)	0.555–0.675 (0.590 ± 0.038)	1.09–1.23 (1.17)	–	–	0.564–0.780 (0.680 ± 0.02)
Vulval opening	2.1–2.5 (2.3)	1.457–2.015	0.85	1.65	1.52–2.89 (2.49)	1.54–2.36 (1.76)	1.1–1.4	1.61 ± 0.038 (1.55–1.67)	1.204–1.428 (1.269 ± 0.066)	2.07–2.43 (2.27)	1.56–1.86 (1.71 ± 0.21)	–	1.112–1.630 (1.406 ± 0.03)
Tail length	0.232–0.690 (0.445)	0.444–0.660	0.435	0.55	0.088–0.110 (0.101)	0.36–0.40 (0.39)	0.360–0.486	0.347–0.537 (0.477 ± 0.06)	0.330–0.372 (0.358 ± 0.016)	0.92–1.14 (1.05)	0.382–0.405(0.393 ± 0.016)	0.34–0.48 (0.42 ± 0.01)	0.30–0.42 (0.39 ± 0.01)
Eggs length	0.097–0.106 (0.101)	0.084–0.090	0.09	0.095	0.093–0.110 (0.102)	0.075–0.090 (0.084)	0.72–0.90	0.084–0.092 (0.087 ± 0.005)	0.054–0.069 (0.061 ± 0.003)	0.092–0.096 (0.094)	0.115–0.129 (0.122 ± 0.008)	0.05–0.07 (0.06 ± 0.01)	0.04–0.06 (0.05 ± 0.01)
Eggs width	0.0390.047 (0.044)	0.036–0.039	0.04	0.045	0.038–0.055 (0.045)	0.038–0.051 (0.045)	0.036 –0.053	0.043–0.052 (0.046 ± 0.005)	0.018–0.030 (0.022 ± 0.003)	0.051–0.058 (0.054)	0.054–0.072 (0.06 ± 0.008)	0.03–0.05 (0.04 ± 0.01)	0.02–0.04 (0.03 ± 0.01)

Main morphological features and measurements of male Aspiculuris tetraptera compared with previous studies_

