Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-17T10:13:24.540Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological and molecular characterization of Quinqueserialis (Digenea: Notocotylidae) species diversity in North America

Published online by Cambridge University Press:  24 May 2021

Demi K. Gagnon Open the ORCID record for Demi K. Gagnon [Opens in a new window] ,
Emily A. Kasl ,
Whitney C. Preisser ,
Lisa K. Belden  and
Jillian T. Detwiler
Demi K. Gagnon*
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MBR3T 2N2, Canada
Emily A. Kasl
Affiliation:
Department of Biology, University of North Alabama, Florence, AL35632, USA
Whitney C. Preisser
Affiliation:
School of Aquatic and Fishery Science, University of Washington, Seattle, WA98105, USA
Lisa K. Belden
Affiliation:
Department of Biological Sciences, Virginia Tech, Blacksburg, VA24061, USA
Jillian T. Detwiler
Affiliation:
Department of Biological Sciences, University of Manitoba, Winnipeg, MBR3T 2N2, Canada
*
Author for correspondence: Demi K. Gagnon, E-mail: demi.gagnon@live.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Estimates of trematode diversity are inaccurate due to unrecognized cryptic species and phenotypic plasticity within species. Integrative taxonomy (genetics, morphology and host use) increases the clarity of species delineation and improves knowledge of parasite biology. In this study, we used this approach to resolve taxonomic issues and test hypotheses of cryptic species in a genus of trematode, Quinqueserialis. Specimens from throughout North America were field collected from hosts and obtained from museums. We found three morphologically distinct groups and successfully sequenced specimens from two of these groups. DNA sequencing at the 28S and CO1 gene regions revealed that two of the three groups were genetically distinct. One genetic group included two morphological clusters demonstrating host-induced phenotypic plasticity within Quinqueserialis quinqueserialis. The other unique genetic group is a novel species, Quinqueserialis kinsellai n. sp., which is described herein. Our study illustrates the importance of integrating multiple sources of evidence when investigating trematode diversity to account for the influence of cryptic species or phenotypic plasticity. However, further sampling is needed to understand Quinqueserialis spp. diversity as some species have no genetic information associated with them.

Keywords

Cryptic speciesintegrative taxonomynovel speciestrematode
Type
Research Article
Information
Parasitology , Volume 148 , Issue 9 , August 2021 , pp. 1083 - 1091
Check for updates
Copyright
Copyright © The Author(s), 2021. 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

