Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Molecular characterization of cosmopolitan and potentially co-invasive helminths of commensal, murid rodents in Gauteng Province, South Africa


Concurrent studies of helminth parasites of introduced and native rodent species are few and miss the opportunity to identify potential co-invasive parasite species. This study employed molecular tools to infer the phylogeny and elucidate the origin of potentially co-invasive parasites of commensal, murid rodents by assessing introduced Rattus norvegicus, Rattus rattus, Rattus tanezumi, and native Mastomys coucha in Gauteng Province, South Africa. Genotypes of Nippostrongylus brasiliensis recovered from R. norvegicus are nearly identical to those recovered from elsewhere in the world. The pinworms, Aspiculurus tetraptera, recovered from introduced R. tanezumi and R. rattus, Syphacia muris recovered from R. tanezumi, and Syphacia obvelata recovered from indigenous M. coucha have affiliations to those recovered of laboratory rodents from the USA and China. Syphacia obvelata was previously only known as a commensal endoparasite of laboratory rodents, and the S. muris genotype recovered from R. tanezumi in this study shows an affiliation to a genotype recovered from the same host species in Indonesia which is part of the native range. The study emphasizes the need for surveillance of potential co-invasive species and contributes in documenting genetic diversity of endoparasites of well-known hosts.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2


  1. Abu-Madi MA, Behnke JM, Mikhail M et al (2005) Parasite populations in the brown rat Rattus norvegicus from Doha, Qatar between years: the effect of host age, sex and density. J Helminthol 79:105–111.

  2. Anderson RC, Willmott S, Chabaud AG (1974) CIH keys to the nematode parasites of vertebrates. Commonwealth Agricultural Bureaux (CAB) Press, Wallingford

  3. Bastos AD, Nair D, Taylor PJ et al (2011) Genetic monitoring detects an overlooked cryptic species and reveals the diversity and distribution of three invasive Rattus congeners in South Africa. BMC Genet 12:26.

  4. Blaxter ML, Dorris M, Frisse LM et al (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75

  5. Callejón R, Nadler S, De Rojas M et al (2013) Molecular characterization and phylogeny of whipworm nematodes inferred from DNA sequences of cox1 mtDNA and 18S rDNA. Parasitol Res 112:3933–3949.

  6. Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552

  7. Chaisiri K, Chaeychomsri W, Siruntawineti J (2010) Gastrointestinal helminth infections in Asian house rats (Rattus tanezumi) from northern and northeastern Thailand. J Trop Med Parasitol 33:29–35

  8. Chilton NB, Huby-Chilton F, Gasser RB, Beveridge I (2006) The evolutionary origins of nematodes within the order Strongylida are related to predilection sites within hosts. Mol Phylogenet Evol 40:118–128.

  9. Dewi K, Hasegawa H (2015) Taxonomical and faunistic studies on the nematode parasites from Indonesian murines (Rodentia; Muridae; Murinae) with special reference to Syphacia spp. and their biogeography. Thesis, Rakuno Gakuen University, Japan

  10. Diagne C, Ribas A, Charbonnel N, Dalecky A, Tatard C, Gauthier P, Haukisalmi V, Fossati-Gaschignard O, Bâ K, Kane M, Niang Y, Diallo M, Sow A, Piry S, Sembène M, Brouat C (2016) Parasites and invasions: changes in gastrointestinal helminth assemblages in invasive and native rodents in Senegal. Int J Parasitol 46:857–869.

  11. Feldman SH, Bowman SG (2007) Molecular phylogeny of the pinworms of mice, rats and rabbits, and its use to develop molecular beacon assays for the detection of pinworms in mice. Lab Anim (NY) 36:22908

  12. Foronda P, López-González M, Hernández M, Haukisalmi V, Feliu C (2011) Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasit Vectors 4:185.

  13. Gesy KM, Schurer JM, Massolo A et al (2014) Unexpected diversity of the cestode Echinococcus multilocularis in wildlife in Canada. Int J Parasitol Parasites Wildl 3:81–87.

  14. Holterman M, Van Der WA, Van Den ES et al (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Mol Biol Evol 23:1792–1800.

  15. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

  16. Hussey KL (1957) Syphacia muris vs. S. obvelata in laboratory rats and mice. J Parasitol 43:555–559

  17. Julius R (2013) Molecular prevalence and diversity of zoonotic bacteria of invasive Rattus from South Africa, with emphasis on the genera Rickettsia and Streptobacillus. MSc Dissertation, University of Pretoria, Pretoria

  18. Julius RS, Schwan EV, Chimimba CT (2017) Helminth composition and prevalence of indigenous and invasive synanthropic murid rodents in urban areas of Gauteng Province, South Africa. J Helminthol 1–10.

  19. Khalil L, Jones A, Bray RA (1994) Keys to the cestode parasites of vertebrates. CAB International, Wallingford

  20. Kosoy M, Khlyap L, Cosson J-F, Morand S (2015) Aboriginal and invasive rats of genus Rattus as hosts of infectious agents. Vector-Borne Zoonotic Dis 15:3–12.

  21. Le Grange A (2014) Molecular prevalence and diversity of Anaplasmataceae and Bartonellaceae in indigenous Muridae from South Africa. MSc Dissertation, University of Pretoria, Pretoria

  22. Li X, Chen X, Fan W et al (2009) PCR amplification and sequence analysis of mitochondrial cytochrome C oxidase subunit 1 (cox1) of Syphacia obvelata from mice. China Anim Husb Vet Med 36:57–59

  23. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452.

