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Nematoda: Protostrongylidae), Lungworms of Ungulates, with Emphasis on a New Nearctic Species

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University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2015-05-01 Contributions to the Biodiversity and Biogeography of the Genus Varestrongylus Bhalerao, 1932 (Nematoda: Protostrongylidae), Lungworms of Ungulates, with Emphasis on a New Nearctic Species Gomes Verocai, Guilherme Gomes Verocai, G. (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Bhalerao, 1932 (Nematoda: Protostrongylidae), Lungworms of Ungulates, with Emphasis on a New Nearctic Species (Unpublished doctoral thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/25450 http://hdl.handle.net/11023/2222 doctoral thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Contributions to the Biodiversity and Biogeography of the Genus Varestrongylus Bhalerao, 1932 (Nematoda: Protostrongylidae), Lungworms of Ungulates, with Emphasis on a New Nearctic Species by Guilherme Gomes Verocai A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY GRADUATE PROGRAM IN VETERINARY MEDICAL SCIENCES CALGARY, ALBERTA APRIL, 2015 © Guilherme Gomes Verocai 2015 Abstract Explorations of parasite biodiversity and biogeography are essential for elucidating evolutionary and ecological patterns and processes that shaped the biosphere. Among relevant nematode parasites of ungulates are species within the family Protostrongylidae Leiper, 1926 (Strongylida: Metastrongyloidea), which often cause pulmonary, muscular or neurological diseases in their hosts. The finding of a novel protostrongylid species infecting North American ungulates in 2007 demonstrated that the knowledge of the biodiversity of this group remained incomplete, despite the substantial advances in recent decades. Through my thesis research I focused on developing and understanding the biodiversity, phylogenetic relationships, and biogeography of the genus Varestrongylus Bhalerao, 1932 (Nematoda: Protostrongylidae), lungworms of cervids and caprine bovids. To do this, I first explored the validity of existing species, and have resurrected and redescribed Varestrongylus alces Demidova & Naumitscheva, 1953 of the Eurasian moose from Europe. Secondly, I described Varestrongylus eleguneniensis Verocai, Kutz, Simard & Hoberg, 2014. This new species primarily infects caribou, but also muskoxen and, rarely moose across a vast range in North America. By exploring the relationships among Varestrongylus species, I have developed a phylogenetic hypothesis for the genus and for co-evolution and biogeography of this host-parasite assemblage. Varestrongylus has a complex history, characterized by multiple events of host-switching and geographic expansion. Moreover, through a geographically wide assessment of the distribution of V. eleguneniensis in caribou, muskoxen and moose populations across North America I have established baselines for future studies monitoring the geographic distribution of a lungworm species. This work also provides a foundation for understanding historical and current processes affecting the biogeography of host- ii parasite assemblages. The present work is an original contribution to the field by adding to the present knowledge on taxonomy and biodiversity of this relevant group of parasites, to the general understanding of the formation of host-parasite assemblages, and the colonization of North America by both parasites and hosts. Ultimately, by understanding the historical and contemporary processes that have lead to current biogeography of V. eleguneniensis, this work can be used for predicting future trends on the distribution, host-associations and biogeography of V. eleguneniensis under a scenario of rapid climate change. iii Preface The following manuscripts have been published in peer-reviewed journals. Guilherme G. Verocai collected and analysed the data, interpreted the results and wrote the papers with guidance from his supervisor, selected members of his supervisory committee and other collaborators. All co-authors contributed technically and intellectually to the content of the papers, and provided critical comments prior to publication. Written permission for reproduction of the scientific articles in its entirety for this thesis has been obtained from the publishers and all co-authors. Verocai, G.G., Hoberg, E. P., Vikøren, 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 the Eurasian moose (Alces alces), with report on associated pathology. Parasites & Vectors 7, 557 [Chapter Two] Verocai, G.G., Simard, M., Kutz, S. J., Hoberg, E. P., 2014, Varestrongylus eleguneniensis sp. n. (Nematoda; Protostrongylidae): a widespread, multi-host lungworm of North American ungulates, with an emended diagnosis for the genus and explorations on biogeography. Parasites & Vectors 7, 556 [Chapter Three] Verocai, G.G., Lejeune, M., Finstad, G. L., Kutz, S. J., 2013, A Nearctic parasite in a Palearctic host: Parelaphostrongylus andersoni (Nematoda; Protostrongylidae) infecting semi- domesticated reindeer in Alaska. International Journal for Parasitology: Parasites and Wildlife 2, 119-123 [Appendix IV] iv Acknowledgements I am sincerely grateful for the outstanding supervision and mentorship I received from Drs Susan Kutz and Eric Hoberg, who for many times believed in myself much more than I did. Susan, thank you so much for your dedication, availability, support, enthusiasm and patience. Thanks for helping to make me a better professional. Equally, I am very proud to have Eric as a mentor. Also, thanks for introducing me to the fascinating field of historical biogeography of host-parasite assemblages. It gave me another perception of the world! I extend my sincere thankfulness to all other members of my supervisory committee, Drs John Gilleard, Alessandro Massolo, and Sean Rogers. Thank you very much for contributing your diverse expertise to this project, for providing me with much valued guidance, and broadening my horizons. A special thanks to John, for all your guidance and mentorship in my career development and plans. Parasitology started in my life over a decade ago, just over a third of my life. As I conclude one more step of my academic formation I would like to recognize the profound influence from many professors that I had the pleasure of interacting and learning from during my veterinary and Masters’ degrees at the beautiful Universidade Federal Rural do Rio de Janeiro, Brazil. Among many, some deserve special mention: Fabio Barbour Scott, Laerte Grisi (in memoriam), Carlos Wilson Gomes Lopes, João Luis Horacio Faccini, and Rita de Cássia de A. A. Menezes. Thanks for infecting me with the passion for the discipline. This work could not be completed without the assistance of many people in the lab and in the field. Thanks for all the past and present members of the Kutz Lab! Many of you directly contributed to my work. I am sorry because I probably cannot even mention all the names. Special thanks to Kutz Lab Dean Brown, Jesse Invik, James Wang, Pat Curry, Bryanne Hoar, v Marianne Jorgenson, Jaynnin Yue, Pauline Bourdette, Kim Koczka, Lynn Klassen, Kamala Sapkota, Pratap Kafle. Special thanks to Manigandan Lejeune and Umer Naveed Chaudhry, who encouraged me taking another big challenge: the board certification in Veterinary Parasitology, and the numerous conversations about career and the future. This work could not be done without a wide collaborative network. I would like to thank Manon Simard, Alasdair Veitch, Richard Popko, Kimberlee Beckmen, Marco Musiani, Margo Pybus, Troy Hegel, Helen Schwantje, Brad and Diane Culling, Robert Serrouya, Serge Couturier, Christine Doucet , Mathieu Dumond, Layne Adams, Sam Wasser, Micheline Manseau, Art Rodgers, Greg Finstad, Heather Stewart, Art Abrams, Patricia Pillit, Rebecca Davidson and the Norwegians, Mariana Panayotova-Pencheva, Arseny Makarikov, etc. Many of these and many others are also mentioned in the acknowledgements of thesis chapters. During these 5-and-a-half years, I was privileged of having many friends here in Calgary that supported me in good and bad times of this long and tough battle! To mention a few: Cyntia Kayo Kashivakura, Mark Chayakul, Stefano Liccioli, Mathieu Pruvot, Regula Waeckerlin, Taya Forde, Camila Dores, Sampson Law, Stefano Catalano, Kathryn Berger, Maria Negron, Anna Zuliani, Larissa Ozeki and Tulio, Barbara Wolfger, Cristina Solis, Laura Solano, Andrew Rezansoff, Marta Marchini, Brad Van Paridon, etc. You were my family away from home! Also, I would like to thank many of my non-UCVM friends, including Felipe Alonso, Michel Araujo, Bruno Medeiros, Ryan Lock and others for the being there for me in the good and the stressful moments. Not only friends that were physically present in Calgary gave me the much needed support. Special thanks go to Clarissa Pimentel de Souza for the true friendship and support! Thank you and Obrigado! vi vii I dedicate this thesis to my family that from far away gave me the means
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