[en] Monogeneans are highly diverse fish ectoparasites with a direct life cycle, widely distributed, and are known to generally display strict host specificity. Factors related to the hosts and the parasite have been suggested to explain this high specificity. Monogeneans have also been observed to colonise fish species not in their natural host range under experimental conditions. We developed a specific metabarcoding protocol and applied it on the Sparidae-Lamellodiscus host-parasite system, to assess parasite diversity on skin and gills of several sparid host species. We first demonstrated that the use of a metabarcoding approach provided a better understanding of the diversity of monogeneans associated with teleost skin and gills than traditional approaches based on morphological identification. We identified a high diversity of both expected and unexpected (never observed on this host species) Lamellodiscus spp. on each host species and on skin and gills. No significant difference in parasite diversity was found between skin and gills. These results suggest that the establishment of the observed host specificity in monogeneans relies on multiple levels of regulation, involving the survival capacity of the larvae and host recognition mechanisms.
Adamson, M., Caira, J., Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:S1 (1994), S85–S95.
Aivelo, T., Harris, K., Cadle, J., Wright, P., Exploring non-invasive sampling of parasites by metabarcoding gastrointestinal nematodes in Madagascar frog species. Basic Appl. Herpetol. 32 (2018), 29–40.
Aivelo, T., Medlar, A., Opportunities and challenges in metabarcoding approaches for helminth community identification in wild mammals. Parasitology 145:5 (2018), 608–621.
Altschul, S., Gish, W., Miller, W., Myers, E., Lipman, D., Basic local alignment search tool. J. Mol. Biol. 215:3 (1990), 403–410.
Amine F., Euzet L., Kechemir-Issad N., 2006. Description de deux nouvelles espèces de Lamellodiscus Johnston and Tiegs, 1922 (Monogenea: Diplectanidae) du groupe morphologique ‘ignoratus’, parasites de Diplodus sargus et D. vulgaris (Teleostei: Sparidae). Syst. Parasitol. 64(1), 37-45.
Amine F., Euzet L., Kechemir-Issad N., 2007. Lamellodiscus theroni sp. nov. (Monogenea, Diplectanidae), a gill parasite from Diplodus puntazzo (Teleostei, Sparidae) from the Mediterranean Sea. Acta Parasitol. 52(4), 305-309.
Bakke, T., Jansen, P., Hansen, L., Experimental transmission of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes, Monogenea) from the Atlantic salmon (Salmo salar) to the European eel (Anguilla anguilla). Can. J. Zool. 69:3 (1991), 733–737.
Barnes, M., Turner, C., Jerde, C., Renshaw, M., Chadderton, W., Lodge, D., Environmental conditions influence eDNA persistence in aquatic systems. Environ. Sci. Technol. 48:3 (2014), 1819–1827.
Barnes, M., Turner, C., The ecology of environmental DNA and implications for conservation genetics. Genet. Conserv. Genet. 17:1 (2016), 1–17.
Bass, D., Stentiford, G., Littlewood, D., Hartikainen, H., Diverse applications of environmental DNA methods in parasitology. Trends Parasitol. 31:10 (2015), 499–513.
Bittleston, L., Baker, C., Strominger, L., Pringle, A., Pierce, N., Metabarcoding as a tool for investigating arthropod diversity in Nepenthes pitcher plants. Austral. Ecol. 41:2 (2016), 120–132.
Boudaya, L., Neifar, L., Euzet, L., Diplectanid parasites of Lithognathus mormyrus (L.) (Teleostei: Sparidae) from the Mediterranean Sea, with the description of Lamellodiscus flagellatus n. sp. (Monogenea: Diplectanidae). Syst. Parasitol. 74:2 (2009), 149–159.
Buchmann, K., Immune mechanisms in fish skin against monogeneans – A model. Folia Parasitol. 46:1 (1999), 1–9.
