Skip to main content
SpringerLink
Log in

Genetic diversity of Syphacia Seurat, 1916 (Nematoda: Oxyuridae) across the hybrid zone of their rodent hosts in Russia

  • Genetics, Evolution, and Phylogeny - Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The genetic diversity of Syphacia nematodes (intestinal parasites of rodents) was studied in the hybrid zone of two sister species of common voles, Microtus arvalis and Microtus obscurus, in the Oka River valley, east of Moscow. Syphacia nematodes of other rodent species (Microtus rossiaemeridionalis, Alexandromys oeconomus, Sylvaemus uralensis, and Apodemus agrarius) that inhabit the area were also studied. Phylogenetic trees for the studied nematodes were inferred from the analysis of nuclear ITS1+5.8S+ITS2, LSU rDNA, and mitochondrial CO1 gene partial sequences. Syphacia nematodes of the studied area form three well-defined clades in the phylogenetic tree of this genus. Morphological analysis revealed similarities between the obtained sequences with those of known Syphacia species from the GenBank database, which enabled identifying these three clades up to the species level: S. montana, S. agraria, and S. frederici. Russian haplotypes of Syphacia are different from West European and East Asian haplotypes with pronounced genetic distances. A high level of specificity was reported for two of these three species (S. frederici, only in Sylvaemus uralensis; S. agraria, only in Apodemus agrarius). S. montana was found in different species of voles. Remarkably, S. montana specimens from M. arvalis and M. obscurus were genetically uniform, while S. montana, specimens from hybrids between these two species formed a separate clade distant from those originating from non-hybridised hosts.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402. https://doi.org/10.1093/nar/25.17.3389

    Article  CAS  PubMed  Google Scholar 

  • Baird SJE, Ribas A, Macholán M, Albrecht T, Piálek J, Goüy de Bellocq J (2012) Where are the wormy mice? A reexamination of hybrid parasitism in the European house mouse hybrid zone. Evolution: International Journal of Organic Evolution 66:2757–2772. https://doi.org/10.1111/j.1558-5646.2012.01633.x

    Article  Google Scholar 

  • Brant SV, Orti G (2003) Evidence for gene flow in parasitic nematodes between two host species of shrews. Mol Ecol 12:2853–2859. https://doi.org/10.1046/j.1365-294x.2003.01927.x

    Article  CAS  PubMed  Google Scholar 

  • Bulatova NS, Golenishchev FN, Koval’skaya YM, Emelyanova LG, Bystrakova NV, Pavlova SV, Nadzhafova RS, Lavrenchenko LA (2010a) Cytogenetic study of the parapatric contact zone between two 46-chromosomal forms of the common vole in European Russia. Russian Journal of Genetics 46:443–448. https://doi.org/10.1134/S1022795410040095

    Article  CAS  Google Scholar 

  • Bulatova NS, Potapov SG, Lavrenchenko LA (2010b) Genomic versus chromosomal polytypy in studies of mitochondrial and nuclear DNA markers in the Microtus arvalis group. Russian Journal of Genetics 46:586–594. https://doi.org/10.1134/S1022795410050121

    Article  CAS  Google Scholar 

  • Chenna R, Sugawara H, Koike T, Lope R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucl Acids Res 31:3497–3500. https://doi.org/10.1093/nar/gkg500

    Article  CAS  PubMed  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nature methods. 9:772. https://doi.org/10.1038/nmeth.2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dewi K (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

  • 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 36:43–50. https://doi.org/10.1038/laban1007-43

    Article  Google Scholar 

  • Ford C, Hamerton JL (1956) A colchicine hypotonic citrate, squash sequence for mammalian chromosomes. Stain Tech 31:247–251. https://doi.org/10.3109/10520295609113814

    Article  CAS  Google Scholar 

  • Golden AM, Noffsinger EM, Baldwin JG, Fortuner R, Geraert E, Luc M, Robbins RT (1989) Suggested format for taxonomic papers published in the Journal of Nematology. J Nematology 21:444–445

