Advertisement

The Systematics of the Trematoda

  • Aneta KostadinovaEmail author
  • Ana Pérez-del-Olmo
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1154)

Abstract

The platyhelminth class Trematoda comprises two subclasses with largely disparate species diversity, the small Aspidogastrea with c.80 species and the speciose Digenea with c.18,000 species, which has attracted much effort towards our understanding of evolutionary relationships among suprageneric taxa. This chapter focuses on insights into the classification of the Digenea that have become apparent from our advanced understanding of both morphological and molecular data. The field of molecular systematics of the Digenea has experienced significant advances over the past 15 years. Phylogenetic analyses of sequence data predominantly from the 18S and 28S rRNA genes have incorporated a considerable diversity of taxa thus increasing the accuracy of phylogenetic inferences at higher taxonomic levels. As a result, the status of long-standing supraspecific taxa has been revised, new higher-level taxa have been defined, and inferences made in association with morphological and life-cycle evidence. A substantial effort has been made towards a classification reflecting the natural system of the Digenea by considering morphological evidence in conjunction with phylogenies inferred from molecular data; this has resulted in considerable congruence. However, limited taxon sampling in the phylogeny of the Digenea still remains relevant especially in relation to some higher-level taxa, and an outline of these omissions is presented. A framework that has led to robust estimates of phylogeny is outlined, and the application of advanced morphological and molecular approaches in digenean taxonomy and systematics is illustrated using the most comprehensively studied digenean superfamilies.

Keywords

Class Trematoda Subclass Aspidogastrea Subclass Digenea Systematics Classification Molecular phylogeny 

References

  1. Aldhoun JA, Littlewood DTJ (2012) Orientobilharzia Dutt & Srivastava, 1955 (Trematoda: Schistosomatidae), a junior synonym of Schistosoma Weinland, 1858. Syst Parasitol 82:81–88PubMedCrossRefGoogle Scholar
  2. Barker SC, Blair D, Garrett AR, Cribb TH (1993) Utility of the D1 domain of nuclear 28S rRNA for phylogenetic inference in the Digenea. Syst Parasitol 26:181–188CrossRefGoogle Scholar
  3. Blair D, Barker S (1993) Affinities of the Glyauchenidae: utility of the 18S rRNA gene for the phylogenetic inference in the Digenea (Platyhelminthes). Int J Parasitol 23:527–532PubMedCrossRefPubMedCentralGoogle Scholar
  4. Blair D, Bray RA, Barker SC (1998) Molecules and morphology in phylogenetic studies of the Hemiuroidea (Digenea: Trematoda: Platyhelminthes). Mol Phylogenet Evol 9:15–25PubMedCrossRefPubMedCentralGoogle Scholar
  5. Brabec J, Kostadinova A, Scholz T, Littlewood DTJ (2015) Complete mitochondrial genomes and nuclear ribosomal RNA operons of two species of Diplostomum (Platyhelminthes: Trematoda): a molecular resource for taxonomy and molecular epidemiology of important fish pathogens. Parasit Vectors 8:336PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bray RA (2005a) Family Enenteridae Yamaguti, 1958. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 657–661CrossRefGoogle Scholar
  7. Bray RA (2005b) Family Gorgocephalidae Manter, 1966. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 663–664CrossRefGoogle Scholar
  8. Bray RA (2005c) Family Lepocreadiidae Odhner, 1905. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 545–602CrossRefGoogle Scholar
