Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-20T10:26:55.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Genetic analyses of the parasitic nematode, Parelaphostrongylus tenuis, in Missouri and Kentucky reveal unexpected levels of diversity and population differentiation

Published online by Cambridge University Press:  15 October 2020

L. S. Eggert Open the ORCID record for L. S. Eggert [Opens in a new window] ,
L. K. Berkman ,
K. Budd ,
B. J. Keller ,
A. M. Hildreth  and
J. J. Millspaugh
L. S. Eggert*
Affiliation:
Division of Biological Sciences, University of Missouri, 226 Tucker Hall, Columbia, MO65211, USA
L. K. Berkman
Affiliation:
Missouri Department of Conservation, Central Regional Office and Conservation Research Center, 3500 E. Gans Rd., Columbia, MO65201, USA
K. Budd
Affiliation:
Division of Biological Sciences, University of Missouri, 226 Tucker Hall, Columbia, MO65211, USA
B. J. Keller
Affiliation:
Missouri Department of Conservation, Central Regional Office and Conservation Research Center, 3500 E. Gans Rd., Columbia, MO65201, USA Minnesota Department of Natural Resources, 500 Lafayette Rd., St. Paul, MN50575, USA
A. M. Hildreth
Affiliation:
Missouri Department of Conservation, Central Regional Office and Conservation Research Center, 3500 E. Gans Rd., Columbia, MO65201, USA
J. J. Millspaugh
Affiliation:
Wildlife Biology Program, University of Montana, 32 Campus Drive, Missoula, MT59812, USA
*
Author for correspondence: L. S. Eggert, E-mail: eggertl@missouri.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Wildlife translocations, which involve the introduction of naive hosts into new environments with novel pathogens, invariably pose an increased risk of disease. The meningeal worm Parelaphostrongylus tenuis is a nematode parasite of the white-tailed deer (Odocoileus virginianus), which serves as its primary host and rarely suffers adverse effects from infection. Attempts to restore elk (Cervus canadensis) to the eastern US have been hampered by disease caused by this parasite. Using DNA sequence data from mitochondrial and nuclear genes, we examined the hypothesis that elk translocated within the eastern US could be exposed to novel genetic variants of P. tenuis by detailing the genetic structure among P. tenuis taken from white-tailed deer and elk at a source (Kentucky) and a release site (Missouri). We found high levels of diversity at both mitochondrial and nuclear DNA in Missouri and Kentucky and a high level of differentiation between states. Our results highlight the importance of considering the potential for increased disease risk from exposure to novel strains of parasites in the decision-making process of a reintroduction or restoration.

Keywords

Brainwormdeer parasiteelkmeningeal wormpopulation structuretranslocation
Type
Research Article
Information
Parasitology , Volume 148 , Issue 1 , January 2021 , pp. 31 - 41
Check for updates
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acevedo-Whitehouse, K, Spraker, TR, Lyons, E, Melin, SR, Gulland, F, Delong, RL and Amos, W (2006) Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Molecular Ecology 15, 1973–1982.CrossRefGoogle ScholarPubMed
Aiello, CM, Nussear, KE, Walde, AD, Esque, TC, Emblidge, PG, Sah, P, Bansal, S and Hudson, PJ (2014) Disease dynamics during wildlife translocations: disruptions to the host population and potential consequences for transmission in desert tortoise contact networks. Animal Conservation 17, 27–39.CrossRefGoogle Scholar
