Phenotypic polymorphism is a commonly observed phenomenon in nature, but extremely rare in free-living stages of parasites. We describe a unique case of somatic polymorphism in conspecific cercariae of the bird schistosome Trichobilharzia sp. "peregra", in which two morphs, conspicuously different in their size, were released from a single Radix balthica snail. A detailed morphometric analysis that included multiple morphological parameters taken from 105 live and formalin-fixed cercariae isolated from several naturally infected snails provided reliable evidence for a division of all cercariae into two size groups that contained either large or small individuals. Large morph (total body length of 1368 and 1339 μm for live and formalin-fixed samples, respectively) differed significantly nearly in all morphological characteristics compared to small cercariae (total body length of 976 and 898 μm for live and formalin samples, respectively), regardless of the fixation method. Furthermore, we observed that small individuals represent the normal/commonly occurring phenotype in snail populations. The probable causes and consequences of generating an alternative, much larger phenotype in the parasite infrapopulation are discussed in the context of transmission ecology as possible benefits and disadvantages facilitating or preventing the successful completion of the life cycle.

Department of Arctic and Marine Biology Faculty of Biosciences Fisheries and Economics UiT The Arctic University of Norway N9037 Tromsø Norway

Department of Parasitology Faculty of Science University of South Bohemia in České Budějovice 370 05 České Budějovice Czech Republic

Institute of Parasitology Biology Centre of the Czech Academy of Sciences 370 05 České Budějovice Czech Republic

Zobrazit více v PubMed

Leimar O. The evolution of phenotypic polymorphism: Randomized strategies versus evolutionary branching. Am. Nat. 2005;165:669–681. doi: 10.1086/429566. PubMed DOI

West-Eberhard M.J. Phenotypic Plasticity. In: Jørgensen S.E., Fath B.D., editors. Encyclopedia of Ecology. Elsevier; Amsterdam, The Netherlands: 2008. pp. 2701–2707.

Fox R.J., Donelson J.M., Schunter C., Ravasi T., Gaitán-Espitia. J.D. Beyond buying time: The role of plasticity in phenotypic adaptation to rapid environmental change. Phil. Trans. R. Soc. B. 2019;374:20180174. doi: 10.1098/rstb.2018.0174. PubMed DOI PMC

Jamie G.A., Meier J.I. The persistence of polymorphisms across species radiations. Trends Ecol. Evol. 2020;35:795–808. doi: 10.1016/j.tree.2020.04.007. PubMed DOI

Ford E.B. Genetic Polymorphism. Faber & Faber; London, UK: 1965. p. 101.

Fusco G., Minelli A. Phenotypic plasticity in development and evolution: Facts and concepts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2010;365:547–556. doi: 10.1098/rstb.2009.0267. PubMed DOI PMC

Pigliucci M., Murren C.J., Schlichting C.D. Phenotypic plasticity and evolution by genetic assimilation. J. Exp. Biol. 2006;209:2362–2367. doi: 10.1242/jeb.02070. PubMed DOI

Wills B.D., Powell S., Rivera M.D., Suarez A.V. Correlates and consequences of worker polymorphism in ants. Annu. Rev. Entomol. 2018;63:575–598. doi: 10.1146/annurev-ento-020117-043357. PubMed DOI

Frances P., Burnie D. Bird: The Definitive Visual Guide. Dorling Kindersley Inc.; London, UK: 2007. p. 512.

Poulin R. The evolution of life history strategies in parasitic animals. Adv. Parasitol. 1996;37:107–134. doi: 10.1016/S0065-308X(08)60220-1. PubMed DOI

Maizels R.M., Kurniawan-Atmadja A. Variation and polymorphism in helminth parasites. Parasitology. 2002;125:25–37. doi: 10.1017/S0031182002001890. PubMed DOI

Thompson C.K., Botero A., Wayne A.F., Godfrey S.S., Lymbery A.J., Thompson R.A. Morphological polymorphism of Trypanosoma copemani and description of the genetically diverse T. vegrandis sp. nov. from the critically endangered Australian potoroid, the brush-tailed bettong (Bettongia penicillata (Gray, 1837)) Parasit. Vectors. 2013;6:121. doi: 10.1186/1756-3305-6-121. PubMed DOI PMC