  9. Bray RA (2005d) Superfamily Lepocreadioidea Odhner, 1905. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 541–543CrossRefGoogle Scholar
  10. Bray RA (2008) Introduction and key to superfamilies. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 1–5Google Scholar
  11. Bray RA, Cribb TH (1997) The subfamily Aephnidiogeninae Yamaguti, 1934 (Digenea: Lepocreadiidae), its status and that of the genera Aephnidiogenes Nicoll, 1915, Holorchis Stossich, 1901, Austroholorchis gen. n., Pseudaephnidiogenes Yamaguti, 1971, Pseudoholorchis Yamaguti, 1958 and Neolepocreadium Thomas, 1960. Syst Parasitol 36:47–68CrossRefGoogle Scholar
  12. Bray RA, Cribb TH (2003) The digeneans of elasmobranchs—distribution and evolutionary significance. In: Combes C, Jourdane J (eds) Taxonomie, écologie et évolution des métazoaires parasites. (Livre hommage à Louis Euzet). Tome 1. PUP, Perpignan, pp. 67–96Google Scholar
  13. Bray RA, Cribb TH (2012) Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Syst Parasitol 83:169–177PubMedCrossRefPubMedCentralGoogle Scholar
  14. Bray RA, Gibson DI (1977) The Accacoeliidae (Digenea) of fishes from the north-east Atlantic. Bull Br Museum Nat Hist (Zool) 31:51–99Google Scholar
  15. Bray RA, Webster BL, Bartoli P, Littlewood DTJ (2005) Relationships within the Acanthocolpidae Lühe, 1906 and their place among the Digenea. Acta Parasitol 50:281–291Google Scholar
  16. Bray RA, Gibson DI, Jones A (eds) (2008) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and LondonGoogle Scholar
  17. Bray RA, Waeschenbach A, Cribb TH, Weedall GD, Dyal P, Littlewood DTJ (2009) The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitol 54:310–329Google Scholar
  18. Bray RA, Cribb TH, Cutmore SC (2018) Lepocreadiidae Odhner, 1905 and Aephnidiogenidae Yamaguti, 1934 (Digenea: Lepocreadioidea) of fishes from Moreton Bay, Queensland, Australia, with the erection of a new family and genus. Syst Parasitol 95:479–498PubMedPubMedCentralCrossRefGoogle Scholar
  19. Brooks DR, McLennan DA (1993) Parascript. Parasites and the language of evolution. Smithsonian Institution Press, WashingtonGoogle Scholar
  20. Brooks DR, O’Grady RT, Glen DR (1985) Phylogenetic analysis of the Digenea (Platyhelminthes: Cercomeria) with comments on their adaptive radiation. Can J Zool 63:411–443CrossRefGoogle Scholar
  21. Brooks DR, Bandoni SM, MacDonald CA, O’Grady RT (1989) Aspects of the phylogeny of the Trematoda Rudolphi, 1808 (Platyhelminthes: Cercomeria). Can J Zool 67:2609–2624CrossRefGoogle Scholar
  22. Cable RM (1974) Phylogeny and taxonomy of trematodes with reference to marine species. In: Vernberg WB (ed) Symbiosis in the sea. University of South California Press, Charleston, pp. 173–193Google Scholar
  23. Cribb TH (2005) Superfamily Allocreadioidea Looss, 1902. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 413–539CrossRefGoogle Scholar
  24. Cribb TH, Bray RA, Littlewood DTJ, Pichelin S, Herniou EA (2001) Relationships of the Digenea—evidence from molecules and morphology. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 186–193Google Scholar
  25. Cribb TH, Bray RA, Olson PD, Littlewood DTJ (2003) Life cycle evolution in the Digenea: a new perspective from phylogeny. Adv Parasitol 54:197–254PubMedCrossRefGoogle Scholar
  26. Deblock S (2008) Family Microphallidae Ward, 1901. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 451–492Google Scholar
  27. Fernandez M, Littlewood DTJ, Latorre A, Raga JA, Rollinson D (1998) Phylogenetic relationships of the family Campulidae (Trematoda) based on 18S rDNA sequences. Parasitology 117:383–391PubMedCrossRefPubMedCentralGoogle Scholar
