Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-17T14:33:41.820Z Has data issue: false hasContentIssue false

Molecular phylogenetic analysis of Neodiplostomum and Fibricola (Digenea, Diplostomidae) does not support host-based systematics

Published online by Cambridge University Press:  19 January 2022

Tyler J. Achatz
Affiliation:
Department of Biology, University of North Dakota, Starcher Hall, 10 Cornell Street Stop 9019, Grand Forks, North Dakota 58202, USA Department of Natural Sciences, Middle Georgia State University, Macon, Georgia 31206, USA
Eric E. Pulis
Affiliation:
Department of Science and Mathematics, Northern State University, Aberdeen, South Dakota 57401, USA
Ethan T. Woodyard
Affiliation:
Department of Pathobiology and Population Medicine, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi 39762, USA
Thomas G. Rosser
Affiliation:
Department of Comparative Biomedical Sciences, College of Veterinary Medicine, Mississippi State University, Mississippi State, Mississippi 39762, USA
Jakson R. Martens
Affiliation:
Department of Biology, University of North Dakota, Starcher Hall, 10 Cornell Street Stop 9019, Grand Forks, North Dakota 58202, USA
Sara B. Weinstein
Affiliation:
School of Biological Sciences, University of Utah, Salt Lake City, Utah 84112, USA
Alan Fecchio
Affiliation:
Programa de Pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Federal de Mato Grosso, Cuiabá, Mato Grosso 78060900, Brazil
Chris T. McAllister
Affiliation:
Science and Mathematics Division, Eastern Oklahoma State College, Idabel, Oklahoma 74745, USA
Carlos Carrión Bonilla
Affiliation:
Museo de Zoología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador
Vasyl V. Tkach*
Affiliation:
Department of Biology, University of North Dakota, Starcher Hall, 10 Cornell Street Stop 9019, Grand Forks, North Dakota 58202, USA
*
Author for correspondence: Vasyl Tkach, E-mail: vasyl.tkach@und.edu

Abstract

Fibricola and Neodiplostomum are diplostomid genera with very similar morphology that are currently separated based on their definitive hosts. Fibricola spp. are normally found in mammals, while Neodiplostomum spp. typically parasitize birds. Previously, no DNA sequence data was available for any member of Fibricola. We generated nuclear ribosomal and mtDNA sequences of Fibricola cratera (type-species), Fibricola lucidum and 6 species of Neodiplostomum. DNA sequences were used to examine phylogenetic interrelationships among Fibricola and Neodiplostomum and re-evaluate their systematics. Molecular phylogenies and morphological study suggest that Fibricola should be considered a junior synonym of Neodiplostomum. Therefore, we synonymize the two genera and transfer all members of Fibricola into Neodiplostomum. Specimens morphologically identified as Neodiplostomum cratera belonged to 3 distinct phylogenetic clades based on mitochondrial data. One of those clades also included sequences of specimens identified morphologically as Neodiplostomum lucidum. Further study is necessary to resolve the situation regarding the morphology of N. cratera. Our results demonstrated that some DNA sequences of N. americanum available in GenBank originate from misidentified Neodiplostomum banghami. Molecular phylogentic data revealed at least 2 independent host-switching events between avian and mammalian hosts in the evolutionary history of Neodiplostomum; however, the directionality of these host-switching events remains unclear.

Type
Research Article
Copyright
Copyright © The Author(s), 2022. 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