Related species	Aspiculuris ackerti	Aspiculuris artigasi	Aspiculuris versterae	Aspiculuris tetraptera	A. ackerti	A. tetraptera	A. tetraptera	A. tetraptera	Aspiculuris huascaensis	Aspiculuris tianjinensis	A. tetraptera	A. tetraptera	A. tetraptera
Parameters	Kruidenier and Mehra (1959)	Araujo (1965)	Hugot (1980)	Hugot (1980)	Miller and Schmidt (1982)	Kohn and Macedo (1984)	Pinto et al. (1994)	Landaeta-Aqueveque et al. (2007)	Falcón-Ordaz et al. (2010)	Liu et al. (2012)	Khalil et al. (2014)	Abdel-Gaber and Fol (2015)	(Present study)
Host species	Neotoma albigtda	M. musculus	Mastomys natalensis	Mastomys natalensis	Neotoma cinerea	Haemulon sciurus	M. musculus	M. musculus	M. musculus	Clethrionomys rufocanus	M. musculus	M. musculus	M. musculus
Host locality	Coconimo, Arizona	Sao Paulo, Brazil	Onderstepoort, South Africa	Maracay, Venezuela	Colorado, Idaho, USA	Rio de Janeiro, Brazil	Río de Janeiro, Brazil	Santiago, Chile	Hidalgo, Mexico	Tianjin, China	Cairo, Egypt	Cairo, Egypt	Cairo, Egypt
Site of infection	Intestine	Intestine	Caecum	Caecum	Caecum	Intestine	Intestine	Caecum and upper colon	Intestine	Intestine	Caecum	Caecum	Caecum and upper colon
Body length	4.41–4.87 (4.64)	2.945–3.472	1.59	2.7	3.01–6.35 (5.03)	2.90–3.60 (3.22)	2.4–3.1	2.65–3.95 (3.393 ± 0.427)	2.16–2.69 (2.48 ± 0.172)	3.69– 5.12 (4.69)	2.55–2.57 (2.56 ± 0.014)	2.73–3.87 (3.21 ± 0.1)	2.23–3.29 (2.79 ± 0.1)
Body width	0.162–0.174 (0.168)	0.156–0.180	0.10	0.11	0.137–0.293 (0.236)	0.15–0.20 (0.17)	0.17–0.21	0.17–0.25 (0.202 ± 0.2)	0.078–0.114 (0.096 ± 0.01)	0.204–0.388 (0.307)	0.088 (0.088 ± 0)	0.18–0.23 (0.20 ± 0.1)	0.16–0.20 (0.18 ± 0.1)
Esophageal length	0.264–0.271 (0.267)	0.213–0.243	0.310	0.38	0.260–0.480 (0.343)	0.18–0.27 (0.23)	0.288–0.360	0.320–0.390 (0.375 ± 0.02)	0.291–0.294 (0.272 ± 0.013)	0.343–0.397 (0.384)	0.439–0.450 (0.44 ± 0.007)	0.38–0.45 (0.41 ± 0.1)	0.32–0.40 (0.39 ± 0.1)
Esophageal width	0.039–0.040 (0.039)	0.036–0.054	–	–	0.033–0.060 (0.051)	–	–	–	–	–	–	0.06–0.11 (0.08 ± 0.01)	0.05–0.09 (0.07 ± 0.01)
Esophageal bulb length	0.145–0.155 (0.150)	0.105–0.135	0.10	0.14	0.113–0.183 (0.157)	0.10-0.12 (0.11)	–	0.110–0.140 (0.133 ± 0.01)	0.090–0.110 (0.097 ± 0.006)	0.074–0.142 (0.122)	0.244 (0.24 ± 0)	0.14–0.19 (0.16 ± 0.1)	0.13–0.17 (0.15 ± 0.1)
Esophageal bulb width	0.071–0.079 (0.075)	0.075–0.096	0.08	0.09	0.065–0.120 (0.090)	0.06–0.08 (0.07)	–	–	0.040–0.063 (0.051 ± 0.006)	0.059–0.123 (0.098)	0.077–0.088 (0.08 ± 0.007)	0.07–0.09 (0.08 ± 0.01)	0.04–0.07 (0.05 ± 0.01)
Distance from anterior extremity Nerve ring	0.158	0.108–0.144	0.09	0.10	0.150–0.213 (0.186)	0.11–0.13 (0.12)	0.115–0.140	0.115–0.145 (0.129 ± 0.013)	0.072–0.093 (0.080 ± 0.008)	0.116–0.133 (0.123)	0.088 (0.088 ± 0)	–	0.065–0.082 (0.078 ± 0.001)
Excretory pore	–	0.600–0.876	0.325	0.78	0.69–1.21 (0.96)	0.69–0.78 (0.73)	0.619	0.750 –0.910 (0.854 ± 0.056)	0.495–0.579 (0.545 ± 0.035)	0.93–1.03 (1.01)	0.144–0.147 (0.145 ± 0.002)	–	0.392–0.547 (0.491 ± 0.03)
No. of Caudal papillae	11	5	5	5	10	12	12	12	12	12	12	12	12
Tail length	0.238–0.280 (0.259)	0.147–0.183	0.12	0.17	0.049–0.117 (0.092)	0.10-0.12 (0.11)	0.144–0.172	0.162–0.187 (0.178 ± 0.009)	0.075–0.114 (0.102 ± 0.013)	0.181–0.245 (0.220)	0.12–0.144 (0.132 ± 0.01)	0.13–0.15 (0.14 ± 0.1)	0.11–0.14 (0.12 ± 0.1)

Morphological Re-Description and 18 S rDNA Sequence Confirmation of the Pinworm Aspiculuris tetraptera (Nematoda, Heteroxynematidae) Infecting the Laboratory Mice Mus musculus

Figures & Tables

Fig. 1

Fig. 2

Nematoda species used in the phylogenetic analysis of Aspiculuris tetraptera in the present study_

Main morphological features and measurements of female Aspiculuris tetraptera compared with previous studies_

Main morphological features and measurements of male Aspiculuris tetraptera compared with previous studies_

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