    CAS  Google Scholar 

  • Goüy de Bellocq J, Ribas A, Baird SJE (2012) New insights into parasitism in the house mouse hybrid zone. In: Macholán M, Baird SJE, Munclinger P, Pialek J (eds) Evolution of the house mouse. Cambridge University Press, Cambridge, pp 455–481

    Chapter  Google Scholar 

  • Goüy de Bellocq J, Wasimuddin RA, Bryja J, Piálek J, Baird SJE (2018) Holobiont suture zones: parasite evidence across the European house mouse hybrid zone. Mol Ecol 27:5214–5227. https://doi.org/10.1111/mec.14938

    Article  PubMed  Google Scholar 

  • Griffin C, Joyce SA, Dix I, Burnell A, Downes M (1994) Characterisation of the entomopathogenic nematode Heterorhabditis (Nematoda: Heterorhabditidae) from Ireland and Britain by molecular and cross-breeding techniques, and the occurrence of the genus in these islands. Fundam and Appl Nematology 17:245–253

    Google Scholar 

  • Hugot J (1991) Les Syphaciinae (Oxyuridae, Nematoda) parasites de rongeurs et de lagomorphes: un exemple de co-évolution hôte-parasite. Bulletin de la Société zoologique de France 116:57–62

    Google Scholar 

  • Kang S, Sultana T, Eom KS, Park YC, Soonthornpong N, Nadler SA, Park JK (2009) The mitochondrial genome sequence of Enterobius vermicularis (Nematoda: Oxyurida)—an idiosyncratic gene order and phylogenetic information for chromadorean nematodes. Gene 429:87–97

    Article  CAS  Google Scholar 

  • Lavrenchenko LA, Potapov SG, Bulatova NS, Golenishchev FN (2009) A genetic study of natural hybridization between two forms of the common vole (Microtus arvalis) with the use of molecular and cytogenetic methods. Dokl Biol Sci 426:222–224. https://doi.org/10.1134/s0012496609030090

    Article  CAS  PubMed  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Proceedings 2010 gateway computing environments workshop (GCE) http://www.phylo.org/sub_sections/portal/cite.php. Accessed 3 Feb 2020

  • Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology. Trends in Ecol & Evol 22:156–165. https://doi.org/10.1016/j.tree.2006.11.012

    Article  Google Scholar 

  • Ogden CG (1971) Observations on the systematics of nematodes belonging to the genus Syphacia Seurat, 1916. Bulletin of the British Museum, Natural History. Zoology. 20:253–280

    Google Scholar 

  • Okamoto M, Urushima H, Iwasa M, Hasegawa H (2007) Phylogenetic relationships of rodent pinworms (genus Syphacia) in Japan inferred from mitochondrial CO1 gene sequences. J Vet Med Sci 69:545–547. https://doi.org/10.1292/jvms.69.545

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Parel JDC, Galula JU, Ooi HK (2008) Characterization of rDNA sequences from Syphacia obvelata, Syphacia muris, and Aspiculuris tetraptera and development of a PCR-based method for identification. Vet Parasitol 153:379–383. https://doi.org/10.1016/j.vetpar.2008.02.001

    Article  CAS  PubMed  Google Scholar 

  • Ryzhikov KM (ed) (1979) Key to the helminth species of rodents of USSR fauna: nematodes and acanthocephals. Nauka, Moscow [In Russian]

    Google Scholar 

  • Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin. Nematologica 4:67–69

    Article  Google Scholar 

  • Shchipanov NA (1987) A universal live trap for small mammals. Zoologicheskii Zhurnal 66:759–761

    Google Scholar 

  • Stewart A, Lowe A, Smales L, Bajer A, Bradley J, Dwużnik D, Franssen F, Griffith J, Stuart P, Turner C, Zaleśny G, Behnke JM (2017) Parasitic nematodes of the genus Syphacia Seurat, 1916 infecting Muridae in the British Isles, and the peculiar case of Syphacia frederici. Parasitology 145:269–280. https://doi.org/10.1017/S0031182017001470