Buchmann, K., Lindenstrøm, T., Interactions between monogenean parasites and their fish hosts. Int. J. Parasitol. 32:3 (2002), 309–319.
Buchmann K., Bresciani J., 2006. Monogenea (Phylum Platyhelminthes). In: Woo P. (Ed), Fish diseases and disorders: protozoan and metazoan infection, Volume 1. CABI, Wallingford, Oxfordshire, UK, pp. 297-344.
Bush, A., Fernández, J., Esch, G., Seed, J., Parasitism: The diversity and ecology of animal parasites. 2001, Cambridge University Press, Cambridge, UK.
Callahan, B., McMurdie, P., Holmes, S., Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11:12 (2017), 2639–2643.
Caporaso, J., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F., Costello, E., Fierer, N., Gonzalez, P.A., Goodrich, J., Gordon, J., Huttley, G., Kelley, S., Knights, D., Koenig, J., Ley, R., Lozupone, C., McDonald, D., Muegge, B., Pirrung, M., Reeder, J., Sevinsky, J., Turnbaugh, P., Walters, W., Widmann, J., Yatsunenko, T., Zaneveld, J., Knight, R., QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:5 (2010), 335–336.
Chiba, S., Iwatsuki, Y., Yoshino, T., Hanzawa, N., Comprehensive phylogeny of the family Sparidae (Perciformes: Teleostei) inferred from mitochondrial gene analyses. Genes Genet. Syst. 84:2 (2009), 153–170.
Chisholm, L., Whittington, I., Morphology and development of the haptors among the Monocotylidae (Monogenea). Hydrobiologia 383 (1998), 251–261.
Clerissi, C., Brunet, S., Vidal-Dupiol, J., Adjeroud, M., Lepage, P., Guillou, L., Escoubas, J.-M., Toulza, E., Protists within corals: The hidden diversity. Front. Microbiol., 9, 2018, 2043.
Cowart, D.A., Pinheiro, M., Mouchel, O., Maguer, M., Grall, J., Miné, J., Arnaud-Haond, S., Mazzuca, S., Metabarcoding is powerful yet still blind: A comparative analysis of morphological and molecular surveys of seagrass communities. PLoS One, 10(2), 2015.
Dejean, T., Valentini, A., Duparc, A., Pellier-Cuit, S., Pompanon, F., Taberlet, P., Miaud, C., Gilbert, J.A., Persistence of environmental DNA in freshwater ecosystems. PLoS One, 6(8), 2011.
Desdevises, Y., Jovelin, R., Jousson, O., Morand, S., Comparison of ribosomal DNA sequences of Lamellodiscus spp. (Monogenea, Diplectanidae) parasitising Pagellus (Sparidae, Teleostei) in the North Mediterranean Sea: species divergence and coevolutionary interactions. Int. J. Parasitol. 30:6 (2000), 741–746.
Desdevises, Y., The phylogenetic position of Furnestinia echeneis (Monogenea, Diplectanidae) based on molecular data: A case of morphological adaptation?. Int. J. Parasitol. 31:2 (2001), 205–208.
Desdevises, Y., Morand, S., Legendre, P., Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea). Biol. J. Linn. Soc. 77:4 (2002), 431–443.
Diamanka, A., Boudaya, L., Toguebaye, B., Pariselle, A., Lamellodiscus euzeti n. sp. (Monogenea: Diplectanidae), a parasite from Dentex canariensis and D. gibbosus (Teleostei: Sparidae) in the Atlantic Ocean and Mediterranean Sea. Parasite 18:2 (2011), 145–150.
Du Preez, L., Kok, D., Supporting experimental evidence of host specificity among southern African polystomes (Polystomatidae: Monogenea). Parasitol. Res. 83:6 (1997), 558–562.
Ernst, I., Whittington, I., Corneillie, S., Talbot, C., Monogenean parasites in sea-cage aquaculture. Austasia Aquacult. 16:1 (2002), 46–48.
