Skip to main content

Advertisement

Log in

Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Phylogenetic analyses of a range of gorgoderid trematodes based on ITS2 and partial 28S rDNA data lead us to propose the Degeneriinae n. subfam. for the genus Degeneria in recognition of its phylogenetic isolation and distinctive morphology and biology. The current concepts of the subfamilies Anaporrhutinae and Gorgoderinae were supported. Within the Gorgoderinae, the large genus Phyllodistomum is shown to be paraphyletic relative to Pseudophyllodistomum and Xystretrum. Notably, the clade of marine Phyllodistomum does not form a clade with the other marine genus, Xystretrum. Distinct clades within the Gorgoderinae correspond variously to identity of first intermediate host, form of cercaria and their marine or freshwater habitat. We are not yet in a position to propose separate genera for these clades.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Anderson GR, Barker SC (1998) Inference of phylogeny and taxonomy within the Didymozoidae (Digenea) from the second internal transcribed spaces (ITS2) of ribosomal DNA. Syst Parasitol 41:87–94

    Article  Google Scholar 

  • Bell FJ (1887) Description of a new species of Distomum. Ann Mag Nat Hist Ser 5(19):116–117

    Article  Google Scholar 

  • Bolek MG, Snyder SD, Janovy J (2009) Alternative life cycle strategies and colonization of young anurans by Gorgoderina attenuata in Nebraska. J Parasitol 95:604–616

    Article  PubMed  Google Scholar 

  • Boomker J (1984) Parasites of South African freshwater fish. II. Redescription of the African species of the genus Phyllodistomum Braun, 1899 (Trematoda: Gorgoderinae) and the description of a new species. Onderstepoort J Vet Res 51:129–139

    PubMed  CAS  Google Scholar 

  • Bott NJ, Cribb TH (2005) First report of intramolluscan stages of a gorgoderid digenean from a marine bivalve. J Parasitol 91:838–842

    Article  PubMed  Google Scholar 

  • Bouchet P, Rocroi JP, Bieler R, Carter JG, Coan EV (2010) Nomenclator of bivalve families with a classification of bivalve families. Malacologia 52:4–172

    Article  Google Scholar 

  • Bowles J, Hope M, Tiu WU, Liu XS, McManus DP (1993) Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop 55:217–229

    Article  PubMed  CAS  Google Scholar 

  • Bray RA (2004) The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol 51:268–274

    PubMed  Google Scholar 

  • Bray RA, Blair D (2008) Superfamily Gorgoderoidea Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI, Wallingford, pp 187–190

    Google Scholar 

  • Bray RA, Littlewood DTJ, Herniou EA, Williams B, Henderson RE (1999) Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology 119(Supp):S125–S144

    PubMed  Google Scholar 

  • Brooks DR, MacDonald CA (1986) A new species of Phyllodistomum Braun, 1899 (Digenea: Gorgoderidae) in a neotropical catfish, with discussion of the generic relationships of the Gorgoderidae. Can J Zool 64:1326–1330

    Article  Google Scholar 

  • Campbell RA (1977) Degeneria halosauri (Bell 1887) gen. et comb. n. (Digenea: Gorgoderidae) from the deep-sea teleost Halosauropsis macrochir. J Parasitol 63:76–79

    Article  PubMed  CAS  Google Scholar 

  • Campbell RA (2008) Family Gorgoderidae Looss, 1899. In: Bray RA, Gibson DI, Jones A (eds) Keys to the Trematoda, vol 3. CABI, Wallingford, pp 191–213

    Google Scholar 

  • Choudhury A, Valdez RR, Johnson RC, Hoffmann B, de Leon GPP (2007) The phylogenetic position of Allocreadiidae (Trematoda: Digenea) from partial sequences of the 18S and 28S ribosomal RNA genes. J Parasitol 93:192–196

    Article  PubMed  CAS  Google Scholar 

  • Coil WH (1953) A new gorgoderid cercaria parasitic in Lampsilis ventricosa Barnes. J Parasitol 39:183–186

