Abstract
In New Zealand, a single morphotype, comprising three genetically distinct opecoelid species, infects four sympatric species of trochid snails. Two species (a and b) are specific to Diloma subrostrata while the third (c) is more general, capable of infecting three species, most commonly D. aethiops but never D. subrostrata. We sampled three D. subrostrata and D. aethiops populations, in which infection levels ranged from 0 to 29.2%, and attempted species assignation based on host information, restriction fragment length polymorphism (RFLP) analysis and morphology. Host information allowed reliable separation of species a and b from species c. Restriction mapping of ribosomal DNA internal transcriber spacer 2 (ITS2) demonstrated that the restriction enzyme SfuI only digested ITS2 from species b and c. Thus, restriction digests + host species information allowed reliable species assignation. Morphological measurements were taken for both sporocysts and cercariae dissected from 83 infected snails. Substantial overlap existed between measurements for the three species, and discriminant analysis showed that parasites could not be unequivocally assigned to a species—error rates ranged from 9 to 58%—despite statistically significant differences among several means. Amongst this group of digeneans, host information + RFLP provide a rapid, unambiguous method of species assignation that host information + morphological measurements cannot.
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References
Adamson ML, Caira JN (1994) Evolutionary factors influencing the nature of parasite specificity. Parasitology 109:85–95
Blair D, Davis GM, Wu B (2001) Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123:S229–S243
Blankespoor HD (1974) Host-induced variation in Plagiorchis noblei Park, 1936 (Plagiorchiidae: Trematoda). Am Midl Nat 92:415–433
Clark W (1958) A new cotylocerous cercaria from Melagraphia aethiops (Gm.) (Gastropoda). Trans Roy Soc NZ 85:681–683
Cribb TH, Bray RA, Littlewood TJ, Pichelin SP, Herniou EA (2001) The Digenea. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminths. Taylor and Francis, London, UK, pp 168–185
Després L, Imbert-Establet D, Combes C, Bonhomme F (1992) Molecular evidence linking hominid evolution to recent radiation of schistosomes (Platyhelminthes: Trematoda). Mol Phylogenet Evol 1:295–304
Donald KM, Kennedy M, Poulin R, Spencer HG (2004) Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int J Parasitol 34:557–568
Donald KM, Kennedy M, Spencer HG (2005) The phylogeny and taxonomy of austral monodontine topshells (Mollusca: Gastropoda: Trochidae), inferred from DNA sequences. Mol Phylogenet Evol 37:474–483
Fredensborg BL, Mouritsen KN, Poulin R (2005) Impact of trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Mar Ecol Prog Ser 290:109–117
Fried B, Mueller TJ, Frazer BA (1997) Observations on Echinostoma revolutum and Echinostoma trivolvis in single and concurrent infections in domestic chicks. Int J Parasitol 27:1319–1322
Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can J Zool 80:2207–2217
Gasser RB, Chilton NB (1995) Characterisation of taeniid cestode species by PCR-RFLP of ITS2 ribosomal DNA. Acta Trop 59:31–40
Gibson DI (1987) Questions in digenean systematics and evolution. Parasitology 95:429–460
Gibson DI, Bray RA (1994) The evolutionary expansion and host-parasite relationship of the Digenea. Int J Parasitol 24:1213–1226
Jousson O, Bartoli P (2001) Molecules, morphology and morphometrics of Cainocreadium labracis and Cainocreadium dentecis n. sp. (Digenea: Opecoelidae) parasitic in marine fishes. Int J Parasitol 31:706–714
Jousson O, Bartoli P, Pawlowski J (1999) Molecular identification of developmental stages in Opecoelidae (Digenea). Int J Parasitol 29:1853–1858
Jousson O, Bartoli P, Pawlowski J (2000) Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). J Evol Biol 13:778–785
Kinsella JM (1971) Growth, development, and intraspecific variation of Quinqueserialis quinqueserialis (Trematoda, Notocotylidae) in rodent hosts. J Parasitol 57:62–70
Lindeque PK, Harris RP, Jones MB, Smerdon GR (1999) Simple molecular method to distinguish the identity of Calanus species (Copepoda: Calanoida) at any developmental stage. Mar Biol 133:91–96
Lucas T, O’Brien EK, Cribb T, Degnan BM (2005) Digenean trematodes infecting tropical abalone Haliotis asinina have species-specific cercarial emergence patterns that follow daily or semilunar spawning cycles. Mar Biol 148:285–292
Luton K, Walker D, Blair D (1992) Comparisons of ribosomal internal transcribed spacer from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Mol Biochem Parasitol 56:323–328
Marcogliese DJ, Cone DK (1997) Food webs: a plea for parasites. Trends Ecol Evol 12:320–325
McDaniel JS (1969) Littorina littorea: lowered heat tolerance due to Cryptocotyle lingua. Exp Parasitol 25:13–15
Miller AA, Poulin R (2001) Parasitism, movement, and distribution of the snail Diloma subrostrata (Trochidae) in a soft-sediment intertidal zone. Can J Zool 79:2029–2035
Moore J, Gotelli NJ (1990) A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In: Barnard CJ, Behnke JM (eds) Parasitism and host behaviour. Taylor and Francis, London, UK, pp 193–233
Mouritsen KN, Poulin R (2002). Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124:S101–S117
Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163
Nunez PE, De Jong-Brink M (1997) The suppressive excretory-secretary product of Trichobilharzia ocellata: a possible factor for determining compatibility in parasite–host interactions. Parasitology 115:193–203
Pérez Ponce de León G (1995) Host-induced morphological variability in adult Posthodiplostomum minimum (Digenea: Neodiplostomidae). J Parasitol 81:818–820
Poulin R (1998) Evolutionary ecology of parasites: from individuals to communities. Chapman and Hall, London, UK
Raffaelli D (2000) Trends in research on shallow water food webs. J Exp Mar Biol Ecol 250:223–232
Schulenburg JHG, Englisch U, Wägele JW (1999) Evolution of ITS1 rDNA in the Digenea (Platyhelminthes: Trematoda): 3′ end sequence conservation and its phylogenetic utility. J Mol Evol 48:2–12
Sousa WP (1991) Can models of soft-sediment community structure be complete without parasites. Am Zool 31:821–830
Stunkard HW (1983) The marine cercariae of the Woods Hole, Massachusetts region, a review and a revision. Biol Bull 164:143–162
Tkach VV, Pawlowski J, Sharpilo VP (2000) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Muller, 1780). Syst Parasitol 47:9–22
Walsh PS, Metzger DA, Higuchi R (1991) Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10:506–513
Acknowledgement
We are grateful to Robert Poulin who provided helpful comments on the manuscript. Brent Hall, Nick Hankey, Peter Knight and Antoni Moore collected the Bluff Harbour samples. Antoni Moore provided the map. This research was supported by the Allan Wilson Centre for Molecular Ecology and Evolution, and all experiments complied with New Zealand law.
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Donald, K.M., Sijnja, A. & Spencer, H.G. Species assignation amongst morphologically cryptic larval Digenea isolated from New Zealand topshells (Gastropoda: Trochidae). Parasitol Res 101, 433–441 (2007). https://doi.org/10.1007/s00436-007-0501-3
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DOI: https://doi.org/10.1007/s00436-007-0501-3