Euzet, L., Oliver, G., Diplectanidae (monogenea) des téléostéens de la méditerranée occidentale. III. Quelques Lamellodiscus Jonhston et Tiegs, 1922, parasites de poissons du genre Diplodus (Sparidae). Ann. Parasitol. Hum. Comp. 41:6 (1966), 573–598.
Euzet, L., Oliver, G., Diplectanidae (Monogenea) de Téléostéens de la Méditerranée occidentale: IV. Quelques Lamellodiscus Johnston et Tiegs, 1922, parasites de Poissons du genre Pagellus Cuvier, 1829 (Sparidae). Ann. Parasitol. Hum. Comp. 42:4 (1967), 407–425.
Euzet, L., Diplectanidae (Monogenea) parasites de poissons des Iles Kerkennah (Tunisie). Arch. Inst. Pasteur Tunis. 61:4 (1984), 463–474.
Flaherty, B., Talundzic, E., Barratt, J., Kines, K., Olsen, C., Lane, M., Sheth, M., Bradbury, R., Restriction enzyme digestion of host DNA enhances universal detection of parasitic pathogens in blood via targeted amplicon deep sequencing. Microbiome., 6(1), 2018, 164.
Fouhy, F., Clooney, A., Stanton, C., Claesson, M., Cotter, P., 16S rRNA gene sequencing of mock microbial populations – impact of DNA extraction method, primer choice and sequencing platform. BMC Microbiol., 16(1), 2016, 123.
Hall, M., Beiko, R., 16S rRNA gene analysis with QIIME2. Methods Mol. Biol. 1849 (2018), 113–129.
Humphery-Smith, I., The evolution of phylogenetic specificity among parasitic organisms. Parasitol. Today. 5:12 (1989), 385–387.
Huver, J., Koprivnikar, J., Johnson, P., Whyard, S., Development and application of an eDNA method to detect and quantify a pathogenic parasite in aquatic ecosystems. Ecol. Appl. 25:4 (2015), 991–1002.
Igarashi, K., Matsunaga, R., Hirakawa, S., Hosoya, S., Suetake, H., Kikuchi, K., Suzuki, Y., Nakamura, O., Miyadai, T., Tasumi, S., Tsutsui, S., Mucosal IgM antibody with d-mannose affinity in fugu Takifugu rubripes is utilized by a monogenean parasite Heterobothrium okamotoi for host recognition. J. Immunol. 198:10 (2017), 4107–4114.
Ings, T., Montoya, J., Bascompte, J., Blüthgen, N., Brown, L., Dormann, C., Edwards, F., Figueroa, D., Jacob, U., Jones, J., Lauridsen, R., Ledger, M., Lewis, H., Olesen, J., van Veen, F., Warren, P., Guy, W.G., Ecological networks - Beyond food webs. J. Anim. Ecol. 78:1 (2009), 253–269.
Ives, A., Carpenter, S., Stability and diversity of ecosystems. Science 317:5834 (2007), 58–62.
Jorge, F., Carretero, M., Roca, V., Poulin, R., Perera, A., What you get is what they have? Detectability of intestinal parasites in reptiles using faeces. Parasitol. Res. 112:12 (2013), 4001–4007.
Kaci-Chaouch, T., Verneau, O., Desdevises, Y., Host specificity is linked to intraspecific variability in the genus Lamellodiscus (Monogenea). Parasitology 135:5 (2008), 607–616.
Kearn, G.C., Experiments on host-finding and host specificity in the monogenean skin parasite Entobdella soleae. Parasitology 57:3 (1967), 585–605.
Kearn, G., An endogenous circadian hatching rhythm in the monogenean skin parasite Entobdella soleae, and its relationship to the activity rhythm of the host (Solea solea). Parasitology 66:1 (1973), 101–122.
Kearn, G., The effects of fish skin mucus on hatching in the monogenean parasite Entobdella soleae from the skin of the common sole, Solea solea. Parasitology 68:2 (1974), 173–188.
