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Infection patterns and molecular data reveal host and tissue specificity of Posthodiplostomum species in centrarchid hosts

Published online by Cambridge University Press:  12 March 2018

Evan C. Boone ,
Jeffrey R. Laursen ,
Robert E. Colombo ,
Scott J. Meiners ,
Michael F. Romani  and
Devon B. Keeney
Evan C. Boone
Affiliation:
Department of Biological Sciences, Eastern Illinois University, Charleston, Illinois 61920, USA
Jeffrey R. Laursen
Affiliation:
Department of Biological Sciences, Eastern Illinois University, Charleston, Illinois 61920, USA
Robert E. Colombo
Affiliation:
Department of Biological Sciences, Eastern Illinois University, Charleston, Illinois 61920, USA
Scott J. Meiners
Affiliation:
Department of Biological Sciences, Eastern Illinois University, Charleston, Illinois 61920, USA
Michael F. Romani
Affiliation:
Department of Biological and Environmental Sciences, Le Moyne College, Syracuse, New York 13214, USA
Devon B. Keeney*
Affiliation:
Department of Biological and Environmental Sciences, Le Moyne College, Syracuse, New York 13214, USA
*
Author for correspondence: Devon B. Keeney, E-mail: keeneydb@lemoyne.edu
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Abstract

Posthodiplostomum minimum utilizes a three-host life cycle with multiple developmental stages. The metacercarial stage, commonly known as ‘white grub’, infects the visceral organs of many freshwater fishes and was historically considered a host generalist due to its limited morphological variation among a wide range of hosts. In this study, infection data and molecular techniques were used to evaluate the host and tissue specificity of Posthodiplostomum metacercariae in centrarchid fishes. Eleven centrarchid species from three genera were collected from the Illinois portion of the Ohio River drainage and necropsied. Posthodiplostomum infection levels differed significantly by host age, host genera and infection locality. Three Posthodiplostomum spp. were identified by DNA sequencing, two of which were relatively common within centrarchid hosts. Both common species were host specialists at the genus level, with one species restricted to Micropterus hosts and the other preferentially infecting Lepomis. Host specificity is likely dictated by physiological compatibility and deviations from Lepomis host specificity may be related to host hybridization. Posthodiplostomum species also differed in their utilization of host tissues. Neither common species displayed strong genetic structure over the scale of this study, likely due to their utilization of bird definitive hosts.

Keywords

COIhost specificityITS1metacercariaePosthodiplostomumtissue specificitywhite grub
Type
Research Article
Information
Parasitology , Volume 145 , Issue 11 , September 2018 , pp. 1458 - 1468
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Copyright
Copyright © Cambridge University Press 2018 

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Footnotes

*

Present address: U. S. Fish and Wildlife Service, Ashland Fish and Wildlife Conservation Office, 2800 Lake Shore Drive East, Ashland, Wisconsin 54806, USA