Hanzelová V., Oros M., Barčák D., Miklisová D., Kirin D., Scholz T. Morphological polymorphism in tapeworms: Redescription of Caryophyllaeus laticeps (Pallas, 1781) (Cestoda: Caryophyllidea) and characterisation of its morphotypes from different fish hosts. Syst. Parasitol. 2015;90:177–190. doi: 10.1007/s11230-014-9536-x. PubMed DOI

Guo Q., Huang M., Liu Y., Zhang X., Gu Z. Morphological plasticity in Myxobolus Bütschli, 1882: A taxonomic dilemma case and renaming of a parasite species of the common carp. Parasit. Vectors. 2018;11:399. doi: 10.1186/s13071-018-2943-0. PubMed DOI PMC

Dobson A., Lafferty K.D., Kuris A.M., Hechinger R.F., Jetz W. Homage to Linnaeus: How many parasites? How many hosts? Proc. Natl. Acad. Sci. USA. 2008;105:11482–11489. doi: 10.1073/pnas.0803232105. PubMed DOI PMC

Poulin R. Parasite biodiversity revisited: Frontiers and constraints. Int. J. Parasitol. 2014;44:581–589. doi: 10.1016/j.ijpara.2014.02.003. PubMed DOI

Pandian T.J. Reproduction and Development in Platyhelminthes. CRC Press; Boca Raton, FL, USA: 2020. p. 320. DOI

Galaktionov K.V., Dobrovolskij A. The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Kluwer Academic Publishers; Dordrecht, The Netherlands: 2003. p. 592.

Soldánová M., Selbach C., Kalbe M., Kostadinova A., Sures B. Swimmer’s itch: Etiology, impact, and risk factors in Europe. Trends Parasitol. 2013;29:65–74. doi: 10.1016/j.pt.2012.12.002. PubMed DOI

Jamieson B.G.M. Schistosoma: Biology, Pathology and Control. CRC Press; Boca Raton, FL, USA: 2017. p. 523. DOI

Kock S. Investigations of intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae) Parasitology. 2001;123:67–70. doi: 10.1017/S0031182001008101. PubMed DOI

Poulin R. Morphological diversification in different trematode lineages: Body size, host type, or time? Parasitology. 2009;136:85–92. doi: 10.1017/S0031182008005179. PubMed DOI

Hechinger R.F., Wood A.C., Kuris A.M. Social organization in a flatworm: Trematode parasites form soldier and reproductive castes. Proc. R. Soc. B. 2011;278:656–665. doi: 10.1098/rspb.2010.1753. PubMed DOI PMC

Garcia-Vedrenne A.E., Quintana A.C., DeRogatis A.M., Martyn K., Kuris A.M., Hechinger R.F. Social organization in parasitic flatworms—four additional echinostomoid trematodes have a soldier caste and one does not. J. Parasitol. 2016;102:11–20. doi: 10.1645/15-853. PubMed DOI

Poulin R., Kamiya T., Lagrue C. Evolution, phylogenetic distribution and functional ecology of division of labour in trematodes. Parasit. Vectors. 2019;12:1–10. doi: 10.1186/s13071-018-3241-6. PubMed DOI PMC

Seppälä O., Karvonen A., Valtonen E.T. Phenotypic variation in infectivity of Diplostomum spathaceum cercariae within a population. J. Parasitol. 2007;93:124–1246. doi: 10.1645/GE-1187R.1. PubMed DOI

Koehler A.V., Springer Y.P., Keeney D.B., Poulin R. Intra-and interclonal phenotypic and genetic variability of the trematode Maritrema novaezealandensis. Biol. J. Linn. Soc. Lond. 2011;103:106–116. doi: 10.1111/j.1095-8312.2011.01640.x. DOI

