Skip to main content
SpringerLink
Log in

Varestrongylus (Nematoda: Protostrongylidae), lungworms of ungulates: a phylogenetic framework based on comparative morphology

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Varestrongylus Bhalerao, 1932 comprises ten valid lungworm species infecting wild and domestic ungulates from Eurasia and North America. Here, we present a phylogenetic hypothesis for the genus based on morphological characters in a broader context for the family Protostrongylidae and discuss species relationships and aspects of character evolution. Phylogenetic analysis of 25 structural attributes, including binary and multistate characters, among the 10 species of Varestrongylus resulted in one fully resolved most parsimonious tree (61 steps; consistency index = 0.672, retention index = 0.722, and consistency index excluding uninformative characters = 0.667). Varestrongylus forms a monophyletic clade and is the sister of Pneumostrongylus, supporting recognition of the subfamily Varestrongylinae. Monophyly for Varestrongylus is diagnosed by six unequivocal synapomorphies, all associated with structural characters of the copulatory system of males. Varestrongylus pneumonicus is basal, and sister to all other species within the genus, which form two subclades. The subclade I contains V. sagittatus + V. tuvae and V. qinghaiensis + V. longispiculatus. Subclade II contains V. alpenae, V. capricola, V. capreoli, and V. eleguneniensis + V. alces. Both subclades are diagnosed by two unambiguous synapomorphies. Highlighted is the continuing importance of phylogenetic assessments based on comparative morphology as a foundation to explore the structure of the biosphere across space and time.

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

Similar content being viewed by others

References

  • Anderson RC (2000) Nematode parasites of vertebrates. Their development and transmission. CAB Publishing, Oxford

    Book  Google Scholar 

  • Bhalerao GD (1932) On some nematodes of goat and sheep of Mutkesar. Indian J Vet Sci 2:242–254

    Google Scholar 

  • Bhatia BB, Pande BP (1960) Studies on lungworms (Metastrongylidae Leiper, 1908) parasitising Indian livestock II. Observations of natural infestations with species of Dictyocaulus Railliet and Henry, 1907 and Varestrongylus Bhalerao, 1932 in the sheep of hills of Uttar Pradesh. Proc Natl Acad Sci India Sec B 30(3):217–233

    Google Scholar 

  • Boev SN (1968) Revision of the subfamily Capreocaulinae. Izdatelstvo Akad Nauk SSSR, Moscow, pp 101–108

    Google Scholar 

  • Boev SN (1975) Fundamentals of nematology, Vol. 25. Protostrongylids [English translation by the U.S. Department of Agriculture, Washington, D.C., and Amerind Publishing Co., New Delhi]. Helminthological Laboratory, Academy of Sciences of the USSR, Moscow

  • Bremer K (1994) Branch support and tree stability. Cladistics 29:173–181

    Google Scholar 

  • Brooks DR, Hoberg EP, Boeger WA, Gardner SL, Galbreath KE, Herczeg D, Mejía-Madrid HH, Rácz SE, Dursahinhan AT (2014) Finding them before they find us: informatics, parasites, and environments in accelerating climate change. Comp Parasitol 81(2):155–164

    Article  Google Scholar 

  • Carreno RA, Hoberg EP (1999) Evolutionary relationships among the Protostrongylidae (Nematoda: Metastrongyloidea) as inferred from morphological characters, with consideration of parasite-host coevolution. J Parasitol 85(4):638–648

    Article  PubMed  CAS  Google Scholar 

  • Carreno RA, Lankester MW (1994) A reevaluation of the phylogeny of Parelaphostrongylus Boev and Schulz, 1950 (Nematoda, Protostrongylidae). Syst Parasitol 28(2):145–151

    Article  Google Scholar 

  • Carreno RA, Nadler SA (2003) Phylogenetic analysis of the Metastrongyloidea (Nematoda: Strongylida) inferred from ribosomal RNA gene sequences. J Parasitol 89(5):965–973

