Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-17T12:20:15.527Z Has data issue: false hasContentIssue false

Assessing the genetic diversity of the metacercariae of Posthodiplostomum minimum (Trematoda: Diplostomidae) in Middle American freshwater fishes: one species or more?

Published online by Cambridge University Press:  18 October 2021

Gerardo Pérez-Ponce de León*
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Ap. Postal 70-153, C.P. 04510, Ciudad de México, Mexico
Ana L. Sereno-Uribe
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Ap. Postal 70-153, C.P. 04510, Ciudad de México, Mexico
Carlos D. Pinacho-Pinacho
Affiliation:
Cátedras CONACyT, Instituto de Ecología, A.C., Red de Estudios Moleculares Avanzados, kilómetro 2.5 Ant. Carretera a Coatepec, Xalapa, Veracruz 91070, Mexico
Martín García-Varela
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Ap. Postal 70-153, C.P. 04510, Ciudad de México, Mexico
*
Author for correspondence: Gerardo Pérez-Ponce de León, E-mail: [email protected]

Abstract

Trematode taxonomy is mainly based on the morphological traits of adults. The identification of metacercariae is challenging because such traits are not developed in larval forms, and they even may show some level of morphological variability. Studies testing the potential correspondence between morphological differences and genetic variation of parasites are still lacking. The metacercariae of Posthodiplostomum minimum are probably the diplostomids more widely distributed in North and Middle American freshwater fish, and their intraspecific morphological variability has been attributed to the effect exerted by the host. Here, we tested the hypothesis whether they represent a single species, or a species complex by assessing the genetic divergence and phylogenetic relationships of metacercariae sampled from several host species in a wide geographical range across Middle America. The internal transcribed spacers (ITS1-5.8S-ITS2), and the mitochondrial COI gene were sequenced for 124 and 55 metacercariae, respectively. Phylogenetic analysis inferred from ITS sequences uncovered six well-supported monophyletic lineages. The six lineages show no correspondence to any Posthodiplostomum species for which sequences are available thus far in GenBank. Lineages exhibit some degree of host specificity; Lineages I, II, IV and V are primarily parasites of cyprinodontiforms of the families Poeciliidae, Goodeidae, Profundulidae and Fundulidae. In poeciliids there are at least four candidate species of Posthodiplostomum, some of them occurring in sympatry; instead, Lineages II and VI are exclusively parasites of cichlids. This study contributes to our understanding of the diversity of larval forms of diplostomids and provides an opportunity to further study their life cycles.

Type
Research Article
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.)

Footnotes

*

Current address: Escuela Nacional de Estudios Superiores Unidad Mérida. Universidad Nacional Autónoma de México (UNAM). Km. 4.5 Carretera Mérida-Tetiz, Municipio de Ucú, C.P. 97357, Yucatán, Mexico.