Prokofiev V.V., Levakin I.A., Losev E.A., Zavirsky Ya A., Galaktionov K.V. Clonal variability in expression of geo-and photoorientation in cercariae of Himasthla elongata (Trematoda: Echinostomatidae) Parazitologiia. 2011;45:345–357. (In Russian) PubMed

Koehler A.V., Poulin R. Clone-specific immune reactions in a trematode-crustacean system. Parasitology. 2012;139:128–136. doi: 10.1017/S0031182011001739. PubMed DOI

Koehler A.V., Springer Y.P., Randhawa H.S., Leung T.L.F., Keeney D.B., Poulin R. Genetic and phenotypic influences on clone-level success and host specialization in a generalist parasite. J. Evol. Biol. 2012;25:66–79. doi: 10.1111/j.1420-9101.2011.02402.x. PubMed DOI

Levakin I.A., Losev E.A., Nikolaev K.E., Galaktionov K.V. In vitro encystment of Himasthla elongata cercariae (Digenea, Echinostomatidae) in the haemolymph of blue mussels Mytilus edulis as a tool for assessing cercarial infectivity and molluscan susceptibility. J. Helminthol. 2013;87:180–188. doi: 10.1017/S0022149X1200017X. PubMed DOI

Louhi K.R., Karvonen A., Rellstab C., Jokela J. Genotypic and phenotypic variation in transmission traits of a complex life cycle parasite. Ecol. Evol. 2013;3:2116–2127. doi: 10.1002/ece3.621. PubMed DOI PMC

Neves R.H., Costa-Silva M., Martinez E.M., Branquinho T.B., de Oliveira R.M., Lenzi H.L., Gomes D.C., Machado-Silva J.R. Phenotypic plasticity in adult worms of Schistosoma mansoni (Trematoda: Schistosomatidae) evidenced by brightfield and confocal laser scanning microscopies. Mem. Inst. Oswaldo Cruz. 2004;99:131–136. doi: 10.1590/S0074-02762004000200003. PubMed DOI

Mati V.L.T., Freitas R.M., Bicalho R.S., Melo A.L. Phenotypic plasticity of male Schistosoma mansoni from the peritoneal cavity and hepatic portal system of laboratory mice and hamsters. J. Helminthol. 2015;89:294–301. doi: 10.1017/S0022149X14000066. PubMed DOI

Bayne C.J., Grevelding C.G. Cloning of Schistosoma mansoni sporocysts in vitro and detection of genetic heterogeneity among individuals within clones. J. Parasitol. 2003;89:1056–1060. doi: 10.1645/GE-3186RN. PubMed DOI

Théron A., Sire C., Rognon A., Prugnolle F., Durand P. Molecular ecology of Schistosoma mansoni transmission inferred from the genetic composition of larval and adult infrapopulations within intermediate and definitive hosts. Parasitology. 2004;129:571–585. doi: 10.1017/S0031182004005943. PubMed DOI

Shalaby I., Gherbawy Y., Banaja A. Genetic diversity among Schistosoma mansoni population in the western region of Saudi Arabia. Trop. Biomed. 2011;28:90–101. PubMed

Korsunenko A., Chrisanfova G., Lopatkin A., Beer S.A., Voronin M., Ryskov A.P., Semyenova S.K. Genetic differentiation of cercariae infrapopulations of the avian schistosome Trichobilharzia szidati based on RAPD markers and mitochondrial cox1 gene. Parasitol. Res. 2012;110:833–841. doi: 10.1007/s00436-011-2562-6. PubMed DOI

Gu M.J., Li Y.W., Emery A.M., Li S.Z., Jiang Y.Z., Dong H.F., Zhao Q.P. The genetic variation of different developmental stages of Schistosoma japonicum: Do the distribution in snails and pairing preference benefit the transmission? Parasit. Vectors. 2020;13:360. doi: 10.1186/s13071-020-04240-w. PubMed DOI PMC

