Molecular systematics of pinniped hookworms (Nematoda: Uncinaria): Species delimitation, host associations and host-induced morphometric variation

International Journal for Parasitology

Volumn 43, Issue 14, 2013, Pages 1119-1132

  Nadler, Steven A ^a   Lyons, Eugene T ^b   Pagan, Christopher ^a   Hyman, Derek ^a   Lewis, Edwin E ^a   Beckmen, Kimberlee ^c   Bell, Cameron M ^d   Castinel, Aurelie ^e   DeLong, Robert L ^f   Duignan, Padraig J ^g   Farinpour, Cher ^a   Huntington, Kathy Burek ^d   Kuiken, Thijs ^h   Morgades, Diana ⁱ   Naem, Soraya ^j   Norman, Richard ^k   Parker, Corwin ^a   Ramos, Paul ^k,l   Spraker, Terry R ^m   Berón Vera, Bárbara ⁿ  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c ALASKA DEPARTMENT OF FISH AND GAME   (United States)

^d Department of Environment and Primary Industries ^*  (United States)

^e CAWTHRON INSTITUTE   (New Zealand)

^f NOAA National Marine Mammal Laboratory   (United States)

^g UNIVERSITY OF CALGARY   (Canada)

^h ERASMUS MEDICAL CENTER   (Netherlands)

ⁱ UNIVERSIDAD DE LA REPÚBLICA   (Uruguay)

^j URMIA UNIVERSITY   (Iran)

^k UNIVERSITY OF MELBOURNE   (Australia)

^l ZOOS VICTORIA   (Australia)

^m Department of Environmental and Radiological Health Sciences   (United States)

ⁿ Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

more..

Author keywords

Cophylogeny; Hookworm; Molecular systematics; Morphometrics; Phylogenetics; Pinniped; Species

Indexed keywords

MITOCHONDRIAL DNA; RIBOSOME DNA;

DNA; GROWTH RESPONSE; HOST-PARASITE INTERACTION; INTRASPECIFIC INTERACTION; JUVENILE; MITOCHONDRIAL DNA; MOLECULAR ANALYSIS; MORPHOMETRY; PARASITE; PHYLOGENETICS; PINNIPED; TAXONOMY;

ARCTOCEPHALUS AUSTRALIS; ARCTOCEPHALUS PUSILLUS; ARTICLE; CALLORHINUS URSINUS; CLADISTICS; CONTROLLED STUDY; GENE LOCUS; HOST PARASITE INTERACTION; MIROUNGA LEONINA; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MONACHUS MONACHUS; MORPHOMETRICS; NONHUMAN; NUCLEOTIDE SEQUENCE; OTARIA FLAVESCENS; PHOCARCTOS HOOKERI; PHYLOGENETIC TREE; SEAL; SEQUENCE ANALYSIS; UNCINARIA; UNCINARIA HAMILTONI; UNINDEXED SEQUENCE; ZALOPHUS CALIFORNIANUS;

ANCYLOSTOMATOIDEA; ARCTOCEPHALUS AUSTRALIS; ARCTOCEPHALUS PUSILLUS; ARCTOCEPHALUS PUSILLUS DORIFERUS; CALLORHINUS; CALLORHINUS URSINUS; EUMETOPIAS JUBATUS; MIROUNGA LEONINA; MONACHUS MONACHUS; NEMATODA; OTARIA BYRONIA; PHOCARCTOS HOOKERI; PINNIPEDIA; UNCINARIA; UNCINARIA HAMILTONI; UNCINARIA LUCASI; ZALOPHUS; ZALOPHUS CALIFORNIANUS;

COPHYLOGENY; HOOKWORM; MOLECULAR SYSTEMATICS; MORPHOMETRICS; PHYLOGENETICS; PINNIPED; SPECIES;

ANCYLOSTOMATOIDEA; ANIMALS; BIOMETRY; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL; FEMALE; MALE; MOLECULAR SEQUENCE DATA; PHYLOGEOGRAPHY; PINNIPEDIA; SEQUENCE ANALYSIS, DNA;

EID: 84888434039     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.08.006     Document Type: Article

References (53)