References

Achatz, TJ, Martens, JR, Kostadinova, A, Pulis, EE, Orlofske, SA, Bell, JA, Fecchio, A, Oyarzún-Ruiz, P, Syrota, YY and Tkach, VV (2021) 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 XX, XXXX. Available online 6 August 2021.Google Scholar
Aguirre-Macedo, ML, Scholz, T, González-Solís, D, Vidal-Martínez, VM, Posel, P, Arjona-Torres, G, Siu-Estrada, E and Dumailo, S (2001) Larval helminths parasitizing freshwater fishes from the Atlantic Coast of Nicaragua. Comparative Parasitology 68, 4251.Google Scholar
American Veterinary Medical Association (AVMA) (2013) Guidelines for the Euthanasia of Animals. Schaumburg, Illinois: American Veterinary Medical Association.Google Scholar
Avault, JW and Allison, R (1965) Experimental biological control of a trematode parasite of bluegill. Experimental Parasitology 17, 296301.CrossRefGoogle ScholarPubMed
Avault, JW and Smitherman, O (1965) Experimental host specificity of Posthodiplostomum minimum. Experimental Parasitology 17, 268270.CrossRefGoogle Scholar
Blasco-Costa, I, Faltynková, A, Georgieva, S, Skirnisson, K, Scholz, T and Kostadinova, A (2014) Fish pathogens near the Arctic circle: molecular, morphological and ecological evidence for unexpected diversity of Diplostomum (Digenea: diplostomidae) in Iceland. International Journal for Parasitology 44, 703715.CrossRefGoogle Scholar
Blouin, MS (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527531.CrossRefGoogle ScholarPubMed
Boone, EC, Laursen, JR, Colombo, RE, Meiners, SJ, Romani, MF and Keeney, DB (2018) Infection patterns and molecular data reveal host and tissue specificity of Posthodiplostomum species in centrarchid hosts. Parasitology 145, 14581468.CrossRefGoogle ScholarPubMed
Bowles, J and McManus, DP (1993) Rapid discrimination of Echinococcus species and strains using a PCR-based method. Molecular Biochemical Parasitology 57, 231239.CrossRefGoogle Scholar
Briosio-Aguilar, PH, Rodríguez-Santiago, MA, López-Garcia, K, García-Varela, M and Pérez-Ponce de León, G (2018) Link between the adult and the metacercaria of Clinostomum heluans Braun, 1899 (Trematoda: Clinostomidae) through DNA sequences, and its phylogenetic position within the genus Clinostomum Leidy,1856. Journal of Parasitology 104, 292296.CrossRefGoogle ScholarPubMed
Bussing, WA (2002) Peces de las aguas continantales de Costa Rica. Editorial Universiaria de Costa Rica, San José, Costa Rica.Google Scholar
Chibwana, FD, Blasco-Costa, I, Georgieva, S, Hosea, KM, Nkwengulila, G, Scholz, T and Kostadinova, A (2013) A first insight into the barcodes for African diplostomids (Digenea: Diplostomidae): Brain parasites in Clarias gariepinus (Siluriformes: Clariidae). Infection Genetic and Evolution 17, 6270.CrossRefGoogle Scholar
Choudhury, A, García-Varela, M and Pérez-Ponce de León, G (2017) Parasites of freshwater fishes and the great American biotic interchange: a bridge too far? Journal of Helminthology 4, 174196.CrossRefGoogle Scholar
Dubois, G (1970) Synopsis des Strigeidae et des Diplostomatidae (Trematoda). Mémoires del Sociéte Neuchâteloise des Sciences Naturelles 10, 259727.Google Scholar
Dubois, G (1988) Quelques Strigeoidea (Trematoda) recoltes au Paraguay parles expeditions du Museum d'Histoire naturelle de Geneve, au cours des annees 1979, 1982 et 1985. Revue Suisse de Zoologie 95, 521532.CrossRefGoogle Scholar
Ferguson, MW (1943) Experimental studies on the fish hosts of Posthodiplostomum minimum (Trematoda: Strigeida). Journal of Parasitology 29, 350353.CrossRefGoogle Scholar
Fernandes, BMM, Justo, MCN, Cárdenas, MQ and Cohen, SC (2015) South American trematode parasites of birds and mammals. Fundção Oswaldo Cruz, Rio de Janeiro, Brasil, p. 544.Google Scholar
Galazzo, DE, Dayanandan, S, Marcogliese, DJ and McLaughlin, JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 30, 22072217.CrossRefGoogle Scholar
García-Varela, M, Sereno-Uribe, AL, Pinacho-Pinacho, CD, Hernández-Cruz, E and Pérez-Ponce de León, G (2016) An integrative taxonomic study reveals new species of Tylodelphys Diesing, 1950 (Digenea: Diplostomidae) in central and northern Mexico. Journal of Helminthology 90, 668679.CrossRefGoogle ScholarPubMed
