Resurrection and redescription of Varestrongylus alces (Nematoda; Protostrongylidae), a lungworm of Eurasian elk (Alces alces), with a report on associated pathology

Authors: VEROCAI, GUILLHERME - University Of Calgary; Hoberg, Eric; VIKOREN, TURID - Norwegian Veterinary Institute; HANDELAND, KJELL - Norwegian Veterinary Institute; YTREHUS, BJORNAR - Norwegian Veterinary Institute; REZANSOFF, ANDREW - University Of Calgary; DAVIDSON, REBECCA - Norwegian Veterinary Institute; GILLEARD, JOHN - University Of Calgary; KUTZ, SUSAN - University Of Calgary

Submitted to: Parasites & Vectors
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/23/2014
Publication Date: 12/17/2014
Publication URL: http://doi:10.1186/s13071-014-0557-8
Citation: Verocai, G.G., Hoberg, E.P., Vikoren, T., Handeland, K., Ytrehus, B., Rezansoff, A.M., Davidson, R.K., Gilleard, J.S., Kutz, S.J. 2014. Resurrection and redescription of Varestrongylus alces (Nematoda; Protostrongylidae), a lungworm of Eurasian elk (Alces alces), with a report on associated pathology. Parasites & Vectors. 7:557.

Interpretive Summary: Understanding of the diversity of ungulate lung-worm faunas continues to undergo a rapid expansion with discovery of previously unknown species and recognition of species-complexes which contain morphologically similar nematodes. Integration of comparative morphology and molecular-based assessments are becoming standard in developing new concepts for diversity in many parasite groups. New field collections of European elk in Norway in conjunction with detailed microscopy and analysis of ITS-2 DNA sequences of lungworm parasites served to reveal that Varestrongylus alces, a miniscule nematode in the lung parenchyma, is a valid species, distinct from others in the genus. This species had been considered as a synonym of another in the genus, an incorrect decision based on a poorly detailed morphological description and the absence of a type series held in a museum collection. Our studies unequivocally establish the independence of V. alces relative to other species in the genus and validate the utility of a suite of structural and molecular attributes in identification. Analysis of evolutionary relationships among species of this group demonstrated a close association with an as yet undescribed species that circulates broadly in North American ungulates at high latitudes and contribute to a broader evaluation of biogeography and history for this parasite assemblage in cervids (deer, caribou and moose). Relationships among Varestrongylus species from Eurasia and North America are complex, consistent with faunal assembly involving recurrent events of geographic expansion and host switching and subsequent speciation. Definition of faunal diversity and the diagnostic characters needed to identify and document the distribution of these nematodes is a critical contribution for use by wildlife biologists, disease ecologists, and parasitologists in the academic and government sectors.

Technical Abstract: Varestrongylus alces Demidova & Naumitscheva, 1953 is resurrected for protostrongylid nematodes of Eurasian elk in Europe. Descriptions of males (11.36-16.95 mm) and females (16.25- 21.52 mm) are based on specimens collected from the terminal bronchioles in the lungs of Eurasian elk, Alces alces (L., 1900), from the municipality of Vestby (59º 30' N, 10º 40' E), Eastern Norway. The species is valid and distinct from others referred to Varestrongylus Bhalerao, 1932, and should be separated from Varestrongylus capreoli (Stroh & Schmidt, 1938), with which it was synonymized due to a poorly detailed morphological description and the absence of a type series. Morphologically, V. alces can be distinguished from other species by characters in the males that include a distally bifurcate gubernaculum, arched denticulate crurae, spicules that are equal in length and relatively short, and a dorsal ray that is elongate and bifurcated. Females have a well-developed provagina, and are very similar to those of V. capreoli. Morphometrics of first-stage larvae largely overlap with those of other Varestrongylus.. Sequences of the ITS-2 region of the nuclear ribosomal DNA strongly support mutual independence of V. alces, V. cf. capreoli from European roe deer, and the yet undescribed Varestrongylus species in caribou, moose and muskoxen from North America. These three taxa form a well-supported crown-clade as the putative sister of V. alpenae. Perhaps, Varestrongylus alces has an ancient association with Alces or its ancestors, and evolved independently from, but in potential sympatry with, other cervid-Varestrongylus assemblages within Eurasia. Alternatively, it may represent speciation following an event of host switching to A. alces from other Odocoileinae cervids. We postulate that the range of V. alces mirrors that of European elk, and previous reports of V. capreoli in this host may, in fact be V. alces. Relationships among Varestrongylus species from Eurasia and North America are complex, consistent with faunal assembly involving recurrent events of geographic expansion and host switching and subsequent speciation. Adult nematodes cause visible lesions consistent with focal verminous pneumonia. Histologically, lesions are restricted to the parenchyma with adult, egg and larval parasites surrounded by multinucleated giant cells, macrophages, eosinophilic granulocytes and lymphocytes.