    Article  PubMed  CAS  Google Scholar 

  • Coil WH (1954a) Contributions to the life cycles of gorgoderid trematodes. Am Midl Nat 52:481–500

    Article  Google Scholar 

  • Coil WH (1954b) Two new rhopalocercariae (Gorgoderinae) parasitic in Lake Erie mussels. Proc Helminthol Soc Wash 21:17–29

    Google Scholar 

  • Cribb TH (1987a) A new species of Phyllodistomum (Digenea: Gorgoderidae) from Australian and New Zealand freshwater fishes with notes on the taxonomy of Phyllodistomum Braun, 1899. J Nat Hist 21:1525–1538

    Article  Google Scholar 

  • Cribb TH (1987b) Studies on gorgoderid digeneans from Australian and Asian freshwater fishes. J Nat Hist 21:1129–1153

    Article  Google Scholar 

  • Cribb TH, Anderson GR, Adlard RD, Bray RA (1998) A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). Int J Parasitol 28:1791–1795

    Article  PubMed  CAS  Google Scholar 

  • Cribb TH, Chisholm LA, Bray RA (2002) Diversity in the Monogenea and Digenea: does lifestyle matter? Int J Parasitol 32:321–328

    Article  PubMed  Google Scholar 

  • Curran SS, Blend CK, Overstreet RM (2009) Nagmia rodmani n. sp., Nagmia cisloi n. sp., and Probolitrema richiardii (Lopez, 1888) (Gorgoderidae: Anaporrhutinae) from elasmobranchs in the Gulf of California, Mexico. Comp Parasitol 76:6–18

    Article  Google Scholar 

  • Curran SS, Tkach VV, Overstreet RM (2006) A review of Polylekithum Arnold, 1934 and its familial affinities using morphological and molecular data, with description of Polylekithum catahoulensis sp nov. Acta Parasitol 51:238–248

    Article  CAS  Google Scholar 

  • Curran SS, Tkach VV, Overstreet RM (2011) Phylogenetic affinities of Auriculostoma (Digenea: Allocreadiidae), with descriptions of two new species from Peru. J Parasitol 97:661–670

    Article  PubMed  Google Scholar 

  • Cutmore SC, Bennett MB, Cribb TH (2010) Staphylorchis cymatodes (Gorgoderidae Anaporrhutinae) from carcharhiniform, orectolobiform and myliobatiform elasmobranchs of Australasia: low host specificity, wide distribution and morphological plasticity. Parasitol Int 59:579–586

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  PubMed  CAS  Google Scholar 

  • Fischthal JH (1951) Rhopalocercariae in the trematode subfamily Gorgoderinae. Am Midl Nat 46:395–443

    Article  Google Scholar 

  • Fischthal JH (1954) Cercaria tiogae Fischthal, 1953, a rhopalocercous form from the clam, Alasmidonta varicosa (Lamarck). T Am Microsc Soc 73:210–215

    Article  Google Scholar 

  • Flook JM, Ubelaker JE (1971) Cercaria amblemae sp. n., a rhopalocercous cercaria from Amblema plicata (Say). Proc Helminthol Soc Wash 38:159–166

    Google Scholar 

  • Goodchild CG (1943) The life-history of Phyllodistomum solidum Rankin, 1937, with observations on the morphology, development and taxonomy of the Gorgoderinae (Trematoda). Biol Bull 84:59–86

    Article  Google Scholar 

  • Goodchild CG (1948) Additional observations on the bionomics and life history of Gorgodera amplicava Looss, 1899 (Trematoda: Gorgoderidae). J Parasitol 34:407–427

    Article  PubMed  CAS  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Krull WH (1935) Studies on the life history of a frog bldder fluke, Gorgodera amplicava Looss, 1899. Pap Mich Acad of Sci Arts Lett 20:697–710

    Google Scholar 

  • Lees E (1953) Life-history of Gorgoderina vitelliloba (Olsson). Nature 4350:485

    Article  Google Scholar 

  • Littlewood DTJ, Curini-Galletti M, Herniou EA (2000) The interrelationships of Proseriata (Platyhelminthes: Seriata) tested with molecules and morphology. Mol Phylogenet Evol 16:449–466