Georgieva, S, Soldánova, M, Pérez-del-Olmo, A, Dangel, DR, Sitko, J, Sures, B and Kostadinova, A (2013) Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. International Journal for Parasitology 43, 5772.CrossRefGoogle ScholarPubMed
Gibson, DI (1996) Trematoda. In Margolis, L and Kabata, Z (eds), Guide to the Parasite of Fishes of Canada, Part IV. Trematoda. Ottawa, Canada: NRC Research Press, p. 373.Google Scholar
Grizzle, JM and Goldsby, MT Jr (1996) White grub Posthodiplostomum minimum centrarchi metacercariae in the liver of largemouth bass: quantification and effects on health. Journal of Aquatic Animal Health 8, 7074.2.3.CO;2>CrossRefGoogle Scholar
Hoffman, GL (1958) Experimental studies on the cercaria and metacercaria of a strigeoid trematode, Posthodiplostomum minimum. Experimental Parasitology 7, 2350.CrossRefGoogle ScholarPubMed
Hoffman, GL (1999) Parasites of North American Freshwater Fishes, 2nd Edn. Ithaca, New York: Comstock Publishing Associates and Cornell University Press.CrossRefGoogle Scholar
Hunter, GWIII and Hunter, WS (1940) Studies on the development of the metacercaria and the nature of the cyst of Posthodiplostomum minimum (MacCallum 1921) (Trematoda; Strigeata). Transactions of the American Microscopical Society 59, 5262.CrossRefGoogle Scholar
Klak, GE (1940) Neascus infection of blackhead, blunt-nosed, and other forage minnows. Transactions of the American Fisheries Society 69, 273278.CrossRefGoogle Scholar
Kvach, Y, Jurajda, P, Bryjová, A, Trichkova, T, Ribeiro, F, Přikrylová, I and Ondračková, M (2017) European distribution for metacercariae of the North American digenean Posthodiplostomum cf. minimum centrarchi (Strigeiformes: Diplostomidae). Parasitology International 66, 635642.CrossRefGoogle Scholar
Lamothe, R and Pérez-Ponce de León, G (1986) Hallazgo de Posthodiplostomum minimum (MacCallum, 1921) Dubois 1936 (Trematoda: Diplostomatidae) en Egretta thula en México. Anales del Instituto de Biología Universidad Nacional Autónoma de México Serie Zoología 57, 235246.Google Scholar
Lane, B, Spier, T, Wiederholt, J and Meagher, S (2015) Host specificity of a parasitic fluke: is Posthodiplostomum minimum a centrarchid-infecting generalist or specialist? Journal of Parasitology 101, 617.CrossRefGoogle ScholarPubMed
Locke, SA, McLaughlin, JD, Dayanandan, S and Marcogliese, DJ (2010) Diversity and specificity in Diplostomum spp. Metacercariae in freshwater fishes revealed b cytochrome c oxidase I and internal transcribed spacer sequences. International Journal for Parasitology 40, 333343.CrossRefGoogle Scholar
Locke, SA, Al-Nasiri, FS, Caffara, M, Drago, F, Kalbe, M, Lapierre, AR, McLaughlin, JD, Nie, P, Overstreet, RM, Souza, GTR, Takemoto, RM and Marcogliese, DJ (2015) Diversity, specificity and speciation in larval Diplostomidae (Platyhelminthes: Digenea) in the eyes of freshwater fish, as revealed by DNA barcodes. International Journal for Parasitology 45, 841855.10.1016/j.ijpara.2015.07.001CrossRefGoogle ScholarPubMed
López-Hernández, D, Locke, SA, Melo, AL, Rabelo, ÉML and Pinto, HA (2018) Molecular, morphological and experimental assessment of the life cycle of Posthodiplostomum nanum Dubois, 1937 (Trematoda: Diplostomidae) from Brazil, with phylogenetic evidence of the paraphyly of the genus Posthodiplostomum Dubois, 1936. Infection Genetic and Evolution 63, 95103.CrossRefGoogle ScholarPubMed
López-Jiménez, A, Pérez-Ponce de León, G and García-Varela, M (2018) Molecular data reveal high diversity of Uvulifer (Trematoda: Diplostomidae) in Middle America, with the description of a new species. Journal of Helminthology 92, 725739.CrossRefGoogle ScholarPubMed
Lumsden, RD and Zischke, JA (1963) Studies on the trematodes of Louisiana birds. Zeitschrift fur Parasitenkunde 22, 316366.CrossRefGoogle ScholarPubMed
Lunaschi, LI, Cremonte, F and Drago, F (2007) Checklist of digenean parasites of birds from Argentina. Zootaxa 1403, 136.CrossRefGoogle Scholar
MacCallum, GA (1921) Studies in helminthology. Zoopatological 1, 142144.Google Scholar
Miller, JH (1954) Studies on the life history of Posthodiplostomum minimum (MacCallum, 1921). Journal of Parasitology 40, 255270.CrossRefGoogle Scholar