  28. Font WF, Lotz JM (2008) Family Telorchiidae Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 425–436Google Scholar
  29. Fraija-Fernández N, Olson PD, Crespo EA, Raga JA, Aznar FJ, Fernández M (2015) Independent host switching events by digenean parasites of cetaceans inferred from ribosomal DNA. Int J Parasitol 45:167–173PubMedCrossRefPubMedCentralGoogle Scholar
  30. Gibson DI (1987) Questions in digenean systematics and evolution. Parasitology 95:429–460PubMedCrossRefPubMedCentralGoogle Scholar
  31. Gibson DI (1996) Trematoda. In: Margolis L, Kabata Z (eds) Guide to the Parasites of Fishes of Canada. Part IV. Canadian Special Publication of Fisheries and Aquatic Sciences No. 124. NRC Press, Ottawa, pp. 1–373Google Scholar
  32. Gibson DI (2002a) Class Trematoda Rudolphi, 1808. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI and The Natural History Museum, Wallingford and London, pp. 1–3CrossRefGoogle Scholar
  33. Gibson DI (2002b) Superfamily Azygioidea Lühe, 1909. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI and The Natural History Museum, Wallingford and London, pp. 19–24CrossRefGoogle Scholar
  34. Gibson DI (2002c) Superfamily Hemiuroidea Looss, 1899. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI, Wallingford, pp. 299–304CrossRefGoogle Scholar
  35. Gibson DI, Bray RA (1977) The Azygiidae, Hirudinellidae, Ptychogonimidae, Sclerodistomidae and Syncoeliidae (Digenea) of fishes from the north-east Atlantic. Bull Br Museum Nat Hist (Zool) 32:167–245Google Scholar
  36. Gibson DI, Bray RA (1979) The Hemiuroidea: terminology, systematics and evolution. Bull Br Museum Nat Hist (Zool) 36:35–146CrossRefGoogle Scholar
  37. Gibson DI, Bray RA (1986) The Hemiuridae (Digenea) of fishes from the north-east Atlantic. Bull Br Museum Nat Hist (Zool) 51:1–125Google Scholar
  38. Gibson DI, Bray RA (1994) The evolutionary expansion and host-parasite relationships of the Digenea. Int J Parasitol 24:1213–1226PubMedCrossRefGoogle Scholar
  39. Gibson DI, Chinabut S (1984) Rohdella siamensis gen. et sp. nov. (Aspidogastridae: Rohdeliinae subfam. nov.) from freshwater fishes in Thailand, with a reorganisation of the classification of the subclass Aspidogastrea. Parasitology 88:383–393CrossRefGoogle Scholar
  40. Gibson DI, Jones A, Bray RA (eds) (2002) Keys to the Trematoda, vol 1. CABI, WallingfordGoogle Scholar
  41. Hall KA, Cribb TH (2005) Family Gyliauchenidae Fukui, 1929. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 665–678CrossRefGoogle Scholar
  42. Hall KA, Cribb TH, Barker SC (1999) V4 region of small subunit rDNA indicates polyphyly of the Fellodistomidae (Digenea) which is supported by morphology and life-cycle data. Syst Parasitol 43:81–92PubMedCrossRefPubMedCentralGoogle Scholar
  43. Hernández-Mena DI, García-Varela M, Pérez-Ponce de León G (2017) Filling the gaps in the classification of the Digenea Carus, 1863: systematic position of the Proterodiplostomidae Dubois, 1936 within the superfamily Diplostomoidea Poirier, 1886, inferred from nuclear and mitochondrial DNA sequences. Syst Parasitol 94:833–848PubMedCrossRefGoogle Scholar
  44. Johnston DA (2006) Genomes and genomics of parasitic flatworms. In: Maule AG, Marks NJ (eds) Parasitic flatworms. Molecular biology, biochemistry, immunology and physiology. CABI, Wallingford, pp. 37–80Google Scholar
  45. Jones A (2008) Family Prosthogonimidae Lühe, 1909. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 577–590Google Scholar
