Folia Parasitologica, vol. 61 (2014), issue 3

Folia Parasitologica 61[3] 223-230 (2014) | 10.14411/fp.2014.033

New genus of opecoelid trematode from Pristipomoides aquilonaris (Perciformes: Lutjanidae) and its phylogenetic affinity within the family Opecoelidae

Michael J. Andres, Eric E. Pulis, Robin M. Overstreet
Department of Coastal Sciences, University of Southern Mississippi, Ocean Springs, Mississippi, USA

Bentholebouria colubrosa gen. n. et sp. n. (Digenea: Opecoelidae) is described in the wenchman, Pristipomoides aquilonaris (Goode et Bean), from the eastern Gulf of Mexico, and new combinations are proposed: Bentholebouria blatta (Bray et Justine, 2009) comb. n., Bentholebouria longisaccula (Yamaguti, 1970) comb. n., Bentholebouria rooseveltiae (Yamaguti, 1970) comb. n., and Bentholebouria ulaula (Yamaguti, 1970) comb. n. The new genus is morphologically similar to Neolebouria Gibson, 1976, but with a longer cirrus sac, entire testes, a rounded posterior margin with a cleft, and an apparent restriction to the deepwater snappers. Morphologically, the new species is closest to B. blatta from Pristipomoides argyrogrammicus (Valenciennes) off New Caledonia but can be differentiated by the nature of the internal seminal vesicle (2-6 turns or loops rather than constrictions), a longer internal seminal vesicle (occupying about 65% rather than 50% of the cirrus sac), a cirrus sac that extends further into the hindbody (averaging 136% rather than 103% of the distance from the posterior margin of the ventral sucker to the ovary), and a narrower body (27% rather than 35% mean width as % of body length). A Bayesian inference analysis of partial sequence of the 28S rDNA from Neolebouria lanceolata (Price, 1934), Cainocreadium lintoni (Siddiqi et Cable, 1960), Hamacreadium mutabile Linton, 1910, Opecoeloides fimbriatus (Linton, 1910), Podocotyloides brevis Andres et Overstreet, 2013, the new species, and previously published comparable sequences from 10 opecoelid species revealed two clades. One clade includes deep-sea (≥ 200 m) and freshwater fish opecoelids + Opecoeloides Bremser in Rudolphi, 1819, and a second clade included those opecoelids from shallow-water marine, perciform fishes.

Keywords: Digenea, molecular phylogeny, 28S rDNA, Neolebouria, Macvicaria, Hamacreadium, fishes, deep-sea

Received: November 26, 2013; Accepted: January 24, 2014; Prepublished online: March 19, 2014; Published: June 19, 2014