Anderson, RC (1963) The incidence, development, and experimental transmission of Parelaphostrongylus tenuis Dougherty (Metastrongyloidea: Protostrongylidae) of the meninges of the white-tailed deer (Odocoileus virginianus borealis) in Ontario. Canadian Journal of Zoology 41, 775–792.CrossRefGoogle Scholar
Anderson, RC (1972) The ecological relationships of meningeal worm and native cervids in North America. Journal of Wildlife Diseases 8, 304–310.CrossRefGoogle ScholarPubMed
Asmundsson, IM, Mortenson, JA and Hoberg, EP (2008) Muscleworms, Parelaphostrongylus andersoni (Nematoda: Protostrongylidae), discovered in the Columbian white-tailed deer from Oregon and Washington: implications for biogeography and host associations. Journal of Wildlife Diseases 44, 16–27.CrossRefGoogle Scholar
Ballou, JD (1993) Assessing the risks of infectious diseases in captive breeding and reintroduction programs. Journal of Zoo and Wildlife Medicine 24, 327–335.Google Scholar
Batson, WG, Gordon, IJ, Fletcher, DB and Manning, AD (2015) Translocation tactics: a framework to support the IUCN guidelines for wildlife translocations and improve the quality of applied methods. Journal of Applied Ecology 52, 1598–1607.CrossRefGoogle Scholar
Bender, LC, Schmitt, SM, Carlson, E, Haufler, JB and Beyer, DE Jr (2005) Mortality of Rocky Mountain elk in Michigan due to meningeal worm. Journal of Wildlife Diseases 41, 134–140.CrossRefGoogle ScholarPubMed
Bennitt, R and Nagel, WO (1937) A survey of the resident game and furbearers of Missouri. University of Missouri Studies XII, 77–85.Google Scholar
Blanchong, JA, Samuel, MD, Scribner, KT, Weckworth, BV, Langenberg, JA and Filcek, KB (2007) Landscape genetics and the spatial distribution of chronic wasting disease. Biology Letters 4, 130–133.CrossRefGoogle Scholar
Blouin, MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle ScholarPubMed
Blouin, MS, Yowell, CA, Courtney, CH and Dame, JB (1995) Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.Google ScholarPubMed
Blouin, MS, Yowell, CA, Courtney, CH and Dame, JB (1998) Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 1719–1727.CrossRefGoogle ScholarPubMed
Budd, K, Berkman, LK, Anderson, M, Koppelman, J and Eggert, LS (2018) Genetic structure and recovery of white-tailed deer in Missouri. Journal of Wildlife Management 82, 1598–1607.CrossRefGoogle Scholar
Carpenter, JW, Jordan, HE and Ward, BC (1973) Neurologic disease in wapiti naturally infected with meningeal worms. Journal of Wildlife Diseases 9, 148–153.CrossRefGoogle ScholarPubMed
Carreno, RA, Caporaso, D, Beade, MS, Marull, C, Uhart, MM, Markwardt, DD and Nadler, SA (2012) Discovery of an undescribed protostrongylid nematode from the endangered pampas deer (Ozotoceros bezoarticus celer) in Argentina. Journal of Wildlife Diseases 48, 724–731.CrossRefGoogle Scholar
Chitwood, MC, Keller, BJ, Al-Warid, HS, Straka, K, Hildreth, AM, Hansen, L and Millspaugh, JJ (2018) Meningeal worm (Parelaphostrongylus tenuis) as a cause of mortality in the elk (Cervus canadensis) population in Missouri, USA. Journal of Wildlife Diseases 54, 95–100.CrossRefGoogle ScholarPubMed
Clement, M, Snell, Q, Walke, P, Posada, D and Crandall, K (2002) TCS: estimating gene genealogies. Proceedings of the 16th International Parallel and Distributed Processing Symposium 2, 184.CrossRefGoogle Scholar
Comer, CE, Kilgo, JC, D'Angelo, GJ, Glenn, TC and Miller, KV (2005) Fine-scale genetic structure and social organization in female white-tailed deer. Journal of Wildlife Management 69, 332–344.2.0.CO;2>CrossRefGoogle Scholar