  24. Lou Y, Zhang Y, Qiu J et al (2015) Sequence variability in four mitochondrial genes among pinworm Aspicularis tetraptera isolates from laboratory mice in four provinces, China. Mitochondrial DNA 26:431–434.

  25. Lymbery AJ, Morine M, Kanani HG et al (2014) Co-invaders: the effects of alien parasites on native hosts. Int J Parasitol Parasites Wildl 3:171–177.

  26. Macnish MG, Morgan-Ryan UM, Monis PT et al (2002) A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125:567–575.

  27. Morand S, Krasnov B, Poulin R (2006) Micromammals and macroparasites: from evolutionary ecology to management. Springer, Tokyo

  28. Morand S, Bordes F, Chen H, Claude J (2015) Global parasite and Rattus rodent invasions: the consequences for rodent-borne diseases. Integr Zool 10:409–423.

  29. Nkouawa A, Haukisalmi V, Li T, Nakao M, Lavikainen A, Chen X, Henttonen H, Ito A (2016) Cryptic diversity in hymenolepidid tapeworms infecting humans. Parasitol Int 65:83–86.

  30. Okamoto M, Urushima H, Hasegawa H (2009) Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from 28S rDNA sequences. Parasitol Int 58:330–333.

  31. Panti-May JA, Hernández-Betancourt SF, Rodríguez-Vivas RI, Robles MR (2013) Infection levels of intestinal helminths in two commensal rodent species from rural households in Yucatan, Mexico. J Helminthol 89:42–48.

  32. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256.

  33. Puza V, Chundelova D, Nermut J, Zurovcova M, Mracek Z (2015) Intra-individual variability of ITS regions in entomopathogenic nematodes (Steinernematidae:Nematoda) :implications for their taxonomy. BioControl 60:547–554.

  34. Ribas A, López S, Makundi RH et al (2013) Trichuris spp. (Nematoda: Trichuridae) from two rodents, Mastomys natalensis and Gerbilliscus vicinus in Tanzania. J Parasitol 99:868–875.

  35. Rojas MDC, Digiani MC (2003) First record of Mastophorus muris (Gmelin, 1790 ) (Nematoda: Spiruroidea) from a wild host in South America. Parasite 10:1–4.

  36. Shimalov VV (2016) Helminth infections of the brown rat (Rattus norvegicus Berkenhout, 1769) in the biocenoses of south-West Belarus. J Parasit Dis 41:9–11.

  37. Smith KF, Carpenter SM (2006) Potential spread of introduced black rat (Rattus rattus) parasites to endemic deer mice (Peromyscus maniculatus) on the California Channel islands. Divers Distrib 12:742–748.

  38. Swofford DL (2002) PAUP* phylogenetic analysis using parsimony (*and other methods), version 4. Sinauer Associates, Sunderland

  39. Tamura K, Peterson D, Peterson N et al (2011) MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739.

  40. Torchin ME, Lafferty KD, Dobson AP et al (2003) Introduced species and their missing parasites. Nature 421:628–630.

  41. Von Nickisch-Rosenegk M, Brown WM, Boore JL (2001) Complete sequence of the mitochondrial genome of the tapeworm Hymenolepis diminuta: gene arrangements indicate that platyhelminths are eutrochozoans. Mol Biol Evol 18:721–730

  42. Wang C, Lou Y, Zhang Y et al (2015) Genetic variability among Syphacia obvelata isolates from laboratory mice in four different geographical locations of China revealed by sequence analyses of five mitochondrial genes. Mitochondrial DNA 26:213–216.

  43. Wang C, Lou Y, Gao J et al (2016) Comparative analyses of the complete mitochondrial genomes of the two murine pinworms Aspiculuris tetraptera and Syphacia obvelata. Gene 585:71–75.

  44. Wasimuddin BJ, Ribas A et al (2016) Testing parasite “intimacy”: the whipworm Trichuris muris in the European house mouse hybrid zone. Ecol Evol 6:2688–2701.

  45. Weaver HJ, Monks S, Gardner SL (2016) Phylogeny and biogeography of species of Syphacia Seurat, 1916 (Nemata:Oxyurida:Oxyuridae) from the Australian bioregion. Aust J Zool 64:1–10.

  46. Whiting MF, Carpenter JC, Wheeler QD, Ard VC (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Syst Biol 46:1–68

Download references


The authors are grateful to the volunteers who assisted in the sample collection, Prof C Sole for the guidance on the molecular work, and Ms. A Le Grange for commenting on the manuscript. We also thank the DST/NRF-Centre of Excellence for Invasion Biology (CIB) for the financial support and the National Research Foundation (NRF) supported DNA sequencing facility of the University of Pretoria (NRF RISP grant 2001/2012; UID 78566).

Author information

Correspondence to R. S. Julius.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Julius, R.S., Schwan, E.V. & Chimimba, C.T. Molecular characterization of cosmopolitan and potentially co-invasive helminths of commensal, murid rodents in Gauteng Province, South Africa. Parasitol Res 117, 1729–1736 (2018).

Download citation


  • Phylogeography
  • Mastomys coucha
  • Rattus
  • Co-invasive
  • Parasites