Mitta G., Adema C.M., Gourbal B., Loker E.S., Theron A. Compatibility polymorphism in snail/schistosome interactions: From field to theory to molecular mechanisms. Dev. Comp. Immunol. 2012;37:1–8. doi: 10.1016/j.dci.2011.09.002. PubMed DOI PMC

Lima M.G., Montresor L.C., Pontes J., Augusto R.C., da Silva J.P., Thiengo S.C. Compatibility polymorphism based on long-term host-parasite relationships: Cross talking between Biomphalaria glabrata and the trematode Schistosoma mansoni from endemic areas in Brazil. Front. Immunol. 2019;10:328. doi: 10.3389/fimmu.2019.00328. PubMed DOI PMC

Pino L.A., Matinella L., Morales G. The size polymorphism of the cercariae of a Venezuelan strain of Schistosoma mansoni. Rev. Soc. Bras. Med. Trop. 1999;32:443–446. doi: 10.1590/S0037-86821999000400016. PubMed DOI

Jouet D., Skírnisson K., Kolářová L., Ferté H. Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): A complex of species. Infect. Genet. Evol. 2010;10:1218–1227. doi: 10.1016/j.meegid.2010.08.001. PubMed DOI

Born-Torrijos A., Paterson R.A., van Beest G.S., Schwelm J., Vyhlídalová T., Henriksen E.H., Knudsen R., Kristoffersen R., Amundsen P.-A., Soldánová M. Temperature does not influence functional response of amphipods consuming different trematode prey. Parasitol. Res. 2020;119:4271–4276. doi: 10.1007/s00436-020-06859-1. PubMed DOI PMC

Born-Torrijos A., Paterson R.A., van Beest G.S., Vyhlídalová T., Henriksen E.H., Knudsen R., Kristoffersen R., Amundsen P.-A., Soldánová M. Cercarial behaviour alters the consumer functional response of three-spined sticklebacks. J. Anim. Ecol. 2021;90:978–988. doi: 10.1111/1365-2656.13427. PubMed DOI

Esch G.W., Curtis L.A., Barger M.A. A perspective on the ecology of trematode communities in snails. Parasitology. 2001;123:57–75. doi: 10.1017/S0031182001007697. PubMed DOI

Combes C., Bartoli P., Théron A. Trematode Transmission Strategies. In: Lewis E.E., Campbell J.F., Sukhdeo M.V.K., editors. The Behavioural Ecology of Parasites. CABI; Wallingford, UK: 2002. pp. 1–12. DOI

Morley N.J. Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia. 2012;691:7–19. doi: 10.1007/s10750-012-1029-9. DOI

Pietrock M., Marcogliese D.J. Free-living endohelminth stages: At the mercy of environmental conditions. Trends Parasitol. 2003;19:293–299. doi: 10.1016/S1471-4922(03)00117-X. PubMed DOI

Thieltges D.W., Jensen K.T., Poulin R. The role of biotic factors in the transmission of free-living endohelminth stages. Parasitology. 2008;135:407–426. doi: 10.1017/S0031182007000248. PubMed DOI

Combes C., Fournier A., Moné H., Théron A. Behaviours in trematode cercariae that enhance parasite transmission: Patterns and processes. Parasitology. 1994;109:3–13. doi: 10.1017/S0031182000085048. PubMed DOI

Haas W. Parasitic worms: Strategies of host finding, recognition and invasion. Zoology. 2003;106:349–364. doi: 10.1078/0944-2006-00125. PubMed DOI

Horák P., Mikeš L., Lichtenbergová L., Skála V., Soldánová M., Brant S.V. Avian schistosomes and outbreaks of cercarial dermatitis. Clin. Microbiol. Rev. 2015;28:165–190. doi: 10.1128/CMR.00043-14. PubMed DOI PMC

Soldánová M., Selbach C., Sures B. The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS ONE. 2016;11:e0149678. doi: 10.1371/journal.pone.0149678. PubMed DOI PMC

Ginetsinskaya T.A. Glycogen in cercariae, and the dependence of its distribution on the specific characters of the parasite. Dokl. Akad. Nauk SSSR. 1960;135:1012–1015.