  46. Jones A, Bray RA, Gibson DI (eds) (2005) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and LondonGoogle Scholar
  47. Khalil LF (2002) Family Schistosomatidae Stiles & Hassall, 1898. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI, Wallingford, pp. 419–432CrossRefGoogle Scholar
  48. Kostadinova A (2005a) Family Echinostomatidae Looss, 1899. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 9–64CrossRefGoogle Scholar
  49. Kostadinova A (2005b) Family Cathaemasiidae Fuhrmann, 1928. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 69–77CrossRefGoogle Scholar
  50. Kostadinova A (2005c) Family Psilostomidae Looss, 1900. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 99–118CrossRefGoogle Scholar
  51. Kostadinova A, Gibson DI (2002) Isthmiophora Lühe, 1909 and Euparyphium Dietz, 1909 (Digenea: Echinostomatidae) re-defined, with comments on their nominal species. Syst Parasitol 52:205–217PubMedCrossRefPubMedCentralGoogle Scholar
  52. Kostadinova A, Jones A (2005) Superfamily Echinostomatoidea Looss, 1899. In: Jones A, Bray RA, Gibson DI (eds) Keys to the Trematoda, vol 2. CABI and The Natural History Museum, Wallingford and London, pp. 5–8CrossRefGoogle Scholar
  53. La Rue GR (1957) The classification of digenetic Trematoda: a review and a new system. Exp Parasitol 6:306–344CrossRefGoogle Scholar
  54. Lawton SP, Hirai H, Ironside JE, Johnston D, Rollinson D (2011) Genomes and geography: genomic insights into the evolution and phylogeography of the genus Schistosoma. Parasit Vectors 4:131PubMedPubMedCentralCrossRefGoogle Scholar
  55. Le TH, Humair PF, Blair D, Agatsuma T, Littlewood DT, McManus DP (2001) Mitochondrial gene content, arrangement and composition compared in African and Asian schistosomes. Mol Biochem Parasitol 117:61–71PubMedCrossRefPubMedCentralGoogle Scholar
  56. Le TH, Nguyen NTB, Nguyen KT, Doan HTT, Dung DT, Blair D (2016) A complete mitochondrial genome from Echinochasmus japonicus supports the elevation of Echinochasminae Odhner, 1910 to family rank (Trematoda: Platyhelminthes). Infect Genet Evol 45:369–377PubMedCrossRefPubMedCentralGoogle Scholar
  57. Littlewood DTJ (2006) The evolution of parasitism in flatworms. In: Maule AG, Marks NJ (eds) Parasitic flatworms. Molecular biology, biochemistry, immunology and physiology. CABI, Wallingford, pp. 1–35Google Scholar
  58. Littlewood DTJ (2008) Platyhelminth systematics and the emergence of new characters. Parasite 15:333–341PubMedCrossRefPubMedCentralGoogle Scholar
  59. Littlewood DTJ, Lockyer AE, Webster BL, Johnston DA, Le TH (2006) The complete mitochondrial genomes of Schistosoma haematobium and Schistosoma spindale and the evolutionary history of mitochondrial genome changes among parasitic flatworms. Mol Phylogenet Evol 39:452–467PubMedCrossRefPubMedCentralGoogle Scholar
  60. Locke SA, Van Dam AV, Caffara M, Alves Pinto H, López-Hernández D, Blanar CA (2018) Validity of the Diplostomoidea and Diplostomida (Digenea, Platyhelminthes) upheld in phylogenomic analysis. Int J Parasitol 48:1043–1059PubMedCrossRefGoogle Scholar
  61. Lockyer AE, Olson PD, Littlewood DTJ (2003a) Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Neodermata (Platyhelminthes): implications and a review of the cercomer theory. Biol J Linn Soc 78:155–171CrossRefGoogle Scholar
  62. Lockyer AE, Olson PD, Østergaard P, Rollinson D, Johnston DA, Attwood SW, Southgate VR, Horak P, Snyder SD, Le TH, Agatsuma T, McManus D, Carmichael AC, Naem S, Littlewood DTJ (2003b) The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 126:203–224PubMedCrossRefPubMedCentralGoogle Scholar