1. Acevedo-Whitehouse K., Spraker T.R., Lyons E., Melin S.R., Gulland F., Delong R.L., Amos W. Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups. Mol. Ecol. 2006, 15:1973-1982.
2. Acevedo-Whitehouse K., Petetti L., Duignan P., Castinel A. Hookworm infection, anaemia and genetic variability of the New Zealand sea lion. Proc. R. Soc. Lond. Ser. B 2009, 276:3523-3529.
3. Adams B.J. Species concepts and the evolutionary paradigm in modern nematology. J. Nematol. 1998, 30:1-21.
4. Adams B.J. The species delimitation uncertainty principle. J. Nematol. 2002, 33:153-160.
5. Alfaro M.E., Zoller S., Lutzoni F. Bayes or Bootstrap? A simulation study comparing the performance of Bayesian Markov chain Monte Carlo sampling and bootstrapping in assessing phylogenetic confidence. Mol. Biol. Evol. 2003, 20:255-266.
6. Avise J.C. Molecular Markers, Natural History and Evolution 1994, Chapman and Hall, New York and London.
7. Baldwin J.G., Nadler S.A., Freckman D.W. Nematodes - pervading the earth and linking all life. Proceedings of the Second National Forum on Biodiversity, Nature and Human Society: The Quest for a Sustainable World 1999, 176-191. National Academy Press, Washington. P.H. Raven, T. Williams (Eds.).
8. Baylis H.A. A new species of the nematode genus Uncinaria from a sea-lion, with some observations on related species. Parasitology 1933, 25:308-316.
9. Baylis H.A. A redescription of Uncinaria lucasi Stiles, a hookworm of seals. Parasitology 1947, 38:160-162.
10. Berón-Vera B., Crespo E.A., Raga J.A., Pedraza S.N. Uncinaria hamiltoni (Nematoda: Ancylostomatidae) in South American sea lions, Otaria flavescens, from Northern Patagonia, Argent. J. Parasitol. 2004, 90:860-863.
11. Beveridge I. Uncinaria hydromidis sp. N. (Nematoda: Ancylostomatidae) from the Australian water rat, Hydromis chrysogaster. J. Parasitol. 1980, 66:1027-1031.
12. Botto C., Mañé-Garzón F. Sobre una nueva especie del género Uncinaria (Nematoda, Strongyloidea) de Otaria flavescens Shaw y la especiación en el género Uncinaria en pinnípedos americanos. Rev. Biol. Urug. 1975, II:127-141.
13. Castinel A., Duignan P.J., Pomroy W.E., Lyons E.T., Nadler S.A., Dailey M.D., Wilkinson I.S., Chilvers B.L. First report and characterization of adult Uncinaria spp. in New Zealand Sea Lion (Phocarctos hookeri) pups from the Auckland Islands, New Zealand. Parasitol. Res. 2006, 98:304-309.
14. Dailey M.D. The distribution and intraspecific variation of helminth parasites in pinnipeds. Rapp. P.-V. Réun. Cons. Int. Explor. Mer. 1975, 169:335-338.
15. Dailey M.D. Parasitic diseases. CRC Handbook of Marine Mammal Medicine 2001, 357-379. CRC Press, Boca Raton. second ed. L.A. Dierauf, F.M.D. Gulland (Eds.).
16. Dailey M.D., Hill B.L. A survey of metazoan parasites infecting the California (Zalophus californianus) and Steller (Eumetopias jubatus) sea lion. Bull. South. Calif. Acad. Sci. 1970, 69:126-132.
17. De Ley P. Lost in worm space: phylogeny and morphology as road maps to nematode diversity. Nematology 2000, 2:9-16.
18. Floyd R., Abebe E., Papert A., Blaxter M. Molecular barcodes for soil nematode identification. Mol. Ecol. 2002, 11:839-850.
19. George-Nascimento M., Lima M., Ortiz E. Phenotypic differentiation among hookworms Uncinaria sp. (Nematoda: Ancylostomatidae) in sympatric and allopatric populations of South American sea lions Otaria byronia, and fur seals Arctocephalus australis (Carnivora: Otariidae). Mar. Biol. 1992, 112:527-533.
20. Higdon J.W., Bininda-Emonds O.R.P., Beck R.M.D., Ferguson S.H. Phylogeny and divergence of the pinnipeds (Carnivora: Mammalia) assessed using a multigene dataset. BMC Evol. Biol. 2007, 7:216.
21. Hoberg E.P. Congruent and synchronic patterns in biogeography and speciation among seabirds, pinnipeds and cestodes. J. Parasitol. 1992, 78:601-615.
22. Hoberg E.P., Adams A. Phylogeny, history and biodiversity: understanding faunal structure and biogeography in the marine realm. Bull. Scand. Soc. Parasitol. 2000, 10:19-37.