References

  1. Andres M.J., Overstreet R.M. 2013: A new species of Podocotyloides (Digenea: Opecoelidae) from the grey conger eel, Conger esculentus, in the Caribbean Sea. J. Parasitol. 99: 619-623 Go to original source... Go to PubMed...
  2. Born-Torrijos A., Kostadinova A., Raga J.A., Holzer A.S. 2012: Molecular and morphological identification of larval opecoelids (Digenea: Opecoelidae) parasitizing prosobranch snails in a Western Mediterranean lagoon. Parasitol. Int. 61: 450-460 Go to original source... Go to PubMed...
  3. Brandt A., Gooday A.J., Brandao S.N., Brix S., Broekeland W., Cedhagen T., Choudhury M., Cornelius N., Danis B., De Mesel I., Diaz R.J., Gillan D.C., Ebbe B., Howe J.A., Janussen D., Kaiser S., Linse K., Malyutina M., Pawlowski J., Raupach M., Vanreusel A. 2007: First insights into the biodiversity and biogeography of the Southern Ocean deep sea. Nature 447: 307-311 Go to original source... Go to PubMed...
  4. Bray R.A. 2004: The bathymetric distribution of the digenean parasites of deep-sea fishes. Folia Parasitol. 51: 268-274 Go to original source... Go to PubMed...
  5. Bray R.A., Campbell R.A. 1996: New plagioporines (Digenea: Opecoelidae) from deep-sea fishes of the Northern Atlantic Ocean. Syst. Parasitol. 33: 101-113 Go to original source...
  6. Bray R.A., Cribb T.H. 2012: Reorganisation of the superfamily Lepocreadioidea Odhner, 1905 based on an inferred molecular phylogeny. Syst. Parasitol. 83: 169-177 Go to original source... Go to PubMed...
  7. Bray R.A., Justine J.-L. 2009a: Neolebouria blatta n. sp. (Digenea: Opecoelidae) from Pristipomoides argyrogrammicus(Valenciennes) and Etelis carbunculus Cuvier (Perciformes: Lutjanidae) off New Caledonia. Syst. Parasitol. 74: 161-167 Go to original source... Go to PubMed...
  8. Bray R.A., Justine J.-L. 2009b: Opecoelids (Platyhelminthes, Digenea) from the fork-tailed threadfin bream Nemipterus furcosus (Valenciennes, 1830) (Perciformes, Nemipteridae), with preliminary keys to the problematic genera Macvicaria Gibson et Bray, 1982 and Neolebouria Gibson, 1976. Acta Parasitol. 54: 218-229 Go to original source...
  9. Bray R.A., Littlewood D.T.J., Herniou E.A., Williams B., Henderson R.E. 1999: Digenean parasites of deep-sea teleosts: a review and case studies of intrageneric phylogenies. Parasitology 119: S125-S144 Go to original source... Go to PubMed...
  10. Bray R.A., Waeschenbach A., Cribb T.H., Weedall G.D., Dyal P., Littlewood D.T.J. 2009: The phylogeny of the Lepocreadioidea (Platyhelminthes, Digenea) inferred from nuclear and mitochondrial genes: implications for their systematics and evolution. Acta Parasitol. 54: 310-329 Go to original source...
  11. Cribb T.H. 2005: Family Opecoelidae Ozaki, 1925. In: A. Jones, R.A. Bray and D.I. Gibson (Eds.), Keys to the Trematoda. Volume 2. CABI Publishing and the Natural History Museum, London, pp. 443-539
  12. Curran S.S., Overstreet R.M., Tkach V.V. 2007: Phylogenetic affinities of Plagiocirrus Van Cleave and Mueller, 1932 with the description of a new species from the Pascagoula River, Mississippi. J. Parasitol. 93: 1452-1458 Go to original source...
  13. Curran S.S., Tkach V.V., Overstreet R.M. 2013: A new species of Homalometron (Digenea: Apocreadiidae) from fishes in the northern Gulf of Mexico. J. Parasitol. 99: 93-101 Go to original source... Go to PubMed...
  14. Detwiler J.T., Bos D.H., Minchella D.J. 2010: Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Mol. Phylogenet. Evol. 55: 611-620 Go to original source... Go to PubMed...
  15. Etter R.J., Boyle E.E., Glazier A., Jennings R.M., Dutra E., Chase M.R. 2011: Phylogeography of a pan-Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic. Mol. Ecol. 20: 829-843 Go to original source... Go to PubMed...
  16. Fischer P.U., Curtis K.C., Marcos L.A., Weil G.J. 2011: Molecular characterization of the North American lung fluke Paragonimus kellicotti in Missouri and its development in Mongolian gerbils. Am. J. Trop. Med. Hyg. 84: 1005-1011 Go to original source... Go to PubMed...
  17. Gage J.D. 2004: Diversity in deep-sea benthic macrofauna: the importance of local ecology, the larger scale, history and the Antarctic. Deep-Sea Res. II 51: 1689-1708