Miller, RR, Minckley, WL and Norris, SM (2005) Freshwater Fishes of Mexico. Chicago, Illinois: University of Chicago Press.Google Scholar
Mitchell, AJ, Smith, CE and Hoffman, GL (1982) Pathogenicity and histopathology of an unusually intense infection of white grubs (Posthodiplostomum m. minimum) in the fathead minnow (Pimephales promelas). Journal of Wildlife Diseases 18, 5157.CrossRefGoogle Scholar
Moszczynska, A, Locke, SA, McLaughlin, JD, 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 helminthes. Molecular Ecology Resource 9, 7582.CrossRefGoogle Scholar
Niewiadomska, K (2002) Family Diplostomidae Poirier, 1886. In Gibson, DI Jones, A, Bray, RA (eds), Keys to the Trematoda, vol. 1. Wallingford: CABI Publishing, pp. 167196.CrossRefGoogle Scholar
Osorio-Sarabia, D, Pérez-Ponce de León, G and García-Marquez, LJ (1986) Helmintos de Peces en Pátzcuaro, Michoacán II: Estudio histopatológico de la lesión causada por metacercarias de Posthodiplostomum minimum (Trematoda: Diplostomatidae) en el hígado de Chirostoma estor. Anales del Instituto de Biología Universidad Nacional Autónoma de México Serie Zoología 57, 247260.Google Scholar
Ostrowski de Núñez, M (1973) Sobre el ciclo biológico de Posthodiplostomum nanum Dubois, 1937 (Trematoda, Diplostomatidae). Physis (rio De Janeiro, Brazil) 32, 121132.Google Scholar
Page, LM and Burr, BM (2011) A Field Guide to Freshwater Fishes of North America North of Mexico. Boston: Houghton Mifflin Harcourt.Google Scholar
Palmieri, JR (1976) Host-parasite relationships and intraspecific variation in Posthodiplostomum minimum (Trematoda: Diplostomatidae). Great Basin Naturalist 36, 334346.Google Scholar
Palmieri, JR (1977 a) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplostomatidae). II. Body measurements and tegument modifications. Great Basin Naturalist 37, 129137.Google Scholar
Palmieri, JR (1977 b) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplotomatidae). III. Organs of attachment. Great Basin Naturalist 37, 375382.Google Scholar
Palmieri, JR (1977 c) Host-induced morphological variations in the strigeoid trematode Posthodiplostomum minimum (Trematoda: Diplostomatidae, IV. Organs of reproduction (ovary and testes), vitelline gland, and egg. Great Basin Naturalist 37, 481488.Google Scholar
Pérez-Ponce de León, G (1992) Sistemática del género Posthodiplostomum Dubois, 1936 y algunos aspectos epizootiológicos de la posthodiplostomiasis en el lago de Pátzcuaro, Michoacán, México (PhD Thesis). Universidad Nacional Autónoma de México.Google Scholar
Pérez-Ponce de León, G (1995) Host-induced morphological variability in adult Posthodiplostomum minimum (Digenea: Neodiplostomidae). Journal of Parasitology 81, 818820.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Choudhury, A (2010) Parasite inventories and DNA-base taxonomy lessons from helminths of freshwater fishes in a megadiverse country. Journal of Parasitology 96, 236244.CrossRefGoogle Scholar
Pérez-Ponce de León, G, García-Prieto, L and Mendoza-Garfias, B (2007) Trematode parasite (Platyhelminthes) of wildlife vertebrates in Mexico. Zootaxa 1534, 1247.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Rosas-Valdez, R, Mendoza-Garfias, B, Aguilar-Aguilar, R, Falcón-Ordaz, J, Garrido-Olvera, L and Pérez-Rodríguez, R (2009) Survey of the endohelminth parasites of freshwater fishes in the upper Mezquital River Basin, Durango State, Mexico. Zootaxa 2164, 120.CrossRefGoogle Scholar
Pérez-Ponce de León, G, Rosas-Valdez, R, Aguilar-Aguilar, R, Mendoza Garfias, B, Mendoza-Palmero, C, García-Prieto, L, Rojas-Sánchez, A, Briosio-Aguilar, R, Pérez-Rodríguez, R and Domínguez-Domínguez, O (2010) Helminth parasites of freshwater fishes, Nazas River basin, northern Mexico. Checklist 6, 2635.CrossRefGoogle Scholar
Pérez-Ponce de León, G, García-Varela, M, Pinacho-Pinacho, CD, Sereno-Uribe, AL and Poulin, R (2016) Species delimitation in trematodes using DNA sequences: middle-American Clinostomum as a case study. Parasitology 143, 17731789.CrossRefGoogle ScholarPubMed