Kearn, G., Macdonald, S., The chemical nature of host hatching factors in the monogenean skin parasites Entobdella soleae and Acanthocotyle lobianchi. Int. J. Parasitol. 6:6 (1976), 457–466.
Kearn, G., Light and gravity responses of the oncomiracidium of Entobdella soleae and their role in host location. Parasitology 81:1 (1980), 71–89.
Kearn, G., Observations on egg production in the monogenean Entobdella soleae. Int. J. Parasitol. 15:2 (1985), 187–194.
Lafferty, K., Allesina, S., Arim, M., Briggs, C., De Leo, G., Dobson, A., Dunne, J., Johnson, P., Kuris, A., Marcogliese, D., Martinez, N., Memmott, J., Marquet, P., McLaughlin, J., Mordecai, E., Pascual, M., Poulin, R., Thieltges, D., Parasites in food webs: The ultimate missing links. Ecol. Lett. 11:6 (2008), 533–546.
Le Brun, N., Renaud, F., Lambert, A., The genus Diplozoon (Monogenea, Polyopisthocotylea) in southern France: speciation and specificity. Int. J. Parasitol. 18 (1988), 395–400.
Leray, M., Agudelo, N., Mills, S.C., Meyer, C.P., Schierwater, B., Effectiveness of annealing blocking primers versus restriction enzymes for characterization of generalist diets: unexpected prey revealed in the gut contents of two coral reef fish species. PLoS One, 8(4), 2013.
Leung, T., Donald, K., Keeney, D., Koehler, A., Peoples, R., Poulin, R., Trematode parasites of Otago Harbour (New Zealand) soft-sediment intertidal ecosystems: Life cycles, ecological roles and DNA barcodes. N. Z. J. Mar. Freshwater Res. 43:4 (2009), 857–865.
Littlewood D., Olson P., 2001. Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood D. and Bray R. (Eds), Interrelationships of the Platyhelminthes, Taylor & Francis, London, UK pp. 262-278.
Liu, C., Qi, R., Jiang, J., Zhang, M., Wang, J., Development of a blocking primer to inhibit the PCR amplification of the 18S rDNA sequences of Litopenaeus vannamei and its efficacy in Crassostrea hongkongensis. Front. Microbiol., 10, 2019, 830.
Llewellyn, J., Larvae and larval development of monogeneans. Adv. Parasitol. 1:C (1963), 287–326.
Lott, M., Hose, G., Power, M., Parasitic nematode communities of the red kangaroo, Macropus rufus: richness and structuring in captive systems. Parasitol. Res. 114:8 (2015), 2925–2932.
Macdonald, S., Jones, A., Egg-laying and hatching rhythms in the monogenean Diplozoon homoion gracile from the southern barbel (Barbus meridionalis). J. Helminthol. 52:1 (1978), 23–28.
Matsui, S., Goto, T., Tsubouchi, Y., Hirakawa, S., Suetake, H., Miyadai, T., Nakamura, O., Tasumi, S., Tsutsui, S., D-mannose-specific Immunoglobulin M in Grass Puffer (Takifugu niphobles), a Nonhost Fish of a Monogenean Ectoparasite Heterobothrium okamotoi, Can Act as a Trigger for its Parasitism. J. Parasitol. 106:2 (2020), 276–282.
Mladineo, I., Maršić-Lučić, J., Host Switch of Lamellodiscus elegans (Monogenea: Monopisthocotylea) and Sparicotyle chrysophrii (Monogenea: Polyopisthocotylea) between Cage-reared Sparids. Vet. Res. Comm. 31:2 (2007), 153–160.
Ohashi, H., Umeda, N., Hirazawa, N., Ozaki, Y., Miura, C., Miura, T., Purification and identification of a glycoprotein that induces the attachment of oncomiracidia of Neobenedenia girellae (Monogenea, Capsalidae). Int. J. Parasitol. 37:13 (2007), 1483–1490.
