Folia Parasitologica, vol. 62 (2015)

Folia Parasitologica 62:003 (2015) | 10.14411/fp.2015.003

The taxonomic identity and phylogenetic relationships of Cercaria pugnax and C. helvetica XII (Digenea: Lecithodendriidae) based on morphological and molecular data

Olena Kudlai1,2, Virmantas Stun¾ėnas1, Vasyl Tkach3,4
1 Laboratory of Parasitology, Nature Research Centre, Vilnius, Lithuania;
2 Department of Parasitology, Institute of Zoology, Kyiv, Ukraine;
3 Department of Biology, University of North Dakota, Grand Forks, North Dakota, USA;
4 Institute of Parasitology, Polish Academy of Sciences, Warszawa, Poland

The present study analysed the taxonomic status and phylogenetic relationships of two species of xiphidiocercariae of the ʻmicrocotylaeʼ group, Cercaria pugnax La Valette St. George, 1855, from Viviparus viviparus (Linnaeus) in the Ukraine and Cercaria helvetica XII Dubois, 1928 from Bithynia tentaculata (Linnaeus) in Lithuania. Molecular phylogenetic analyses based on sequences of the ITS2 region and partial 28S gene of the nuclear rDNA revealed that both these xiphidiocercariae belong to the Lecithodendriidae Lühe, 1901 and represent larval stages of lecithodendriids parasitic in bats. Cercaria helvetica XII clustered with the typical representatives of the genus Lecithodendrium Looss, 1896, being very close, but not identical, to Lecithodendrium linstowi Dollfus, 1931. Sequences of C. pugnax matched exactly the sequences of adult Paralecithodendrium chilostomum (Mehlis, 1831). Morphological descriptions of the cercariae are included; these represent the first report of non-virgulate xiphidiocercariae belonging to the family Lecithodendriidae. Until now, the presence of glandular virgula organ in the region of the oral sucker was considered a robust synapomorphy for the Lecithodendriidae and several closely related families. Our results have shown that the relative importance of this character is in need of a re-assessment.

Keywords: Paralecithodendrium, Lecithodendrium, xiphidiocercaria, morphology, phylogeny, rDNA sequences

Received: June 6, 2014; Accepted: August 3, 2014; Prepublished online: November 26, 2014; Published online: January 1, 2015