Ginetsinskaya T.A. Trematodes; Their Life-Cycles, Biology and Evolution. Amerind Publ. Co., Pvt. Ltd.; New Delhi, India: 1988. p. 559.

Morley N.J. Cercarial swimming performance and its potential role as a key variable of trematode transmission. Parasitology. 2020;147:1369–1374. doi: 10.1017/S0031182020001171. PubMed DOI PMC

Lawson R.J., Wilson R.A. The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology. 1980;81:337–348. doi: 10.1017/S0031182000056079. PubMed DOI

Lowenberger C.A., Rau M.E. Plagiorchis elegans: Emergence, longevity and infectivity of cercariae, and host behavioural modifications during cercarial emergence. Parasitology. 1994;109:65–72. doi: 10.1017/S0031182000077775. PubMed DOI

Pechenik J.A., Fried B. Effect of temperature on survival and infectivity of Echinostoma trivolvis cercariae: A test of the energy limitation hypothesis. Parasitology. 1995;111:373–378. doi: 10.1017/S0031182000081920. DOI

Karvonen A., Paukku S., Valtonen E.T., Hudson P.J. Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Parasitology. 2003;127:217–224. doi: 10.1017/S0031182003003561. PubMed DOI

Johnson P.T.J., Thieltges D.W. Diversity, decoys and the dilution effect: How ecological communities affect disease risk. J. Exp. Biol. 2010;213:961–970. doi: 10.1242/jeb.037721. PubMed DOI

Johnson P.T.J., Dobson A., Lafferty K.D., Marcogliese D.J., Memmott J., Orlofske S.A., Poulin R., Thieltges D.W. When parasites become prey: Ecological and epidemiological significance of eating parasites. Trends Ecol. Evol. 2010;25:362–371. doi: 10.1016/j.tree.2010.01.005. PubMed DOI

Keesing F., Belden L.K., Daszak P., Dobson A., Harvell C.D., Holt R.D., Hudson P., Jolles A., Jones K.E., Mitchell C.E., et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468:647–652. doi: 10.1038/nature09575. PubMed DOI PMC

Goedknegt A., Welsh J., Thieltges D.W. Parasites as Prey. John Wiley & Sons, Ltd.; Hoboken, NJ, USA: 2012. p. 7. DOI

Stanicka A., Migdalski Ł., Szopieray K., Cichy A., Jermacz Ł., Lombardo P., Żbikowska E. Invaders as diluents of the cercarial dermatitis etiological agent. Pathogens. 2021;10:740. doi: 10.3390/pathogens10060740. PubMed DOI PMC

Kaplan A.T., Rebhal S., Lafferty K.D., Kuris A.M. Small estuarine fishes feed on large trematode cercariae: Lab and field investigations. J. Parasitol. 2009;95:477–480. doi: 10.1645/GE-1737.1. PubMed DOI

Orlofske S.A., Jadin R.C., Johnson P.T.J. It’s a predator-eat-parasite world: How characteristics of predator, parasite and environment affect consumption. Oecologia. 2015;178:537–547. doi: 10.1007/s00442-015-3243-4. PubMed DOI

Catania S.V., Koprivnikar J., McCauley S.J. Size-dependent predation alters interactions between parasites and predators. Can. J. Zool. 2016;94:631–635. doi: 10.1139/cjz-2016-0088. DOI

Welsh J.E., Hempel A., Markovic M., Van der Meer J., Thieltges D.W. Consumer and host body size effects on the removal of trematode cercariae by ambient communities. Parasitology. 2019;146:342–347. doi: 10.1017/S0031182018001488. PubMed DOI

Gilbert S.F. Ecological developmental biology: Developmental biology meets the real world. Dev. Biol. 2001;233:1–12. doi: 10.1006/dbio.2001.0210. PubMed DOI

Loker E.S. A comparative study of the life-histories of mammalian schistosomes. Parasitology. 1983;87:343–369. doi: 10.1017/S0031182000052689. PubMed DOI