Achatz, TJ, Curran, SS, Patitucci, KF, Fecchio, A and Tkach, VV (2019 a) Phylogenetic affinities of Uvulifer spp. (Digenea: Diplostomidae) in the Americas with description of two new species from Peruvian Amazon. Journal of Parasitology 105, 704717.CrossRefGoogle ScholarPubMed
Achatz, TJ, Dmytrieva, I, Kuzmin, Y and Tkach, VV (2019 b) Phylogenetic position of Codonocephalus Diesing, 1850 (Digenea, Diplostomoidea), an unusual diplostomid with progenetic metacercariae. Journal of Parasitology 105, 821826.CrossRefGoogle Scholar
Achatz, TJ, Pulis, EE, Fecchio, A, Schlosser, IJ and Tkach, VV (2019 c) Phylogenetic relationships, expanded diversity and distribution of Crassiphiala spp. (Digenea, Diplostomidae), agents of black spot disease in fish. Parasitology Research 118, 27812787.CrossRefGoogle Scholar
Achatz, TJ, Pulis, EE, Junker, K, Tran, BT, Snyder, SD and Tkach, VV (2019 d) Molecular phylogeny of the Cyathocotylidae (Digenea, Diplostomoidea) necessitates systematic changes and reveals a history of host and environment switches. Zoologica Scripta 48, 545556.CrossRefGoogle ScholarPubMed
Achatz, TJ, Pulis, EE, González-Acuña, D and Tkach, VV (2020) Phylogenetic relationships of Cardiocephaloides spp. (Digenea, Diplostomoidea) and the genetic characterization of Cardiocephaloides physalis from Magellanic penguin, Spheniscus magellanicus, in Chile. Acta Parasitologica 65, 525534.CrossRefGoogle ScholarPubMed
Achatz, TJ, Bell, JA, Melo, FTV, Fecchio, A and Tkach, VV (2021 a) Phylogenetic position of Sphincterodiplostomum Dubois, 1936 (Digenea: Diplostomoidea) with description of a second species from Pantanal, Brazil. Journal of Helminthology 95, E6.CrossRefGoogle ScholarPubMed
Achatz, TJ, Brito, ES, Fecchio, A and Tkach, VV (2021 b) Description and phylogenetic position of a new species of Herpetodiplostomum from Phrynops geoffroanus in Brazil and a re-evaluation of Cheloniodiplostomum. Journal of Parasitology 107, 455462.CrossRefGoogle Scholar
Achatz, TJ, Chermak, TP, Martens, JR, Pulis, EE, Fecchio, A, Bell, JA, Greiman, SE, Cromwell, KJ, Brant, SV, Kent, ML and Tkach, VV (2021 c) Unravelling the diversity of the Crassiphialinae (Digenea: Diplostomidae) with molecular phylogeny and descriptions of five new species. Current Research in Parasitology & Vector-Borne Diseases 1, 100051.CrossRefGoogle ScholarPubMed
Achatz, TJ, Martens, JR, Kostadinova, A, Pulis, EE, Orlofske, SA, Bell, JA, Fecchio, A, Oyarzún-Ruiz, P, Syrota, YY and Tkach, VV (2022) Molecular phylogeny of Diplostomum, Tylodelphys, Austrodiplostomum and Paralaria (Digenea: Diplostomidae) necessitates systematic changes and reveals a history of evolutionary host switching events. International Journal for Parasitology 52, 47–63. doi: 10.1016/j.ijpara.2021.06.002CrossRefGoogle ScholarPubMed
Achatz, TJ, Chermak, TP, Martens, JR, Woodyard, ET, Rosser, TG, Pulis, EE, Weinstein, SB, McAllister, CT, Kinsella, JM and Tkach, VV (in press) Molecular phylogeny supports invalidation of Didelphodiplostomum and Pharyngostomoides (Digenea: Diplostomoidea) and reveals a Tylodelphys from mammals. Zoological Journal of the Linnean Society.Google Scholar
Barker, F (1915) Parasites of the American muskrat (Fiber zibethicus). Journal of Parasitology 1, 184195.CrossRefGoogle Scholar
Bisseru, B (1957) On two new trematodes (Proterodiplostomidae) from an African crocodile, and a list of strigeid parasites from Africa. Journal of Helminthology 31, 85102.CrossRefGoogle Scholar
Blasco-Costa, I and Locke, SA (2017) Life history, systematics and evolution of the Diplostomoidea Poirier, 1886: progress, promises and challenges emerging from molecular studies. Advances in Parasitology 98, 167225.CrossRefGoogle ScholarPubMed