Cullingham, CI, Merrill, EH, Pybus, MJ, Bollinger, TK, Wilson, GA and Coltman, DW (2011) Broad and fine-scale genetic analysis of white-tailed deer populations: estimating the relative risk of chronic wasting disease spread. Evolutionary Applications 4, 116–131.CrossRefGoogle ScholarPubMed
Cunningham, AA (1996) Disease risks of wildlife translocations. Conservation Biology 10, 349–353.CrossRefGoogle Scholar
Dent, R (2014) Elk Restoration 2010–2013. Jefferson City, MO: Missouri Department of Conservation, 682 pp.Google Scholar
Deyoung, RW, Demarais, S, Honeycutt, RL, Rooney, AP, Gonzales, RA and Gee, KL (2003) Genetic consequences of white-tailed deer (Odocoileus virginianus) restoration in Mississippi. Molecular Ecology 12, 3237–3252.CrossRefGoogle ScholarPubMed
Dobey, CL, Grunenwald, C, Newman, SJ, Muller, L and Gerhold, RW (2014) Retrospective study of central nervous system lesions and association with Parelaphostrongylus species by histology and specific nested polymerase chain reaction in domestic camelids and wild ungulates. Journal of Veterinary Diagnostic Investigation 26, 748–754.CrossRefGoogle ScholarPubMed
Doerner, KC, Braden, W, Cork, J, Cunningham, T, Rice, A, Furman, BJ and McElroy, D (2005) Population genetics of resurgence: white-tailed deer in Kentucky. Journal of Wildlife Management 69, 345–355.2.0.CO;2>CrossRefGoogle Scholar
Dybdahl, MF and Storfer, A (2003) Parasite local adaptation: red queen versus suicide king. Trends in Ecology & Evolution 18, 523–530.CrossRefGoogle Scholar
Eveland, JF, George, JL, Hunter, NB, Forney, DM and Harrison, RL (1979) A preliminary evaluation of the ecology of the elk in Pennsylvania. In Boyce, MS and Hayden-Wing, LD (eds), North American elk: Ecology, Behavior, and Management. Laramie, Wyoming: University of Wyoming, pp. 145–151.Google Scholar
Ewen, JG, Acevedo-Whitehouse, K, Alley, MR, Carraro, C, Sainsbury, AW, Swinnerton, K and Woodroffe, R (2012) Empirical consideration of parasites and health in reintroduction. In Ewen, JG, Armstrong, DP, Parker, KA and Seddon, PJ (eds), Reintroduction Biology: Integrating Science and Management. Oxford, UK: Blackwell Publishing Ltd., pp. 290–335.CrossRefGoogle Scholar
Excoffier, L and Lischer, HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Faria, PJ, van Oosterhout, C and Cable, J (2010) Optimal release strategies for captive-bred animals in reintroduction programs: experimental infections using the guppy as a model organism. Biological Conservation 14, 35–41.CrossRefGoogle Scholar
Gajadhar, A, Steeves-Gurnsey, R, Kendall, J, Lankester, M and Stéen, M (2000) Differentiation of dorsal-spined elaphostrongyline larvae by polymerase chain reaction amplification of ITS-2 of rDNA. Journal of Wildlife Diseases 36, 370–373.CrossRefGoogle ScholarPubMed
Gassett, JW (2001) Restoration of white-tailed deer in Kentucky: from absence to overabundance. In Maehr, DS, Noss, RF and Larkin, JL (eds), Large Mammal Restoration: Ecological and Sociological Challenges in the 21st Century. Washington, DC, USA: Island Press, pp. 119–123.Google Scholar
Gerhold, R and Hickling, G (2016) Diseases associated with translocations of captive cervids in North America. Wildlife Society Bulletin 40, 25–31.CrossRefGoogle Scholar
Gerhold, RW, Keel, MK, Arnold, K, Hotton, D and Beckstead, RB (2010) Parelaphostrongylus tenuis-associated meningoencephalitis in a sika deer (Cervus Nippon). Journal of Wildlife Diseases 46, 287–290.CrossRefGoogle Scholar