References

  1. Azim M.A. 1936: On the life history of Lecithodendrium pyramidum Looss, 1896 and its development from a xiphiodiocercaria, C. pyramidum sp. nov. from Melania tuberculata. Ann. Trop. Med. Parasitol. 30: 351-354. Go to original source...
  2. Bartoli P., Jousson O., Russell-Pinto F. 2000: The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. J. Parasitol. 86: 479-489. Go to original source... Go to PubMed...
  3. Besprozvannykh V.V. 1990: [Life cycle of Prosthodendrium dollfusi sp. n. and Acanthotrium ovatum (Trematoda: Lecithodendriidae) in the south of the Far East of the USSR.] Parazitologiya 24: 431-439. (In Russian.)
  4. Bowles J., Blair D., McManus D.P. 1995: A molecular phylogeny of the human schistosomes. Mol. Phylogenet. Evol. 4: 103-109. Go to original source... Go to PubMed...
  5. Brant S.V., Morgan J.A., Mkoji G.M., Snyder S.D., Rajapakse R.P., Loker E.S. 2006: An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of keyreference data including DNA sequence from single life cycle stages. J. Parasitol. 92: 77-88. Go to original source... Go to PubMed...
  6. Brooks D.R., Bandoni S.M., Macdonald C.A., O'Grady R.T. 1989: Aspects of the phylogeny of the Trematoda Rudolphi, 1808 (Platyhelminthes: Cercomeria). Can. J. Zool. 67: 2609-2624. Go to original source...
  7. Brooks D.R., O'Grady R.T., Glen D.R. 1985: Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Can. J. Zool. 63: 411-443. Go to original source...
  8. Brown F.J. 1933: On the excretory system and life history of Lecithodendrium chilostomum (Mehl.) and other bat trematodes, with a note on the life history of Dicrocoelium dendriticum (Rudolphi). Parasitology 25: 317-328. Go to original source...
  9. Burns W.C. 1961a: Six virgulate xiphidocercariae from Oregon, including redescriptions of Allassogonoporus vespertilionis and Acantharium oregonense. J. Parasitol. 47: 919-925. Go to original source...
  10. Burns W.C. 1961b: Penetration and development of Allassogonoporus vespertilionis and Acanthatrium oregonense (Trematoda: Lecithodendriidae) cercariae in caddis larvae. J. Parasitol. 47: 927-932. Go to original source... Go to PubMed...
  11. Bychovskaya-Pavlovskaya I.E., Kulakova A.P. 1971: [Cercariae of Bithynia tentaculata and B. leachi from the Kurish Gulf.] Parazitologiya 5: 222-232. (In Russian.)
  12. Cichy A., Faltýnková A., ¯bikowska E. 2011: Cercariae (Trematoda, Digenea) in European freshwater snails - a checklist of records from over one hundred years. Folia Malacol. 19: 165-189. Go to original source...
  13. Dubois G. 1928: Les cercaires de la region de Neuchâtel. Bull. Soc. Neuchâtel. Sci. Nat. 53: 1-177.
  14. Etges F.J. 1960: On the life history of Prosthodendrium (Acanthatrium) anaplocami n. sp. (Trematoda: Lecithodendriide). J. Parasitol. 46: 235-240. Go to original source... Go to PubMed...
  15. Galaktionov K.V, Blasco-Costa I., Olson P.D. 2012: Life cycles, molecular phylogeny and historical biogeography of the 'pygmaeus' microphallids (Digenea: Microphallidae): widespread parasites of marine and coastal birds in the Holarctic. Parasitology 139: 1346-1360. Go to original source... Go to PubMed...
  16. Ginetsinskaya T.A., Dobrovolskii A.A. 1968: [Larval trematode fauna of freshwater mollusks of the Volga Delta. Part III. Furcocercariae (Cyathocotylidae) and xiphidiocercariae.] Proceedings of the Astrakhan state nature reserve 11: 29-95. (In Russian.)
  17. Glöer P. 2002: Die Süsswassergastropoden Nord- und Mitteleuropas. Bestimmungsschlüssel, Lebensweise, Verbreitung. Die Tierwelt Deutschlands 73. ConchBooks, Hackenheim, 326 pp.
  18. Heneberg P., Literák I. 2013: Molecular phylogenetic characterization of Collyriclum faba with reference to its three host-specific ecotypes. Parasitol. Int. 62: 262-267. Go to original source... Go to PubMed...
  19. Jensen K., Bullard S.A. 2010: Characterization of a diversity of tetraphyllidean and rhinebothriidean cestode larval types, with comments on host associations and life-cycles. Int. J. Parasitol. 40: 889-910. Go to original source... Go to PubMed...
  20. Knight R.A., Pratt I. 1955: The life-histories of Allassogonoporus vespertilionis Macy and Acanthatrium oregonense Macy (Trematoda: Lecithodendriidae). J. Parasitol. 41: 248-255. Go to original source... Go to PubMed...
  21. La Valette St. George A. 1855: Symbolae ad Trematodum Evolutionis Historiam. Dissertation, Berlin, 40 pp.
  22. Locke S.A., McLaughlin J.D., Lapierre A.P., Johnson P.T.J., Marcogliese D.J. 2011: Linking larvae and adults of Apharyngostrigea cornu, Hysteromorpha triloba, and Alaria mustelae (Diplostomoidea: Digenea) using molecular data. J. Parasitol. 97: 846-851. Go to original source... Go to PubMed...
  23. Lord J.S., Parker S., Parker F., Brooks D.R. 2012: Gastrointestinal helminths of pipistrelle bats (Pipistrellus pipistrellus/Pipistrellus pygmaeus) (Chiroptera: Vespertilionidae) of England. Parasitology 139: 366-374. Go to original source... Go to PubMed...
  24. Lotz J.M., Font W.F. 2008: Family Lecithodendriidae Lühe, 1901. In: R.A. Bray, A. Jones and D.I. Gibson (Eds.), Keys to the Trematoda. Volume 3. CABI, Wallingford and Natural History Museum, London, pp. 527-536.
  25. Lubarskaya O.D., Galeeva L.Kh. 1980: [Rates of infection with trematode metacercariae of dragonflies in the Tatar ASSR.]. Problems of Parasitology of Aquatic Invertebrates: 68-70. (In Russian.)
  26. Petkevièiūtė R., Stun¾ėnas V., Stanevièiūtė G. 2014: Differentiation of European freshwater bucephalids (Digenea: Bucephalidae) based on karyotypes and DNA sequences. Syst. Parasitol. 87: 199-212. Go to original source... Go to PubMed...
  27. Pina S.M.R., Russell-Pinto F., Rodrigues P. 2007: Clarification of Cercaria sevillana (Digenea: Microphallidae) life cycle using morphological and molecular data. J. Parasitol. 93: 318-322. Go to original source... Go to PubMed...
  28. Posada D. 2008: jModelTest: Phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256. Go to original source... Go to PubMed...
  29. Seitner P.G. 1945: Studies on five new species of xiphidiocercariae of the virgule type. J. Parasitol. 31: 272-281. Go to original source...
  30. Sharpilo V.P., Iskova N.I. 1989: [Fauna of the Ukraine. Vol. 34. Trematoda. Part 3. Plagiorchiata]. Naukova dumka, Kiev, 279 pp. (In Russian.)
  31. Shevchenko N.N. 1966: [Helminth fauna of some species of mammals of valley of Seversky Donets (Kharkiv oblast) and their influence on the composition and circulation of parasites of water biocenosis.] Materialy Nauchnoy Konferentsii VOG 3: 321-327. (In Russian.)
  32. Stenko R., Korol E., Dulitskii A.I. 2005: [Lecithodendriids - parasites of the Chiroptera from the protected areas of the Crimea.]. Materialy III Nauchnoy Konferentsii "Zapovedniky Kryma: zapovednoe delo, bioraznoobrazie, ekoobrazovanie", Simferopol, Ukraine, 22 April 2005, pp. 83-87. (In Russian.)
  33. Stun¾ėnas V., Petkevièiūtė R., Stanevièiūtė G. 2011: Phylogeny of Sphaerium solidum (Bivalvia) based on karyotype and sequences of 16S and ITS1 rDNA. Centr. Eur. J. Biol. 6: 105-117. Go to original source... Go to PubMed...
  34. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 24: 2731-2739. Go to original source... Go to PubMed...
  35. Thompson J.D., Higgins D.G., Gibson .T.J. 1994: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673-4680. Go to original source... Go to PubMed...
  36. Tkach V., Grabda-Kazubska B., Pawlowski J., Swiderski Z. 1999: Molecular and morphological evidences for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus, and Paralepoderma (Digenea, Plagiorchioidea). Acta Parasitol. 44: 170-179.
  37. Tkach V., Littlewood D.T.J., Olson P.D., Kinsella J.M., Swiderski Z. 2003: Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst. Parasitol. 56: 1-15. Go to original source... Go to PubMed...
  38. Tkach V., Pawlowski J., Mariaux J. 2000: Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int. J. Parasitol. 30: 83-93. Go to original source... Go to PubMed...