  18. Gibson D.I. 1976: Monogenea and Digenea from fishes. Discovery Rep. 36: 179-266
  19. Gibson D.I., Bray R.A. 1982: A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. J. Nat. Hist. 16: 529-559 Go to original source...
  20. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Res. 41: 95-98
  21. Huelsenbeck J. P., Ronquist F. 2001: MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17: 754-755 Go to original source... Go to PubMed...
  22. 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 Go to original source... Go to PubMed...
  23. Jousson O., Bartoli P., Pawlowski J. 1999: Molecular identification of developmental stages in Opecoelidae (Digenea). Int. J. Parasitol. 29: 1853-1858 Go to original source... Go to PubMed...
  24. 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 Go to original source...
  25. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. 2007: Clustal W and Clustal X version 2.0. Bioinfromatics 23: 2947-2948 Go to original source...
  26. Manter H.W. 1966: Parasites of fishes as biological indicators of recent and ancient conditions. In: J.E. McCauley (Ed.), Host-Parasite Relationships. Oregon State University Press, Corvallis, Oregon, pp. 59-71
  27. Miller T.L., Cribb T.H. 2007: Two new cryptogonimid genera (Digenea, Cryptogonimidae) from Lutjanus bohar (Perciformes, Lutjanidae): analyses of ribosomal DNA reveals wide geographic distribution and presence of cryptic species. Acta Parasitol. 52: 104-113 Go to original source...
  28. Olson P.D., Cribb T.H., Tkach V.V., Bray R.A., Littlewood D.T.J. 2003: Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int. J. Parasitol. 33: 733-755 Go to original source... Go to PubMed...
  29. Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P., Thollesson M. 2008: Phylogenies without roots? A plea for the use of vouchers in molecular phylogenetic studies. Mol. Phylogenet. Evol. 48: 369-371 Go to original source... Go to PubMed...
  30. Posada D. 2008: jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256 Go to original source... Go to PubMed...
  31. Poulin R. 2011: Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biol. Lett. 7: 241-244 Go to original source... Go to PubMed...
  32. Price E.W. 1934: New digenetic trematodes from marine fishes. Smithson. Misc. Collect. 91: 1-8
  33. Reimer L.W. 1987: Opecoelidae (Trematoda) von Meeresfischen vor Mocambique. Angew. Parasitol. 28: 148-158
  34. Ronquist F., Huelsenbeck J. P. 2003: MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574 Go to original source... Go to PubMed...
  35. Shimazu T. 1990: Trematodes of a new genus, Neoplagioporus gen. n. (Digenea: Opecoelidae: Plagioporinae), and an unidentified opecoelid from freshwater fishes of Japan. Jpn. J. Parasitol. 39: 384-396
  36. Shimazu T., Nagasawa K. 1985: Trematodes of marine fishes from Moroiso Bay, Misaki, Kanagawa Prefecture, Japan. J. Nagano-ken Junior College 40: 7-15
  37. Tkach V.V., Littlewood D.T.J., Olson P.D., Kinsella J.N., 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.V., Pawlowski J., Mariaux, J. 2000: Phylogenetic analysis of the suborder Plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int. J. Parsitol. 30: 83-93 Go to original source...
  39. Tkach V.V., Pawlowski J., Mariaux J., Swiderski Z. 2001: Molecular phylogeny of the suborder Plagiorchiata and its position in the system of Digenea. In: D.T.J. Littlewood and R.A. Bray (Eds.), Interrelationships of the Platyhelminthes. Taylor and Francis, London, pp. 186-193
  40. Yamaguti S. 1970: Digenetic trematodes of Hawaiian fishes. Keigaku, Tokyo, pp. 436
  41. Zdzitowiecki K. 1988: Occurrence of digenetic trematodes in fishes off South Shetlands (Antarctic). Acta Parasitol. Pol. 33: 155-167
  42. Zdzitowiecki K. 1990: Reexamination of five Antarctic and subantarctic digenean and acanthocephalan species from Professor Szidat's collection. Acta Parasitol. Pol. 35: 31-36
  43. Zdzitowiecki K. 1991: Occurrence of digeneans in open sea fishes off the South Shetland Islands and South Georgia, and a list of fish digeneans in the Antarctic. Pol. Polar Res. 12: 55-72