Gerhold, R, Grunenwald, C, Muller, L and Su, C (2016) Genetic characterization of the meningeal worm Parelaphostrongylus tenuis from multiple host species and across spatial scales. July, 2016, 65th Annual International Conference of the Wildlife Disease Association, Cortland, NY, USA. Available at http://programme.exordo.com/wda2016/.Google Scholar
Hartley, M and Sainsbury, A (2017) Methods of disease risk analysis in wildlife translocations for conservation purposes. EcoHealth 14, 16–29.CrossRefGoogle ScholarPubMed
Jacques, CN, Jenks, JA, Grovenburg, TW, Klaver, RW and Dubay, SA (2015) Influence of ecologic factors on prevalence of meningeal worm (Parelaphostrongylus tenuis) infection in South Dakota, USA. Journal of Wildlife Diseases 51, 332–340.CrossRefGoogle ScholarPubMed
Keller, BJ, Montgomery, RA, Campa, HR III, Beyer, DE Jr, Winterstein, SR, Hansen, LP and Millspaugh, JJ (2015) A review of vital rates and cause-specific mortality of elk Cervus elaphus populations in eastern North America. Mammal Review 45, 146–159.CrossRefGoogle Scholar
Kutz, SJ, Veitch, AM, Hoberg, EP, Elkin, BT, Jenkins, EJ and Polley, L (2001) New host and geographic records for two protostrongylids in Dall's sheep. Journal of Wildlife Diseases 37, 761–774.CrossRefGoogle ScholarPubMed
Lankester, MW (2001) Extrapulmonary lungworms of cervids. In Samuel, WM, Pybus, MJ and Kocan, AA (eds), Parasitic Diseases of Wild Mammals. Ames, IA, USA: Iowa State University Press, pp. 228–278.CrossRefGoogle Scholar
Lankester, MW (2010) Understanding the impact of meningeal worm, Parelaphostrongylus tenuis, on moose populations. ALCES 46, 53–70.Google Scholar
Lankester, MW and Anderson, RC (1968) Gastropods as intermediate hosts of Pneumostrongylus tenuis Dougherty of whitetailed deer. Canadian Journal of Zoology 46, 373–383.CrossRefGoogle Scholar
Larkin, JL, Alexy, KJ, Bolin, DC, Maehr, DS, Cox, JJ, Wichrowski, MW and Seward, N (2003) Meningeal worm in a reintroduced elk population in Kentucky. Journal of Wildlife Diseases 39, 588–592.CrossRefGoogle Scholar
Leigh, JW and Bryant, D (2015) PopART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6, 1110–1116.CrossRefGoogle Scholar
LoGiudice, K (2003) Trophically transmitted parasites and the conservation of small populations: raccoon roundworm and the imperiled Allegheny woodrat. Conservation Biology 17, 258–266.CrossRefGoogle Scholar
Lopez, JV, Yuhki, N, Modi, W, Masuda, R and O'Brien, SJ (1994) Numt, a recent transfer and tandem amplification of mitochondrial DNA in the nuclear genome of the domestic cat. Journal of Molecular Evolution 39, 174–190.Google ScholarPubMed
Mathews, F, Moro, D, Strachan, R, Gelling, M and Buller, N (2006) Health surveillance in wildlife reintroductions. Biological Conservation 131, 338–347.CrossRefGoogle Scholar
McDonald, JS and Miller, KV (2004) A History of White-Tailed Deer Restocking in the United States 1878 to 2004. Bogart, GA, USA: The Quality Deer Management Association.Google Scholar
Mitchell, KJ, Peters-Kennedy, J, Stokol, T, Gerhold, RW, Beckstead, R and Divers, T (2011) Parelaphostrongylus tenuis infections as a cause of meningomyelitis in 5 calves. Journal of Veterinary Internal Medicine 23, 1097–1103.Google Scholar
Nadler, SA (1992) Phylogeny of some ascaridoid nematodes, inferred from comparison of 18S and 28S rRNA sequences. Molecular Biology and Evolution 9, 932–944.Google ScholarPubMed
Parker, KA, Dickens, MJ, Clarke, RH, Lovegrove, TG, Ewen, JG and Armstrong, DP (2012) The theory and practice of catching, holding, moving and releasing animals. In Ewen, JG, Armstrong, DP, Parker, KA and Seddon, PJ (eds), Reintroduction Biology: Integrating Science and Management. Oxford, UK: Blackwell Publishing Ltd., pp. 105–137.CrossRefGoogle Scholar