Bolek, MG and Coggins, JR (2003) Helminth community structure of sympatric eastern American toad, Bufo americanus, northern leopard frog, Rana pipiens and blue-spotted salamander, Ambystoma laterale, from southeastern Wisconsin. Journal of Parasitology 89, 673680.CrossRefGoogle ScholarPubMed
Chandler, AC (1942) The morphology and life cycle of a new strigeid, Fibricola texensis, parasitic in raccoons. Transactions of the American Microscopical Society 61, 156167.CrossRefGoogle Scholar
Chandler, AC and Rausch, R (1946) A study of strigeids from Michigan mammals with comments on the classification of mammalian strigeids. Transactions of the American Microscopical Society 65, 328337.CrossRefGoogle Scholar
Chandler, AC and Rausch, R (1947) A study of strigeids from owls in North Central United States. Transactions of the American Microscopical Society 66, 283292.CrossRefGoogle Scholar
Cribb, TH and Pearson, JC (1993) Neodiplostomum spratti n. sp. (Digenea: Diplostomidae) from Antechinus spp. (Arsupialia: Dasyuridae) in Australia, with notes on other diplostomids from Australian mammals. Systematic Parasitology 25, 2535.CrossRefGoogle Scholar
Dubois, G (1932) Revision des Hemistomes et étude de forms nouvelles. Bulletin de la Société des Sciences Naturelles de Neuchâtel 56, 375412.Google Scholar
Dubois, G (1937) Sur quelques Strigidés. Revue Suisse de Zoologie 44, 391396.CrossRefGoogle Scholar
Dubois, G (1938) Monographie des Strigeida (Trematoda). Mémoires de la Société des Sciences Naturelles de Neuchâtel 6, 1535.Google Scholar
Dubois, G (1944) A propos de la spécificité parasitaire des Strigeida. Bulletin de la Société des Sciences Naturelles de Neuchâtel 69, 5103.Google Scholar
Dubois, G (1962) Sur quelques néodiplostomes (Trematoda: Strigeida). Bulletin de la Société Neuchâtaloise des Sciences Naturelles 85, 121142.Google Scholar
Dubois, G (1968) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mémoires de la Société des Sciences Naturelles de Neuchâtel 10, 1258.Google Scholar
Dubois, G (1970) Les fondements de la taxonomie des Strigeata La Rue (Trematoda: Strigeida). Revue Suisse de Zoologie 77, 663685.CrossRefGoogle Scholar
Dubois, G (1982) Répertoire des synonymes récents de genres et d'espéces de la superfamille des Strigeoidea Railliet, 1919 (Trematoda). Bulletin de la Société des Sciences Naturelles de Neuchâtel 105, 163183.Google Scholar
Dubois, G (1983) Quelques Strigeoidea (Trematoda) récoltés chez des oiseaux du Paraguay par la mission claude Weber, Automne 1983, du Muséum d'Histoire naturelle de Genève. Revue Suisse de Zoologie 92, 641648.CrossRefGoogle Scholar
Dubois, G and Macko, JK (1972) Contribution à l’étude des Strigeata La Rue, 1926 (Trematoda: Strigeida) de Cuba. Annales de Parasitologie Humaine et Comparee 47, 5175.CrossRefGoogle Scholar
Dubois, G and Rausch, R (1950) Troisième contribution a l’étude des strigeides (Trematoda) Nord-Américains. Société Neuchâteloise des Sciences Naturelles 73, 1950.Google Scholar
Gillilland, MG and Muzzall, PM (1999) Helminths infecting froglets of the Northern leopard frog (Rana pipiens) from Foggy Bottom Marsh, Michigan. Journal of the Helminthological Society of Washington 66, 7377.Google Scholar
Goldberg, SR and Bursey, C (2001) Intestinal helminths of four species of skinks (Mabuya) (Sauria: Scincidae) from Southern Africa. Onderstepoort Journal of Veterinary Research 68, 143147.Google ScholarPubMed
Goldberg, SR, Bursey, CR and Gergus, EWA (2001) Helminth communities of subpopulations of the Pacific treefrog, Hyla regilla (Hylidae), from Baja California, México. Southwestern Naturalist 46, 223230.CrossRefGoogle Scholar
Heneberg, P, Sitko, J and Těšínský, M (2020) Paraphyly of Conodiplostomum Dubois, 1937. Parasitology International 76, 102033.CrossRefGoogle ScholarPubMed
Hernández-Mena, DI, García-Varela, M and Pérez-Ponce de León, G (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Systematic Parasitology 94, 833848.CrossRefGoogle ScholarPubMed