    Article  PubMed  Google Scholar 

  • Velikov VA (2013) Molecular biology. A practical guide. Saratovskiy istochnik, Saratov [In Russian]

    Google Scholar 

  • Vrain TC, Wakarchuk DA, Levesque AC, Hamilton RI (1992) Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology 15:563–573

    Google Scholar 

  • Wang C-R, Yan L, Yan Z, Wang W-T, Xu Z, Xu W-W, Ying Z, Si-Qin T, Lu N, Qiao-Cheng C (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. https://doi.org/10.3109/19401736.2014.905861

    Article  CAS  PubMed  Google Scholar 

  • Wasimuddin BJ, Ribas A, Baird SJ, Piálek J, Goüy de Bellocq J (2016) Testing parasite ‘intimacy’: the whipworm Trichuris muris in the European house mouse hybrid zone. Ecol Evol 6:2688–2701. https://doi.org/10.1002/ece3.2022

    Article  CAS  PubMed  Google Scholar 

  • Wiger R, Barus V, Tenora F (1978) Scanning electron microscopic studies on four species of the genus Syphacia (Nematoda, Oxyuridae). Zool Scr 7:25–31. https://doi.org/10.1111/j.1463-6409.1978.tb00586.x

    Article  Google Scholar 

  • Zelck UE, Bialek R, Weiß M (2011) Molecular phylogenetic analysis of Enterobius vermicularis and development of an 18S ribosomal DNA-targeted diagnostic PCR. J Clin Microbiol 49:1602–1604

    Article  CAS  Google Scholar 

Download references

The field work of parasite collection was supported by the Russian Foundation for Basic Research (project no. 18-04-00563-a). We thankfully acknowledge the practical and logistic help of our colleagues Vlasenko P.G., D.S. Kostin, T.A. Mironova, A.A. Martynov, V.A. Komarova, and N.A. Illarionova. The molecular analysis in this study (i.e. the amplification, sequencing, and analysis) were supported by RSF grant no. 19-74-20147.

Availability of data and material

The datasets generated during the current study are available from the corresponding author on reasonable request.

Code availability

Freeware for the processing of sequence data and phylogenetic analysis were used. Bayesian analysis was performed on the CIPRES Science Gateway (platform for free phylogenetic analysis). Vector graphic and halftone figures were prepared with the use of CorelDraw Home and Student 2019 purchased by one of the authors (S.E.S., serial number DH21R22-Y6FLFY3-CWF7VEL-HYTM78E).

Author information

Authors and Affiliations

  1. Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii prospect, 33, Moscow, Russian Federation, 119071

    Daria I. Gorelysheva & Sergei E. Spiridonov

  2. Laboratory of Mammalian Microevolution, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii prospect, 33, Moscow, Russian Federation, 119071

    Anton R. Gromov & Leonid A. Lavrenchenko

Authors
  1. Daria I. Gorelysheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anton R. Gromov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Leonid A. Lavrenchenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergei E. Spiridonov
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the study concept and design, material collection and processing, and manuscript preparation and fully agreed in the content of submission.

Corresponding author

Correspondence to Daria I. Gorelysheva.

Ethics declarations

Ethical approval

All procedures in the present study were approved by the Animal Care and Use Committee of the A.N. Severtsov Institute of Ecology and Evolution of the Russian Academy of Sciences and complied with the Federal Law of the Russian Federation no. 498-FZ from 19 December 2018 (on responsible treatment of animals).

The collection of rodent material was possible through the general permit issued by the government for the scientific institutions of the Russian Academy of Sciences (including A.N. Severtsov Institute of Ecology and Evolution) to study not endangered species of animals throughout the territory of the Russian Federation.

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Hiroshi Sato

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gorelysheva, D.I., Gromov, A.R., Lavrenchenko, L.A. et al. Genetic diversity of Syphacia Seurat, 1916 (Nematoda: Oxyuridae) across the hybrid zone of their rodent hosts in Russia. Parasitol Res 120, 2017–2030 (2021). https://doi.org/10.1007/s00436-021-07134-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-021-07134-7

Keywords

Search

Navigation