Sequencher® version 5.4.6 DNA sequence analysis software, Gene Codes Corporation, Ann Arbor, MI USA http://www.genecodes.com.Google Scholar
Abdi, H and Williams, LJ (2010) Principal component analysis. WIREs Computational Statistics 2, 433–459.CrossRefGoogle Scholar
Baker, RJ and Bradley, RD (2006) Speciation in mammals and the genetic species concept. Journal of Mammalogy 87, 643–662.CrossRefGoogle ScholarPubMed
Barker, FD and Laughlin, JW (1911) A new species of trematode from the muskrat, Fiber zibethicus. Transactions of the American Microscopical Society 30, 261–274.CrossRefGoogle Scholar
Blasco-Costa, I, Balbuena, JA, Raga, JA, Kostadinova, A and Olson, PD (2010) Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 137, 287–302.CrossRefGoogle ScholarPubMed
Blasco-Costa, I, Cutmore, SC, Miller, TL and Nolan, MJ (2016) Molecular approaches to trematode systematics: “best practice” and implications for future study. Systematic Parasitology 93, 295–306.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
Detwiler, JT, Zajac, AM, Minchella, DJ and Belden, LK (2012) Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. Journal of Parasitology 98, 1148–1155.CrossRefGoogle Scholar
Gagnon, DK and Detwiler, JT (2019) Broader geographic sampling increases extent of intermediate host specificity for a trematode parasite (Notocotylidae: Quinqueserialis quinqueserialis). Journal of Parasitology 105, 874–877.CrossRefGoogle Scholar
Getz, LL (1961) Home ranges, territoriality, and movement of the meadow vole. Journal of Mammology 42, 24–36.CrossRefGoogle Scholar
Harwood, PD (1939) Notes on Tennessee helminths. IV. North American trematodes of the subfamily Notocotylinae. Journal of the Tennessee Academy of Science 14, 421–437.Google Scholar
Herber, EC (1942) Life history studies on two trematodes of the subfamily Notocotylinae. Journal of Parasitology 28, 179–196.CrossRefGoogle Scholar
Kinsella, JM (1969) Intraspecific Variation of Quinqueserialis quinqueserialis (Barker and Laughlin 1911) in Rodent Hosts (PhD Dissertation). University of Montana.Google Scholar
Kinsella, JM (1971) Growth, development, and intraspecific variation of Quinqueserialis quinqueserialis (Trematoda: Notocotylidae) in rodent hosts. Journal of Parasitology 57, 62–70.CrossRefGoogle Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lively, CM (1999) Migration, virulence, and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34–S47.CrossRefGoogle ScholarPubMed
Marinelli, L and Messier, F (1993) Space use and the social system of muskrats. Canadian Journal of Zoology 71, 869–875.CrossRefGoogle Scholar
McIntosh, A and McIntosh, G (1934) A new trematode, Notocotylus hassalli, n. sp. (Notocotylidae), from a meadow mouse. Proceedings of the Helminthological Society of Washington 1, 36–37.Google Scholar
Moszczynska, A, Locke, SA, McLaughlin, D, Marcogliese, DJ and Crease, TJ (2009) Development of primers for the mitochondrial cytochrome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9, S75–S82.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, FG, Friendly, M, Kindt, R, Legendre, P, McGlinn, D, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH, Szoecs, E and Wagner, H (2019) Vegan: Community ecology package. R package version 2.5–4.Google Scholar
Olson, PD, Cribb, TH, Tkach, VVR, Bray, A and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Hernández-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the 'next-generation' Tree of Life. Journal of Helminthology 93, 260–276.CrossRefGoogle ScholarPubMed
Pérez-Ponce de León, G and Nadler, SA (2010) What we don’t recognize can hurt us: a plea forawareness about cryptic species. Journal of Parasitology 96, 453–464.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Poulin, R (2017) An updated look at the uneven distribution of cryptic diversity among parasitic helminths. Journal of Helminthology 92, 197–202.CrossRefGoogle Scholar
Pleijel, F, Jondelius, U, Norlinder, E, Nygren, A, Oxelman, B, Schander, C, Sundberg, P and Thollesson, M (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Molecular Phylogenetics and Evolution 48, 369–371.CrossRefGoogle Scholar
Poulin, R and Leung, TLF (2010) Taxonomic resolution in parasite community studies: are things getting worse? Parasitology 137, 1967–1973.CrossRefGoogle ScholarPubMed
Rausch, R (1952 a) Helminths from the round-tailed muskrat, Neofiber alleni nigrescens Howell, with descriptions of two new species. Journal of Parasitology 38, 151–156.CrossRefGoogle Scholar
Rausch, R (1952 b) Studies on the helminth fauna of Alaska. XI. Helminth parasites of microtine rodents—taxonomic considerations. Journal of Parasitology 38, 415–444.CrossRefGoogle ScholarPubMed
Smith, CF (1954) Studies on Quinqueserialis hassalli and taxonomic considerations of the species of Quinqueserialis (Trematoda: Notocotylidae). Journal of Parasitology 40, 209–215.CrossRefGoogle Scholar
Van Steenkiste, N, Locke, SA, Castelin, M, Marcogliese, DJ and Abbott, CL (2015) New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources 15, 945–952.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th Edn. New York, NY, USA: Springer.CrossRefGoogle Scholar
Vilas, R, Criscione, CD and Blouin, MS (2005) A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 1–8.CrossRefGoogle ScholarPubMed
Supplementary material: File

Gagnon et al. supplementary material

Tables S1-S4

Download Gagnon et al. supplementary material(File)
File 31.6 KB