Pérez-Vigueras, I (1955) Contribución al conocimiento de la fauna helmintológica Cubana. Memorias de la Sociedad Cubana de Historia Natural 22, 2171.Google Scholar
Pinacho-Pinacho, CD, García-Varela, M, Hernández-Orts, JS, Mendoza-Palmero, CA, Sereno-Uribe, AL, Martínez-Ramírez, E, Andrade-Gómez, L, López-Jiménez, A, Hernández-Cruz, E and Pérez-Ponce de León, G (2015) Checklist of the helminth parasites of the genus Profundulus Hubbs, 1924 (Cyprinodontiformes, Profundulidae), an endemic family of freshwater fishes in Middle-America. ZooKeys 523, 130.CrossRefGoogle Scholar
Pinto, HA and Melo, AL (2012) Infecção natural de Poecilia reticulata (Actinopterygii: Poeciliidae) por metacercárias na represa da Pampulha, Belo Horizonte, Minas Gerais, Brasil. Boletin Instituto de Pesca 38, 257264.Google Scholar
Pinto, HA, Mati, VLT and Melo, AL (2013) New records and a checklist of trematodes from Butorides striata (Aves: Ardeidae). Revista Mexicana de Biodiversidad 8, 11001110.CrossRefGoogle Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 12531256.CrossRefGoogle ScholarPubMed
Rambaut, A (2012) FigTree v1.4.0. Institute of Evolutionary Biology. University of Edinburgh, UK.Google Scholar
Rietschel, G and Werding, B (1978) Trematodes of birds from Northern Colombia. Zeitschrift fur Parasitenkunde 57, 5782.CrossRefGoogle Scholar
Ritossa, L, Flores, V and Viozzio, G (2013) Life-cycle stages of a Posthodiplostomum species (Digenea:Diplostomidea) from Patagonia, Argentina. Journal of Parasitology 99, 777780.CrossRefGoogle Scholar
Ronquist, F, Teslenko, M, Van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, M and Huelsenbeck, JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539542.CrossRefGoogle ScholarPubMed
Scholz, T and Choudhury, A (2014) Parasites of freshwater fishes in North America: why so neglected? Journal of Parasitology 100, 2645.CrossRefGoogle Scholar
Sereno-Uribe, AL, Andrade Gómez, L, Ostrowski de Nuñez, M, Pérez-Ponce de León, G and García-Varela, M (2019 a) Assessing the taxonomic validity of Austrodiplostomum spp. (Digenea: Diplostomidae) through nuclear and mitochondrial data. Journal of Parasitology 105, 102112.CrossRefGoogle ScholarPubMed
Sereno-Uribe, AL, Andrade-Gómez, L, Pérez-Ponce de León, G and García-Varela, M (2019 b) Exploring the genetic diversity of Tylodelphys (Diesing, 1850) metacercariae in the cranial and body cavities of Mexican freshwater fishes using nuclear and mitochondrial DNA sequences, with the description of a new species. Parasitology Research 118, 203217.CrossRefGoogle ScholarPubMed
Spall, RD and Summerfelt, C (1970) Life cycle of the white grub, Posthodiplostomum minimum (MacCallum 1921: Trematoda, Diplostomatidae), and observations on host-parasite relationships of the metacercaria in fish. A symposium on diseases of fishes and shellfishes, Special Publication number 5, American Fisheries Society, Washington, D.C., pp. 218230.Google Scholar
Stamatakis, A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatic 22, 26882690.CrossRefGoogle ScholarPubMed
Stoyanov, B, Georgieva, S, Pankov, P, Kudlai, O, Kostadinova, A and Georgiev, BB (2017) Morphology and molecules reveal the alien Posthodiplostomum centrarchi Hoffman, 1958 as the third species of Posthodiplostomum Dubois, 1936 (Digenea: Diplostomidae) in Europe. Systematic Parasitology 94, 120.CrossRefGoogle ScholarPubMed
Tamura, K, Stecher, G, Peterson, D, Filipski, A and Kumar, S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 27252729.CrossRefGoogle ScholarPubMed
Thompson, JD, Gibson, TJ, Plewniak, F and Jeanmougin, F (1997) The Clustal windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle ScholarPubMed
Travassos, L, Teixeira de Freitas, JF and Kohn, A (1969) Trematodeos do Brasil. Memorias do Instituto Oswaldo Cruz 67, 8187.Google Scholar
Vidal-Martínez, VM, Aguirre-Macedo, L, Scholz, T, González-Solís, D and Mendoza-Franco, E (2001) Atlas of the Helminth Parasites of Cichlid Fish of Mexico. Praha: Academia, 165 pp.Google Scholar
Supplementary material: File

Pérez-Ponce de León et al. supplementary material

Pérez-Ponce de León et al. supplementary material

Download Pérez-Ponce de León et al. supplementary material(File)
File 35.3 KB