    Article  PubMed  CAS  Google Scholar 

  • Maddison WP, Maddison DR (2009) Mesquite: a modular system for evolutionary analysis. Version 2.72 http://mesquiteproject.org. Accessed 30 June 2012

  • Miller MA, et al. (2009) The CIPRES Portals. CIPRES. 2012-08-04. URL: http://www.phylo.org/sub_sections/portal. (Archived by WebCite(r) at http://www.webcitation.org/5imQlJeQa). Accessed 2012-08-04

  • Molloy DP, Roitman VA, Shields JD (1996) Survey of the parasites of zebra mussels (Bivalvia: Dreissenidae) in northwestern Russia, with comments on records of parasitism in Europe and North America. J Helminthol Soc Wash 63:251–256

    Google Scholar 

  • Mwambungu JA (2004) The diversity of benthic mollusks of Lake Victoria and Lake Burigi. Tanzania J Sci 30:21–32

    Google Scholar 

  • Nagaty HF, Abdel Aal TM (1961) Trematodes of fishes from the Red Sea Part 9. Six new anaporrhutine species including a new genus. J Parasitol 47:765–769

    Article  PubMed  CAS  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    Article  PubMed  CAS  Google Scholar 

  • Orecchia P, Paggi L, Castagnolo L, Della Seta G, Minervini R (1975) Ricerche sperimentali sul ciclo biologico di Phyllodistomum elongatum Nybelin, 1926 (Digenea: Gorgoderidae Looss, 1901). Parassitologia 17:95–101

    PubMed  CAS  Google Scholar 

  • Pandey KC (1970) On a new phyllodistome metacercaria (Phyllodistomum lucknowensis) and its adult. Indian J Zootomy 11:22–35

    Google Scholar 

  • Peribáñez MA, Ordovas L, Benito J, Benejam L, Gracia MJ, Rodellar C (2011) Prevalence and sequence comparison of Phyllodistomum folium from zebra mussel and from freshwater fish in the Ebro River. Parasitol Int 60:59–63

    Article  PubMed  Google Scholar 

  • Petkevičiūtė R, Stunžėnas V, Stanevičiūtė G (2004) Cytogenetic and sequence comparison of adult Phyllodistomum (Digenea: Gorgoderidae) from the three-spined stickleback with larvae from two bivalves. Parasitology 129:771–778

    Google Scholar 

  • Petkevičiūtė R, Stunžėnas V, Stanevičiūtė G, Sokolov SG (2010) Comparison of the developmental stages of some European allocreadiid trematode species and a clarification of their life-cycles based on ITS2 and 28S sequences. Syst Parasitol 76:169–178

    Article  PubMed  Google Scholar 

  • Pleijel F et al (2008) Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol Phylogenet Evol 48:369–371

    Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Google Scholar 

  • Rai SL (1964) Observations on the life-history of Phyllodistomum srivastavai sp. nov. (Trematoda: Gorgoderidae). Parasitology 54:43–51

    Article  Google Scholar 

  • Rankin JS (1939) The life cycle of the frog bladder fluke, Gorgoderina attenuata Stafford, 1902 (Trematoda: Gorgoderidae). Am Midl Nat 21:476–488

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rosas-Valdez R, Choudhury A, De Leon GPP (2011) Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zool Scr 40:296–305

    Article  Google Scholar 

  • Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Schell SC (1967) The life history of Phyllodistomum staffordi Pearse, 1924 (Trematoda: Gorgoderidae Looss, 1901). J Parasitol 53:569–576

    Article  PubMed  CAS  Google Scholar 

  • Sinitsin DF (1905) [Materials on the natural history of trematodes. Distomes of fishes and frogs in the vicinity of Warsaw.]. Izv Varshavskogo Univ 7–9:1–96 (In Russian)

    Google Scholar 

  • Snyder SD, Tkach VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). J Parasitol 87:1433–1440