Hong, ST and Shoop, WL (1994) Neodiplostomum seoulensis n. comb. (Trematoda: Neodiplostomidae). Journal of Parasitology 80, 660663.CrossRefGoogle Scholar
Huh, S, Lee, SU and Huh, SC (1994) A follow-up examination of intestinal parasitic infections of the army soldiers in Whachon-gun, Korea. Korean Journal of Parasitology 32, 6163.CrossRefGoogle ScholarPubMed
Kifune, T and Uyema, N (1982) Reports of Fukuoka University scientific expedition to Peru, 1976. Part 3. Taxonomical studies on trematodes from marsupials and rodents with records of two crabs. Medical Bulletin of Fukuoka University 9, 241256.Google Scholar
Kudlai, O, Stunžėnas, V and Tkach, V (2015) The taxonomic identity and phylogenetic relationships of Cercaria pugnax and C. helvetica XII (Digenea: Lecithodendriidae) based on morphological and molecular data. Folia Parasitologica 62, 3.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, 18701874.CrossRefGoogle ScholarPubMed
Lima, CR, Hoppe, EGL, Tebaldi, JH, Cruz, BC, Barros Gomes, AA and Nascimento, AA (2013) Gastrintestinal helminths of Cerdocyon thous (Linnaeus, 1766, Smith, 1839) from the caatinga area of the Paraíba State, Brazil. Semina Ciências Agrárias 34, 28792888.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood, DTJ and Bray, RA (eds), Interrelationships of Platyhelminthes. London, UK: Taylor & Francis, pp. 186193.Google Scholar
Locke, SA, Van Dam, AR, Caffara, M, Pinto, HA, López-Hernández, D and Blanar, CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. International Journal of Parasitology 48, 10431059.CrossRefGoogle ScholarPubMed
Locke, SA, Drago, FB, López-Hernández, D, Chibwana, FD, Núñez, V, Van Dam, A, Achinelly, MF, Johnson, PTJ, Assis, JCA, Melo, AL and Pinto, HA (2021) Intercontinental distributions, phylogenetic position and life cycles of species of Apharyngostrigea (Digenea, Diplostomoidea) illuminated with morphological, experimental, molecular and genomic data. International Journal for Parasitology 51, 667683.CrossRefGoogle ScholarPubMed
Lutz, HL, Tkach, VV and Weckstein, JD (2017) Methods for specimen-based studies of avian symbionts. In Webster, M (eds), The Role of Collections in Ornithology: The Extended Specimen. Studies in Avian Biology. Boca Raton, Florida, USA: CRC Press, pp. 157183.Google Scholar
Miller, MJ (1940) A new trematode, Fibricola laruei, from the racoon in Canada. Canadian Journal of Research 18, 333335.CrossRefGoogle Scholar
Niewiadomska, K (2002) Family Diplostomidae Poirier, 1886. In Gibson, DI, Jones, A, Bray, RA (eds), Keys to the Trematoda. Vol. I. CAB International and the Natural History Museum, London, pp. 167196.CrossRefGoogle Scholar
Odening, K (1965) Kie lebenszyklen der trematoden Neodiplostomum spathoides Dubois and N. attenuatum (V. Linstow) in Raum Berlin. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin 7, 952954.Google Scholar
Pearson, JC (1959) Observations on the morphology and life cycle of Strigea elegans Chandler & Rausch, 1947 (Trematoda: Strigeidae). Journal of Parasitology 45, 155174.CrossRefGoogle Scholar
Penrod, FW (1947) Neodiplostomum banghami, a new diplostomid strigeoidean trematode from an eagle. Transactions of the American Microscopical Society 66, 144148.CrossRefGoogle Scholar
Premvati, G and Bair, TD (1979) Trematode parasites of the opossum, Didelphis virginiana, from Florida. Proceedings of the Helminthological Society of Washington 46, 207212.Google Scholar
Queiroz, MS, López-Hernández, D, Locke, SA, Pinto, HA and Anjos, LA (2020) Metacercariae of Heterodiplostomum lanceolatum (Trematoda: Proterodiplostomidae) found in Leptodactylus podicipinus (Anura: Leptodactylidae) from Brazil: a morphological, molecular and ecological study. Journal of Helminthology 94, E66.CrossRefGoogle Scholar