  63. Lotz JM, Font WF (2008) Family Pleurogenidae Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 563–575CrossRefGoogle Scholar
  64. Mallatt J, Giribet G (2006) Further use of nearly complete 28S and 18S rRNA genes to classify Ecdysozoa: 37 more arthropods and a kinorhynch. Mol Phylogenet Evol 40:772–794PubMedCrossRefPubMedCentralGoogle Scholar
  65. Mallatt J, Winchell CJ (2002) Testing the new animal phylogeny: first use of combined large-subunit and smallsubunit rRNA gene sequences to classify the protostomes. Mol Biol Evol 19:289–301PubMedCrossRefPubMedCentralGoogle Scholar
  66. Mallatt JM, Garey JR, Shultz JW (2004) Ecdysozoan phylogeny and Bayesian inference: first use of nearly complete 28S and 18S rRNA gene sequences to classify the arthropods and their kin. Mol Phylogenet Evol 31:178–191PubMedCrossRefPubMedCentralGoogle Scholar
  67. Nolan MJ, Cribb TH (2005) The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Adv Parasitol 60:101–163PubMedCrossRefPubMedCentralGoogle Scholar
  68. Odening K (1961) Historische und moderne Gesichtspunkte beim Aufbau eines natürlichen Systems der digenetischen Trematoden. Biol Beitr 1:73–90Google Scholar
  69. Odening K (1964) Exkretionssystem und systematische stellung einiger Fledermaustrematoden aus Berlin und Umgebung nebst Bemerkungen zum lecithodendrioiden Komplex. Z Parasitenkd 24:453–483PubMedCrossRefPubMedCentralGoogle Scholar
  70. Odening K (1974) Verwandtschaft, system und zyklo-ontogenetische Besonderheiten der Trematoden. Zool Jahrb Systematik 101:345–396Google Scholar
  71. Olson PD, Tkach VV (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Adv Parasitol 60:165–243PubMedCrossRefPubMedCentralGoogle Scholar
  72. Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755PubMedCrossRefPubMedCentralGoogle Scholar
  73. Pankov P, Webster BL, Blasco MI, Gibson DI, Littlewood DTJ, Kostadinova A (2006) Robinia aurata n. g., n. sp. (Digenea: Hemiuridae) from Liza aurata (Perciformes: Mugilidae) in the western Mediterranean described from morphology and molecules. Parasitology 133:217–227PubMedCrossRefPubMedCentralGoogle Scholar
  74. Pearson JC (1972) A phylogeny of life-cycle patterns of the Digenea. Adv Parasitol 10:153–189PubMedCrossRefPubMedCentralGoogle Scholar
  75. Pearson JC (1992) On the position of the digenean family Heronimidae: an enquiry into a cladistic classification of the Digenea. Syst Parasitol 21:81–166CrossRefGoogle Scholar
  76. Philippe H, Brinkmann H, Lavrov DV, Littlewood DTJ, Manuel M, Wörheide G, Baurain D (2011) Resolving difficult phylogenetic questions: why more sequences are not enough. PLoS Biol 9:e1000602PubMedPubMedCentralCrossRefGoogle Scholar
  77. Poche F (1926) Das System der Platodaria. Arch Naturgesch 91:1–459Google Scholar
  78. Rohde K (1972) The Aspidogastrea, especially Multicotyle purvisi Dawes, 1941. Adv Parasitol 10:77–151CrossRefGoogle Scholar
  79. Rohde K (1994) The minor groups of parasitic Platyhelminthes. Adv Parasitol 33:145–234PubMedCrossRefPubMedCentralGoogle Scholar
  80. Rohde K (2001) The Aspidogastrea: an archaic group of Platyhelminthes. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 159–166Google Scholar
  81. Rohde K (2002) Subclass Aspidogastrea Faust & Tang, 1936. In: Gibson DI, Jones A, Bray RA (eds) Keys to the Trematoda, vol 1. CABI, Wallingford, pp. 5–14CrossRefGoogle Scholar
  82. Snyder SD (2004) Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). Int J Parasitol 34:1385–1392PubMedCrossRefGoogle Scholar
  83. Snyder SD, Loker ES (2000) Evolutionary relationships among the Schistosomatidae (Platyhelminthes: Digenea) and an Asian origin for Schistosoma. J Parasitol 86:283–288PubMedCrossRefPubMedCentralGoogle Scholar