    Article  PubMed  CAS  Google Scholar 

  • Carreno RA et al. (2012) Discovery of an undescribed protostrongylid nematode from the endangered Pampas deer (Ozotoceros bezoarticus celer) in Argentina. J Wildl Dis 48(3):724–731

    Article  PubMed  Google Scholar 

  • Cook JA et al (2017) The Beringian coevolution project: holistic collections of mammals and associated parasites reveal novel perspectives on changing environments in the north. Arctic. Science 3:585–617

    Google Scholar 

  • Demidova NV, Naumitscheva MI (1953) A new nematode Varestrongylus alces sp. nov. in moose. Moskovskij Pushno-Mekhovoj Institut Trudy 4:303–306

    Google Scholar 

  • Dougherty EC (1949) The phylogeny of the nematode family Metastrongylidae Leiper (1909): a correlation of host and symbiote evolution. Parasitology 39:222–234

    Article  PubMed  CAS  Google Scholar 

  • Dougherty EC, Goble FC (1946) The genus Protostrongylus Kamenskii, 1905 (Nematoda: Metastrongylidae), and its relatives: preliminary note. J Parasitol 32:7–16

    Article  PubMed  CAS  Google Scholar 

  • Grubb P (2005) Order Artiodactyla. In: Wilson DE, Reeder DM (eds) Manual species of the world: a taxonomic and geographic reference. The Johns Hopkins University Press, Baltimore, pp 652–722

    Google Scholar 

  • Hoberg EP (2002) Foundations for an integrative parasitology: collections, archives, and biodiversity informatics. Comp Parasitol 69(2):24–131

    Article  Google Scholar 

  • Hoberg EP, Lichtenfels JR, Gibbons LM (2004) Phylogeny for species of Haemonchus (Nematoda: Trichostrongyloidea): considerations of their evolutionary history and global biogeography among Camelidae and Pecora (Artiodactyla). J Parasitol 90(5):1085–1102

    Article  PubMed  Google Scholar 

  • Hoberg EP, Lichtenfels JR, Rickard LG (2005) Phylogeny for genera of Nematodirinae (Nematoda: Trichostrongylina). J Parasitol 91(2):382–389

    Article  PubMed  Google Scholar 

  • Hoberg EP, Pilitt PA, Galbreath KE (2009) Why museums matter: a tale of pinworms (Oxyuroidea: Heteroxynematidae) among pikas (Ochotona princeps and O. collaris) in the American west. J Parasitol 95:490–501

    Article  PubMed  CAS  Google Scholar 

  • Hoberg EP, Agosta SJ, Boeger WA, Brooks DR (2015) An integrated parasitology: revealing the elephant through tradition and invention. Trends Parasitol 31(4):128–133

    Article  PubMed  Google Scholar 

  • Kutz SJ, Asmundsson I, Hoberg EP, Appleyard GD, Jenkins EJ, Beckmen K, Branigan M, Butler L, Chilton NB, Cooley D, Elkin B, Huby-Chilton F, Johnson D, Kuchboev A, Nagy J, Oakley M, Polley L, Popko R, Scheer A, Simard M, Veitch A (2007) Serendipitous discovery of a novel protostrongylid (Nematoda: Metastrongyloidea) in caribou, muskoxen, and moose from high latitudes of North America based on DNA sequence comparisons. Can J Zool 85(11):1143–1156. https://doi.org/10.1139/z07-091

    Article  CAS  Google Scholar 

  • Liu W-D (1984) A new species of nematode in the family Protostrongylidae. Acta Zootaxon Sin 9(1):8–11

    Google Scholar 

  • Liu S-X (1989) A new species of Protostrongylid lungworm from takin. Acta Zootaxon Sin 14:269–272

    Google Scholar 

  • Mönnig HO (1932) New strongylid nematodes of antelopes (preliminary notes). J S Afr Vet Med Assoc 3:171–175