Poulin, R (2007). Evolutionary Ecology of Parasites, 2nd Edn. Princeton, NJ, USA: Princeton University Press.CrossRefGoogle Scholar
Raskevitz, RF, Kocan, AA and Shaw, JH (1991) Gastropod availability and habitat utilization by wapiti and white-tailed deer sympatric on range enzootic for meningeal worm. Journal of Wildlife Diseases 27, 92–101.CrossRefGoogle ScholarPubMed
Samuel, WM, Pybus, MJ, Welch, DA and Wilke, CJ (1992) Elk as a potential host for meningeal worm: implications for translocation. Journal of Wildlife Management 56, 629–639.CrossRefGoogle Scholar
Savage, AE and Zamudio, KR (2011) MHC Genotypes associate with resistance to a frog-killing fungus. Proceedings of the National Academy of Sciences, USA 108, 16705–16710.CrossRefGoogle ScholarPubMed
Seddon, PJ, Armstrong, DP and Maloney, RF (2007) Developing the science of reintroduction biology. Conservation Biology 21, 303–312.CrossRefGoogle ScholarPubMed
Seddon, PJ, Strauss, WM and Innes, J (2012) Animal translocations: what are they and why do we do them. In Ewen, JG, Armstrong, DP, Parker, KA and Seddon, PJ (eds), Reintroduction Biology: Integrating Science and Management. Oxford, UK: Blackwell Publishing Ltd., pp. 1–32.Google Scholar
Severinghaus, CW and Darrow, RW (1976) Failure of elk to survive in the Adirondacks. New York Fish and Game Journal 23, 98–99.Google Scholar
Shostak, AW and Samuel, WM (1984) Moisture and temperature effects on survival and infectivity of first-stage larvae of Parelaphostrongylus odocoilei and P. tenuis (Nematoda: Metastrongyloidea). Journal of Parasitology 70, 261–269.CrossRefGoogle Scholar
Slabach, BL, Hast, JT, Murphy, SM, Bowling, WE, Crank, RD, Jenkins, G, Johannsen, K and Cox, JJ (2018) Survival and cause-specific mortality of elk Cervus canadensis in Kentucky, USA. Wildlife Biology 2018, wlb-00459. doi: 10.2981/wlb.00459.CrossRefGoogle Scholar
Southard, T, Bender, H, Wade, SE, Grunenwald, C and Gerhold, RW (2012) Naturally occurring Parelaphostrongylus tenuis-associated choriomeningitis in a guinea pig with neurologic signs. Veterinary Pathology 50, 560–562.CrossRefGoogle Scholar
Swoffford DL, (2002) PAUP*: Phylogenetic analysis using parsimony (and other methods), version 4.0 b10. Sunderland, UK: Sinauer Associates.Google Scholar
Tanabe, M, Gerhold, RW, Beckstead, RB, de Lahunta, A and Wade, SE (2010) Molecular confirmation of Parelaphostrongylus tenuis infection in a horse with verminous encephalitis. Veterinary Pathology 47, 759.CrossRefGoogle Scholar
Viggers, KL, Lindenmayer, DB and Spratt, DM (1993) The importance of disease in reintroduction programmes. Wildlife Research 20, 687–698.CrossRefGoogle Scholar
Villesen, P (2007) FaBox: an online toolbox for fasta sequences. Molecular Ecology Notes 7, 965–968.CrossRefGoogle Scholar
Wasel, SM, Samuel, WM and Crichton, V (2003) Distribution and ecology of meningeal worm, Parelaphostrongylus tenuis (Nematoda), in northcentral North America. Journal of Wildlife Diseases 39, 338–346.CrossRefGoogle Scholar
Weiss, RB, Sarver, CS, Thilsted, J and Wolfe, BA (2008) Clinical Parelaphostrongylus tenuis infection in two captive American bison (Bison bison). Journal of the American Veterinary Medical Association 233, 1127–1130.CrossRefGoogle Scholar
Whitehead, CE and Bedenice, D (2009) Neurologic diseases in llamas and alpacas. Veterinary Clinics of North America Food Animal Practice 25, 385–405.CrossRefGoogle ScholarPubMed
Supplementary material: File

Eggert et al. supplementary material

Table S1

Download Eggert et al. supplementary material(File)
File 42 KB