Oliver, G., Recherches sur les Diplectanidae (Monogenea) parasites de Téléostéens du Golfe du Lion. II. Lamellodiscinae nov. sub. fam. Vie Milieu 19 (1968), 95–138.
Oliver, G., Lamellodiscus obeliae n. sp. une nouvelle espèce de Diplectanidae (Monogenea, Monopisthocotylea) parasite de Pagellus centrodontus (Delaroche, 1809) (Pisces, Sparidae). Z. F. Parasitenkunde 41 (1973), 103–108.
Oliver G., 1974. Nouveaux aspects du parasitisme des Diplectanidae Bychowsky, 1957 (Monogenea, Monopisthocotylea) chez les Téléostéens Perciformes des côtes de France. C. R. Acad. Sci, Paris. 279(10), 803-805.
Öztürk, T., Özer, A., Monogenean fish parasites, their host preferences and seasonal distributions in the lower Kizigrmak Delta (Turkey). Turk. J. Fish. Aquat. Sci. 14:2 (2014), 367–378.
Pedersen, A., Fenton, A., Emphasizing the ecology in parasite community ecology. Trends Ecol. Evol. 22:3 (2007), 133–139.
Pilliod, D.S., Goldberg, C.S., Arkle, R.S., Waits, L.P., Richardson, J., Estimating occupancy and abundance of stream amphibians using environmental DNA from filtered water samples. Can. J. Fish. Aquat. Sci. 70:8 (2013), 1123–1130.
Poisot, T., Verneau, O., Desdevises, Y., Steinke, D., Morphological and molecular evolution are not linked in Lamellodiscus (Plathyhelminthes, Monogenea). PLoS One, 6(10), 2011.
Poulin, R., Determinants of host-specificity in parasites of freshwater fishes. Int. J. Parasitol. 22:6 (1992), 753–758.
Poulin, R., Evolutionary Ecology of Parasites: From Individuals to Communities. 1998, Chapman and Hall, New York, NY.
Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., Peplies, J., Glöckner, F.O., The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 41:D1 (2013), D590–D596.
Reed, P., Francis-Floyd, R., Klinger, R., Petty, D., Monogenean Parasites of Fish. 2012, Institute of Food and Agricultural Sciences, University of Florida, FA28.
Roubal, F., Attachment of eggs by Lamellodiscus acanthopagri (Monogenea, Diplectanidae) to the gills of Acanthopagrus australis (Pisces, Sparidae), with evidence for auto-infection and postsettlement migration. Can. J. Zool. 72:1 (1994), 87–95.
Sanchez-García, N., Raga, J., Montero, F.E., Morphological and attachment changes of Lamellodiscus theroni (Monogenea: Diplectanidae) during its post-larval development on fish. Folia Parasitol., 62(2015), 2015, 026.
Sasal, P., Desdevises, Y., Morand, S., Host-specialization and species diversity in fish parasites: Phylogenetic conservatism?. Ecography 21:6 (1998), 639–643.
Sasal, P., Morand, S., Comparative analysis: a tool for studying monogenean ecology and evolution. Int. J. Parasitol. 28:10 (1998), 1637–1644.
Sasal, P., Trouvé, S., Müller-Graf, C., Morand, S., Specificity and host predictability: A comparative analysis among monogenean parasites of fish. J. Anim. Ecol. 68:3 (1999), 437–444.
Sasal, P., Desdevises, Y., Durieux, E., Lenfant, P., Romans, P., Parasites in marine protected areas: Success and specificity of monogeneans. J. Fish Biol. 64:2 (2004), 370–379.
Scheifler, M., Ruiz-Rodríguez, M., Sanchez-Brosseau, S., Magnanou, E., Suzuki, M.T., West, N., Duperron, S., Desdevises, Y., Duplouy, A.M.R., Characterization of ecto- and endoparasite communities of wild Mediterranean teleosts by a metabarcoding approach. PLoS One, 14(9), 2019.