  84. Thaenkham U, Blair D, Nawa Y, Waikagul J (2012) Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitol Int 61:90–93PubMedCrossRefPubMedCentralGoogle Scholar
  85. Timmermans MJTN, Dodsworth S, Culverwell CL, Bocak L, Ahrens D, Littlewood DTJ, Pons J, Vogler AP (2010) Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Res 38:e197PubMedPubMedCentralCrossRefGoogle Scholar
  86. Tkach VV (2008a) Family Glypthelminthidae Cheng, 1959. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 357–360CrossRefGoogle Scholar
  87. Tkach VV (2008b) Family Haematoloechidae Freitas & Lent, 1939. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 361–366CrossRefGoogle Scholar
  88. Tkach VV (2008c) Family Leptophallidae Dayal, 1938. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 367–371CrossRefGoogle Scholar
  89. Tkach VV (2008d) Family Plagiorchiidae Lühe, 1901. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI and The Natural History Museum, Wallingford and London, pp. 295–325CrossRefGoogle Scholar
  90. Tkach VV, Grabda-Kazubska B, Pawlowski J, Świderski Z (1999) Molecular and morphological evidence for close phylogenetic affinities of the genera Macrodera, Leptophallus, Metaleptophallus and Paralepoderma (Digenea, Plagiorchiata). Acta Parasitol 44:170–179Google Scholar
  91. Tkach VV, Pawlowski J, Mariaux J (2000a) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 30:89–93CrossRefGoogle Scholar
  92. Tkach VV, Pawlowski J, Sharpilo VP (2000b) Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Müller, 1780). Syst Parasitol 47:9–22PubMedCrossRefPubMedCentralGoogle Scholar
  93. Tkach VV, Pawlowski J, Mariaux J, Swiderski Z (2001a) Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor & Francis, London, pp. 186–192Google Scholar
  94. Tkach VV, Grabda-Kazubska B, Świderski Z (2001b) Systematic position and phylogenetic relationships of the family Omphalometridae Odening, 1959 (Digenea, Plagiorchiida) inferred from the partial lsrDNA sequences. Int J Parasitol 31:81–85PubMedCrossRefPubMedCentralGoogle Scholar
  95. Tkach VV, Snyder SD, Swiderski Z (2001c) On the phylogenetic relationships of some members of Macroderoididae and Ochetosomatidae (Digenea, Plagiorchioidea). Acta Parasitol 46:267–275Google Scholar
  96. Tkach VV, Littlewood DTJ, Olson PD, Kinsella JM, Swiderski Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Syst Parasitol 56:1–15PubMedCrossRefPubMedCentralGoogle Scholar
  97. Tkach VV, Kudlai O, Kostadinova A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). Int J Parasitol 46:171–185PubMedCrossRefPubMedCentralGoogle Scholar
  98. Waeschenbach A, Webster BL, Bray RA, Littlewood DTJ (2007) Added resolution among ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with complete small and large subunit nuclear ribosomal RNA genes. Mol Phylogenet Evol 45:311–325PubMedCrossRefPubMedCentralGoogle Scholar
  99. Zamparo D, Brooks DR (2003) Phylogenetic systematic assessment of the Aspidobothrea (Platyhelminthes, Neodermata, Trematoda). Zool Scr 32:83–93CrossRefGoogle Scholar
  100. Zarowiecki MZ, Huyse T, Littlewood DT (2007) Making the most of mitochondrial genomes-markers for phylogeny, molecular ecology and barcodes in Schistosoma (Platyhelminthes: Digenea). Int J Parasitol 37:1401–1148PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of SciencesSofiaBulgaria
  2. 2.Unitat de Zoologia MarinaInstitut Cavanilles de Biodiversitat i Biologia Evolutiva, Parc Científic, Universitat de ValènciaValenciaSpain

Personalised recommendations