Gérard C.J., Moné H., Théron A. Schistosoma mansoni-Biomphalaria glabrata: Dynamics of the sporocyst population in relation to the miracidial dose and the host size. Can. J. Zool. 1993;71:1880–1885. doi: 10.1139/z93-268. DOI

Podhorský M., Hůzová Z., Mikeš L., Horák P. Cercarial dimensions and surface structures as a tool for species determination of Trichobilharzia spp. Acta Parasitol. 2009;54:28–36. doi: 10.2478/s11686-009-0011-9. DOI

Poulin R. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology. 2006;132:143–151. doi: 10.1017/S0031182005008693. PubMed DOI

Horák P., Kolářová L., Adema C.M. Biology of the schistosome genus Trichobilharzia. Adv. Parasitol. 2002;52:155–233. doi: 10.1016/S0065-308X(02)52012-1. PubMed DOI

Grevelding C.G. Genomic instability in Schistosoma mansoni. Mol. Biochem. Parasitol. 1999;101:207–216. doi: 10.1016/S0166-6851(99)00078-X. PubMed DOI

Semyenova S.K., Khrisanfova G.G., Korsunenko A.V., Voronin M.V., Beer S.V., Vodyanitskaya S.V., Serbina E.A., Yurlova N.I., Ryskov A.P. Multilocus variation in cercariae, parthenogenetic progeny of different species of the class Trematoda. Dokl. Biol. Sci. 2007;414:235–238. doi: 10.1134/S0012496607030192. PubMed DOI

Galaktionov N.K., Podgornaya O.I., Strelkov P.P., Galaktionov K.V. Genomic diversity of cercarial clones of Himasthla elongata (Trematoda, Echinostomatidae) determined with AFLP technique. Parasitol. Res. 2016;115:4587–4593. doi: 10.1007/s00436-016-5249-1. PubMed DOI

Minchella D.J., Sollenberger K.M., Pereira de Souza C. Distribution of schistosome genetic diversity within molluscan intermediate hosts. Parasitology. 1995;111:217–220. doi: 10.1017/S0031182000064970. PubMed DOI

Davies C.M., Webster J.P., Krüger O., Munatsi A., Ndamba J., Woolhouse M.E. Host–parasite population genetics: A cross-sectional comparison of Bulinus globosus and Schistosoma haematobium. Parasitology. 1999;119:295–302. doi: 10.1017/S0031182099004722. PubMed DOI

Soldánová M., Georgieva S., Roháčová J., Knudsen R., Kuhn J.A., Henriksen E.H., Siwertsson A., Shaw J.C., Kuris A.M., Amundsen P.-A., et al. Molecular analyses reveal high species diversity of trematodes in a sub-Arctic lake. Int. J. Parasitol. 2017;47:327–345. doi: 10.1016/j.ijpara.2016.12.008. PubMed DOI

Reier S., Haring E., Billinger F., Blatterer H., Duda M., Gorofsky C., Grasser H.P., Heinisch W., Hörweg C., Kruckenhauser L., et al. First confirmed record of Trichobilharzia franki Müller & Kimmig, 1994, from Radix auricularia (Linnaeus, 1758) for Austria. Parasitol. Res. 2020;119:4135–4141. doi: 10.1007/s00436-020-06938-3. PubMed DOI PMC

Helmer N., Blatterer H., Hörweg C., Reier S., Sattmann H., Schindelar J., Szucsich N.U., Haring E. First record of Trichobilharzia physellae (Talbot, 1936) in Europe, a possible causative agent of cercarial dermatitis. Pathogens. 2021;10:1473. doi: 10.3390/pathogens10111473. PubMed DOI PMC

Brant S.V., Loker E.S. Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J. Parasitol. 2009;95:941–963. doi: 10.1645/GE-1870.1. PubMed DOI PMC

Abràmoff M.D., Magalhães P.J., Ram S.J. Image processing with ImageJ. Biophotonics Int. 2004;11:36–42.

Cercariae of a Bird Schistosome Follow a Similar Emergence Pattern under Different Subarctic Conditions: First Experimental Study