Sengupta, M., Hellström, M., Kariuki, H., Olsen, A., Thomsen, P., Mejer, H., Willerslev, E., Mwanje, M., Madsen, H., Kristensen, T., Stensgaard, A.-S., Vennervald, B., Environmental DNA for improved detection and environmental surveillance of schistosomiasis. Proc. Natl. Acad. Sci. U.S.A. 116:18 (2019), 8931–8940.
Simková, A., Verneau, O., Gelnar, M., Morand, S., Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish. Evolution 60:5 (2006), 1023–1037.
Tanaka, R., Hino, A., Tsai, I.J., Palomares-Rius, J.E., Yoshida, A., Ogura, Y., Hayashi, T., Maruyama, H., Kikuchi, T., Gobert, G.N., Assessment of helminth biodiversity in wild rats using 18S rDNA-based metagenomics. PLoS One, 9(10), 2014, e110769.
Tinsley, R., Owen, R., Studies on Biology of Protopolystoma-Xenopodis (Monogenoidea) – Oncomiracidium and Life-Cycle. Parasitology 71:3 (1975), 445–463.
Tinsley, R., Oviposition, hatching and the oncomiracidium of Eupolystoma anterorchis (Monogenoidea). Parasitology 77:2 (1978), 121–132.
Tinsley, R., Ovoviviparity in platyhelminth life-cycles. Parasitology 86:4 (1983), 161–196.
Vestheim, H., Jarman, S., Blocking primers to enhance PCR amplification of rare sequences in mixed samples – A case study on prey DNA in Antarctic krill stomachs. Front. Zool., 5(1), 2008, 12.
Whittington, I., Kearn, G., Rhythmical hatching and oncomiracidial behaviour in the hexabothriid monogenean Rajonchocotyle emarginata from the gills of Raja spp. J. Mar. Biolog. Assoc. U.K. 66:1 (1986), 93–111.
Whittington, I., Kearn, G., Rapid hatching of mechanically-distubed eggs of the monogenean gill parasite Diclidophora luscae, with observations on sedimentation of egg bundles. Int. J. Parasitol. 18:6 (1988), 847–852.
Whittington, I., Kearn, C., Rapid hatching induced by light intensity reduction in the polypisthocotylean monogenean Plectanocotyle gurnardi from the gills of Gurnards triglidae with observations on the anatomy and behaviour of the oncomiracidium. J. Mar. Biolog. Assoc. U.K. 69 (1989), 609–624.
Whittington, I., Cribb, B., Hamwood, T., Halliday, J., Host-specificity of monogenean (platyhelminth) parasites: A role for anterior adhesive areas?. Int. J. Parasitol. 30:3 (2000), 305–320.
Whittington, I., The Capsalidae (Monogenea: Monopisthocotylea): a review of diversity, classification and phylogeny with a note about species complexes. Folia Parasitol. 51:2–3 (2004), 109–122.
Whittington, I., Kearn, G., Hatching strategies in monogenean (Platyhelminth) parasites that facilitate host infection. Integr. Comp. Biol. 51:1 (2011), 91–99.
Whittington, I., Woo, P., Buchmann, K., Benedenia seriolae and Neobenedenia species. Woo, P., Buchmann, K., (eds.) Fish parasites: pathobiology and protection, 2012, CABI, Wallingford, Oxfordshire, UK, 225–244.
Yilmaz, P., Parfrey, L., Yarza, P., Gerken, J., Pruesse, E., Quast, C., Schweer, T., Peplies, J., Ludwig, W., Glöckner, F., The SILVA and “all-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 42:Database issue (2014), D643–D648.
Yoshinaga, T., Nagakura, T., Ogawa, K., Fukuda, Y., Wakabayashi, H., Attachment-inducing capacity of fish skin epithelial extracts on oncomiracidia of Benedenia seriolae (Monogenea: Capsalidae). Int. J. Parasitol. 32:3 (2002), 381–384.