    PubMed  CAS  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Stunžėnas V, Cryan JR, Molloy DP (2004) Comparison of rDNA sequences from colchicine treated and untreated sporocysts of Phyllodistomum folium and Bucephalus polymorphus (Digenea). Parasitol Int 53:223–228

    Article  PubMed  Google Scholar 

  • Tang CC (1985) [Studies on the life history of Phyllodistomum mingensis sp. nov.]. Acta Zool Sin 31:246–253 (In Chinese)

    Google Scholar 

  • Thomas JD (1958a) Studies on the structure, life history and ecology of the trematode Phyllodistomum simile Nybelin, 1926 (Gorgoderidae: Gorgoderinae) from the urinary bladder of brown trout, Salmo trutta L. P Roy Soc Lond B Bio 130:397–435

    Google Scholar 

  • Thomas JD (1958b) Three new digenetic trematodes, Emoleptalea proteropora, n. sp., (Cephalogonimidae: Cephalogoniminae), Phyllodistomum symmetrorchis, n. sp., and Phyllodistomum ghanense, n. sp., (Gorgoderidae: Gorgoderinae) from West African freshwater fishes. Proc Helminthol Soc Wash 25:1–8

    Google Scholar 

  • Tkach VV, Pawlowski J, Mariaux J (2000) Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 30:83–93

    Article  PubMed  CAS  Google Scholar 

  • Tkach VV, Pawlowski J, Mariaux J, Swiderski Z (2001) 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 186–193

    Google Scholar 

  • Ubelaker JE, Olsen OW (1972) Life cycle of Phyllodistomum bufonis (Digenea: Gorgoderidae) from the boreal toad, Bufo boreas. Proc Helminthol Soc Wash 39:94–100

    Google Scholar 

  • Wanson WW, Larson OR (1972) Studies on helminths of North Dakota. V. Life history of Phyllodistomum nocomis Fischthal, 1942 (Trematoda: Gorgoderidae). J Parasitol 58:1106–1109

    Article  PubMed  CAS  Google Scholar 

  • Wu K (1938) Progenesis of Phyllodistomum lesteri sp. nov. (Trematoda: Gorgoderidae) in freshwater shrimps. Parasitology 30:4–19

    Article  Google Scholar 

  • Yamaguti S (1934) Studies on the helminth fauna of Japan. Part 2. Trematodes of fishes, I. Jpn J Zool 5:249–541

    Google Scholar 

Download references

Acknowledgments

We thank John Page and Vivian Geow and Drs. Rob Adlard, Nathan Bott, Rod Bray and Stephen Taylor for their assistance in the collection of specimens in Australia and Caleb Olgawi for help in Africa. We thank Sea World Research and Rescue Foundation and the Tangalooma Wild Dolphin Resort for support of a broader project, of which this was a part. We also thank the staff of the Sea Turtle Stranding Response Program of the Virginia Aquarium and Marine Science Center for generously allowing us to collect specimens from a loggerhead turtle that had died during post-trauma rehabilitation. Collecting in Australian waters was funded in part by the Australian node of the CReefs global research initiative, a partnership between the Australian Biological Resource Study (ABRS), BHP Billiton, the Great Barrier Reef Foundation, the Census of Marine Life and the Australian Institute of Marine Science (AIMS). The CReefs Australia Project is generously sponsored by BHP Billiton in partnership with The Great Barrier Reef Foundation, the Australian Institute of Marine Science, the Australian Biological Resources Study and the Alfred P. Sloan Foundation. Collecting in French Polynesia was supported by the BioCode, Coral Spot program (financially supported by the French Polynesian Territory and the French Government) and Pakaihi ite Moana in Marquesas (financially supported by AAMP, by the French Polynesian Territory and the French Government).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Scott C. Cutmore.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cutmore, S.C., Miller, T.L., Curran, S.S. et al. Phylogenetic relationships of the Gorgoderidae (Platyhelminthes: Trematoda), including the proposal of a new subfamily (Degeneriinae n. subfam.). Parasitol Res 112, 3063–3074 (2013). https://doi.org/10.1007/s00436-013-3481-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3481-5

Keywords

Navigation