References

Blasco-Costa, I and Poulin, R (2013) Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology 140, 1316–1322.Google Scholar
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.Google Scholar
Bowles, J and McManus, DP (1993) Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231–240.Google Scholar
Bowles, J, Blair, B and McManus, DP (1995) A molecular phylogeny of the human schistosomes. Molecular Phylogenetics and Evolution 4, 103–109.Google Scholar
Breden, F, Ptacek, MB, Rashed, M, Taphorn, D and Figueiredo, CA (1999) Molecular phylogeny of the live-bearing fish genus Poecilia (Cyprinodontiformes: Poeciliidae). Molecular Phylogenetics and Evolution 12, 95–104.Google Scholar
Bush, AO, Lafferty, KD, Lotz, JM, Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cheng, L, Connor, TR, Sirén, J, Aanensen, DM and Corander, J (2013) Hierarchical and spatially explicit clustering of DNA sequences with BAPS software. Molecular Biology and Evolution 30, 1224–1228.Google Scholar
Chow, S and Takeyama, H (2000) Nuclear and mitochondrial DNA analyses reveal four genetically separated breeding units of the swordfish. Journal of Fish Biology 56, 1087–1098.Google Scholar
Corander, J, Waldmann, P and Sillanpää, MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163, 367–374.Google Scholar
De León, GP and Nadler, SA (2010) What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453–464.Google Scholar
De León, GP-P, 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, 1773–1789.Google Scholar
Dupont, F and Crivelli, AJ (1988) Do parasites confer a disadvantage to hybrids? A case study of Alburnus alburnus × Rutilus rubilio, a natural hybrid of Lake Mikri Prespa, northern Greece. Oecologia 75, 587–592.Google Scholar
ESRI (2015) ArcGIS 10.3. Redlands, California: Environmental System Research Institute, Inc.Google 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.Google Scholar
Godbout, JD, Aday, DD, Rice, JA, Bangs, MR and Quattro, JM (2009) Morphological models for identifying largemouth bass, spotted bass, and largemouth bass x spotted bass hybrids. North American Journal of Fisheries Management 29, 1425–1437.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, 70–74.Google Scholar
Herrmann, KK and Poulin, R (2011) Encystment site affects the reproductive strategy of a progenetic trematode in its fish intermediate host: is host spawning an exit for parasite eggs? Parasitology 138, 1183–1192.Google Scholar
Hoberg, EP and Brooks, DR (2008) A macroevolutionary mosaic: episodic host-switching, geographical colonization and diversification in complex host-parasite systems. Journal of Biogeography 35, 1533–1550.Google Scholar
Hoffman, GL (1958) Experimental studies on the cercaria and metacercaria of a strigeoid trematode, Posthodiplostomum minimum. Experimental Parasitology 7, 23–50.Google Scholar
Hoffman, GL (1999) Parasites of North American Freshwater Fishes. Ithaca, New York: Cornell University Press, 539p.Google Scholar
Ivanova, NV, Zemlak, TS, Hanner, RH and Hebert, PDN (2007) Universal primer cocktails for fish DNA barcoding. Molecular Ecology Notes 7, 544–548.Google Scholar
Keeney, DB, Waters, JM and Poulin, R (2007) Clonal diversity of the marine trematode Maritrema novaezealandensis within intermediate hosts: the molecular ecology of parasite life cycles. Molecular Ecology 16, 431–439.Google Scholar
Klak, G (1940) Neascus infestation of black-head, blunt-nosed, and other forage minnows. Transactions of the American Fisheries Society 69, 273–278.Google 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.Google 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, 635–642.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, 6–17.Google Scholar
Le Brun, N, Renaud, F, Berrebi, P and Lambert, A (1992) Hybrid zones and host-parasite relationships: effect on the evolution of parasitic specificity. Evolution 46, 56–61.Google Scholar
Locke, SA, McLaughlin, JD and Marcogliese, DJ (2010) DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River, Canada. Molecular Ecology 19, 2813–2827.Google 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, 841–855.Google Scholar
Meade, TG and Bedinger, CA (1967) Posthodiplostomum minimum (Trematoda: Diplostomidae) in fishes of Madison County, eastern Texas. Southwestern Naturalist 12, 334–335.Google Scholar
Mladineo, I, Bott, NJ, Nowak, BF and Block, BA (2010) Multilocus phylogenetic analyses reveal that habitat selection drives the speciation of Didymozoidae (Digenea) parasitizing Pacific and Atlantic bluefin tunas. Parasitology 137, 1013–1025.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(Suppl. 1), 75–82.Google Scholar
Near, TJ, Bolnick, DI and Wainwright, PC (2005) Fossil calibrations and molecular divergence time estimates in centrarchid fishes (Teleostei: Centrarchidae). Evolution 59, 1768–1782.Google Scholar
Perkins, SL, Martinsen, ES and Falk, BG (2011) Do molecules matter more than morphology? Promises and pitfalls in parasites. Parasitology 138, 1664–1674.Google Scholar
Pflieger, WL (1997) The Fishes of Missouri. Jefferson City, Missouri: Missouri Department of Conservation, 372p.Google Scholar
Poulin, R (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241–244.Google Scholar
Poulin, R, Krasnov, BR and Mouillot, D (2011) Host specificity in phylogenetic and geographic space. Trends in Parasitology 27, 355–361.Google Scholar
Pracheil, BM and Muzzall, PM (2010) Population dynamics of larval trematodes in juvenile bluegills from Three Lakes II, Michigan, and the potential for overwinter parasite-induced host mortality. Transactions of the American Fisheries Society 139, 652–659.Google Scholar
Presa, P, Pardo, BG, Martínez, P and Bernatchez, L (2002) Phylogeographic congruence between mtDNA and rDNA ITS markers in brown trout. Molecular Biology and Evolution 19, 2161–2175.Google Scholar
Quist, MC, Pegg, MA and DeVries, DR (2012) Age and growth. In Zale, AV, Parrish, DL and Sutton, TM (eds). Fisheries Techniques, 3rd edn. Bethesda, Maryland: American Fisheries Society, pp. 677–731.Google Scholar
R Development Core Team (ed.) (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org.Google Scholar
Rambaut, A (2009) FigTree v1.3.1. Available at http://tree.bio.ed.ac.uk/.Google Scholar
Rauch, G, Kalbe, M and Reusch, TBH (2005) How a complex life cycle can improve a parasite's sex life. Journal of Evolutionary Biology 18, 1069–1075.Google Scholar
Ronquist, F, Teslenko, M, van der Mark, P, Ayres, DL, Darling, A, Höhna, S, Larget, B, Liu, L, Suchard, MA and Huelsenbeck, JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.Google Scholar
Šimková, A, Davidova, M, Papousek, I and Vetesnik, L (2013) Does interspecies hybridization affect the host specificity of parasites in cyprinid fish? Parasites and Vectors 6, 95.Google Scholar
Soldánová, M, Georgieva, S, Roháčová, J, Knudsen, R, Kuhn, JA, Henriksen, EH, Siwertsson, A, Shaw, JC, Kuris, AM, Amundsen, PA, Scholz, T, Lafferty, KD and Kostadinova, A (2017) Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. International Journal for Parasitology 47, 327–345.Google Scholar
Spall, RD and Summerfelt, RC (1969) Host-parasite relations of certain endoparasitic helminths of the channel catfish and white crappie in an Oklahoma reservoir. Bulletin of the Wildlife Disease Association 5, 48–67.Google Scholar
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, 1–20.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.Google 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, 839–846.Google Scholar
Walsh, PS, Metzger, DA and Higuchi, R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. BioTechniques 10, 506–513.Google Scholar
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