Read, CP (1948) Strigeids from Texas mink with notes on the genus Fibricola Dubois. Transactions of the American Microscopical Society 67, 165168.CrossRefGoogle Scholar
Richardson, DJ (2013) Helminth parasites of the raccoon (Procyon lotor), Virginia opossum (Didelphis virginiana), and striped skunk (Mephitis mephitis) from Keith County, Nebraska. Transactions of the Nebraska Academy of Sciences and Affiliated Societies 33, 3538.Google Scholar
Ronquist, F and Huelsenbeck, JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.CrossRefGoogle ScholarPubMed
Seo, BS (1989) Comparative growth and development of the metacercariae of Fibricola seoulensis (Trematoda: Diplostomidae) in vitro, in vivo and on the chick chorioallantois. Korean Journal of Parasitology 27, 231248.CrossRefGoogle ScholarPubMed
Seo, BS, Rim, HJ and Lee, CW (1964) Studies on the parasitic helminths of Korea I. Trematodes of rodents. Korean Journal of Parasitology 2, 2026.CrossRefGoogle Scholar
Sereno-Uribe, AL, Andrade-Gómez, L, Ostrowski de Núñez, M, Pérez-Ponce de León, GP and García-Varela, M (2019) Assessing the taxonomic validity of Austrodiplostomum spp. (Digenea: Diplostomidae) through nuclear and mitochondrial data. Journal of Parasitology 105, 102112.CrossRefGoogle ScholarPubMed
Shoop, WL (1989) Systematic analysis of the Diplostomidae and Strigeidae (Trematoda). Journal of Parasitology 75, 2132.CrossRefGoogle Scholar
Snyder, SD and Tkach, VV (2007) Neosychnocotyle maggiae, n. gen., n. sp. (Platyhelminthes: Aspidogastrea) from freshwater turtles in northern Australia. Journal of Parasitology 93, 399403.CrossRefGoogle Scholar
Tkach, VV and Pawlowski, J (1999) A new method of DNA extraction from the ethanol-fixed parasitic worms. Acta Parasitologica 44, 147148.Google Scholar
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 115.CrossRefGoogle Scholar
Tkach, VV, Achatz, TJ, Pulis, EE, Junker, K, Snyder, SD, Bell, JA, Halajan, A and Melo, FTV (2020) Phylogeny and systematics of the Proterodiplostomidae Dubois, 1936 (Digenea: Diplostomoidea) reflect the complex evolutionary history of the ancient digenean group. Systematic Parasitology 97, 409439.CrossRefGoogle ScholarPubMed
Ulmer, MJ (1955) Notes on the morphology and host–parasite specificity of Fibricola cratera (Barker and Noll, 1915) Dubois 1932 (Trematoda: Diplostomatidae). Journal of Parasitology 41, 456466.CrossRefGoogle Scholar
Ulmer, MJ (1970) Notes on rearing snails in the laboratory. In MacInnis, AJ and Voge, M (eds), Experiments and Techniques in Parasitology. San Francisco, USA: WH Freeman and Company, pp. 143144.Google Scholar
Weinstein, SB, Van Wert, JC, Kinsella, JM, Tkach, VV and Laffery, KD (2019) Infection at an ecotone: cross-system foraging increases satellite parasites but decreases core parasites in raccoons. Ecology 100, e02808.CrossRefGoogle ScholarPubMed
Woodyard, ET, Rosser, TG and Griffin, MJ (2017) New data on Neodiplostomum americanum Chandler and Rausch, 1947 (Digenea: Diplostomidae), in the great horned owl Bubo virginianus Gmelin, 1788 and the eastern screech owl Megascops asio Linnaeus, 1758 in Mississippi, USA. Parasitology Research 116, 20752089.CrossRefGoogle Scholar
Zerecero, C (1943) Algunos tremátodos de las ratas domésticas de la Ciudad de México. Anales del Instituto de Biología serie Zoología 14, 507526.Google Scholar
Supplementary material: File

Achatz et al. supplementary material

Table S1

Download Achatz et al. supplementary material(File)
File 15.6 KB
Supplementary material: File

Achatz et al. supplementary material

Table S2

Download Achatz et al. supplementary material(File)
File 12.2 KB
Supplementary material: File

Achatz et al. supplementary material

Table S3

Download Achatz et al. supplementary material(File)
File 20.2 KB