    Google Scholar 

  • Ortlepp (1962) Lungworms of south African antelopes. Onderstepoort J Vet Res 29:173–181

    Google Scholar 

  • Sarwar MM (1955) On a new lungworm, Pneumostrongylus ovis Sarwar, 1953, and some remarks on Varestrongylus species from sheep and goats in Pakistan. Parasitology 45(3–4):426–430

    Article  PubMed  CAS  Google Scholar 

  • Stroh G, Schmid F (1938) Protostrongylus capreoli nov. spec., der häufigste Lungenwurm des Rehes. Berliner Tierärztliche Wochenschrift 9:121–123

    Google Scholar 

  • Swofford DL (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), 4th edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Verocai GG (2015) Contributions to the biodiversity and biogeography of the genus Varestrongylus Bhalerao, 1932 (Nematoda: Protostrongylidae), lungworms of ungulates, with emphasis on a new Nearctic species. Thesis, University of Calgary

  • Verocai GG, Kutz SJ, Simard M, Hoberg EP (2014a) Resurrection and redescription of Varestrongylus alces (Nematoda; Protostrongylidae), a lungworm of the Eurasian moose (Alces alces), with report on associated pathology. Parasit Vectors 7:556

    Article  PubMed  PubMed Central  Google Scholar 

  • Verocai GG, Kutz SJ, Simard M, Hoberg EP (2014b) Varestrongylus eleguneniensis sp. n. (Nematoda: Protostrongylidae): a widespread, multi-host lungworm of wild north American ungulates, with an emended diagnosis for the genus and explorations of biogeography. Parasit Vectors 7:557

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watrous LE, Wheeler QD (1981) The out-group comparison method of character analysis. Syst Zool 30(1):1–11

    Article  Google Scholar 

Download references

Acknowledgements

This research is part of G. Verocai’s PhD Thesis and was supported by the Faculty of Veterinary Medicine of the University of Calgary, Alberta Innovates Health Solutions, Alberta Conservation Association–Grants in Biodiversity, and International Polar Year funding to the CircumArctic Rangifer Monitoring and Assessment Network (CARMA, http://www.carmanetwork.com) and NSERC Discovery Grant and NSERC Northern Supplement secured by S.J. Kutz; the Beringian Coevolution Project (DEB-Biotic Surveys and Inventory-0415668) with funding from the National Science Foundation to J. A. Cook (University of New Mexico) and E. P. Hoberg (USNPC). Our study was completed through the Integrated Inventory of Biomes of the Arctic (NSF, DEB-Biodiversity Discovery and Analysis–1258010) to J. A. Cook, E. P. Hoberg, K. E. Galbreath (Northern Michigan University) and E. Dechaine (Western Washington University).

The authors thank Manon Simard (Nunavik Research Centre, Makivik Corporation), colleagues of the Norwegian Veterinary Institute, Dr. Margo Pybus and Bob McClymont (Alberta Fish and Wildlife Division), and Patricia Pilitt and Art Abrams (USNPC, USDA).

Author information

Authors and Affiliations

  1. Department of Infectious Diseases, College of Veterinary Medicine, University of Georgia, 510 D.W. Brooks Drive, Athens, GA, 30602, USA

    Guilherme G. Verocai

  2. Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, AB, T2N 4N1, Canada

    Guilherme G. Verocai & Susan J. Kutz

  3. Museum of Southwestern Biology, Department of Biology, University of New Mexico, Albuquerque, NM, 87108, USA

    Eric P. Hoberg

Authors
  1. Guilherme G. Verocai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susan J. Kutz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eric P. Hoberg
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guilherme G. Verocai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Verocai, G.G., Kutz, S.J. & Hoberg, E.P. Varestrongylus (Nematoda: Protostrongylidae), lungworms of ungulates: a phylogenetic framework based on comparative morphology. Parasitol Res 117, 2075–2083 (2018). https://doi.org/10.1007/s00436-018-5893-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-018-5893-8

Keywords

Search

Navigation