23. Hoberg E.P., Brooks D.R. Beyond vicariance: integrating taxon pulses, ecological fitting and oscillation in historical biogeography and evolution. The Geography of Host-Parasite Interactions 2010, 7-20. Oxford University Press, Oxford. S. Morand, B.R. Krasnov (Eds.).
24. Hoberg E.P., Klassen G.J. Revealing the faunal tapestry: co-evolution and historical biogeography of hosts and parasites in marine systems. Parasitology 2002, 124:S3-S22.
25. Huelsenbeck J.P., Ronquist F. MRBAYES: Bayesian inference of phylogeny. Bioinformatics 2001, 17:754-755.
26. Johnston T.H., Mawson P.M. Parasitic nematodes. BANZ Antarct. Res. Exped. Ser. B 1945, 73:160.
27. Kluge A.G. Total evidence or taxonomic congruence: cladistics or consensus classification. Cladistics 1998, 14:151-158.
28. Lyons E.T., Biggs M.A. On the longevity of larvae of the hookworm Uncinaria lucasi in tissues of northern fur seals (Callorhinus ursinus). J. Parasitol. 1983, 69:442-443.
29. Lyons E.T., Keyes M.C. Observations on the infectivity of parasitic third-stage larvae of Uncinaria lucasi Stiles 1901 (Nematoda: Ancylostomatidae) of Northern fur seals, Callorhinus ursinus Linn., on St. Paul Island, Alaska. J. Parasitol. 1978, 64:454-458.
30. Lyons E.T., Keyes M.C. Further indication of viability of larvae of the hookworm (Uncinaria lucasi) for several years in tissues of Northern fur seals (Callorhinus ursinus). J. Parasitol. 1984, 70:459-460.
31. Lyons E.T., DeLong R.L., Melin S.R., Tolliver S.C. Uncinariasis in northern fur seal and California sea lion pups from California. J. Wildl. Dis. 1997, 33:848-852.
32. Lyons E.T., Melin S.R., DeLong R.L., Orr A.J., Gulland F.M., Tolliver S.C. Current prevalence of adult Uncinaria spp. in northern fur seal (Callorhinus ursinus) and California sea lion (Zalophus californianus) pups on San Miguel Island, California, with notes on the biology of these hookworms. Vet. Parasitol. 2001, 97:309-318.
33. Lyons E.T., Delong R.L., Spraker T.R., Melin S.R., Laake J.L., Tolliver S.C. Seasonal prevalence and intensity of hookworms (Uncinaria spp.) in California sea lion (Zalophus californianus) pups born in 2002 on San Miguel Island, California. Parasitol. Res. 2005, 96:127-132.
34. Nadler S.A. Molecular approaches to studying helminth population genetics and phylogeny. Int. J. Parasitol. 1990, 20:11-29.
35. Nadler S.A. Species delimitation and nematode biodiversity: phylogenies rule. Nematology 2002, 4:615-625.
36. Nadler S.A., Pérez-Ponce de León G. Cryptic species of parasites: implications for research programs in parasitology. Parasitology 2011, 138:1688-1709.
37. Nadler S.A., Adams B.J., Lyons E.T., DeLong R.L., Melin S.R. Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: hypothesis testing supplants verification. J. Parasitol. 2000, 86:1099-1106.
38. Naem S., Pagan C., Nadler S.A. Structural restoration of nematodes fixed in high percentage alcohol using DESS solution and rehydration. J. Parasitol. 2010, 96:809-811.
39. Olsen, O.W., 1952. Report on investigations of hookworms, Uncinaria lucasi Stiles, 1901, and hookworm disease of fur seals, Callorhinus ursinus Linn. on the Pribilof Islands, Alaska from July 7 to September 2, 1951. With a supplementary report by Jellison WL, U.S. Fish and Wildlife Service, Washington, DC.
40. Olsen, O.W., 1958. Hookworms, Uncinaria lucasi Stiles, 1901, in fur seals, Callorhinus ursinus (Linn.), on the Pribilof Islands. Twenty-third North American Wildlife Conference, Wildlife Management Institute, Washington, D.C., pp. 152-175.
41. Olsen O.W., Lyons E.T. Life cycle of Uncinaria lucasi Stiles, 1901 (Nematoda: Ancylostomatidae) of fur seals, Callorhinus ursinus Linn., on the Pribilof Islands, Alaska. J. Parasitol. 1965, 51:689-700.
42. Pérez-Ponce de León G., Nadler S.A. Critical Comment. What we don't recognize can hurt us: a plea for awareness about cryptic species. J. Parasitol. 2010, 96:453-464.
43. Posada D., Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
44. Ramos P., Lynch M., Hu M., Arnould J.P.Y., Norman R., Beveridge I. Morphometric and molecular characterization of the species of Uncinaria Frölich, 1789 (Nematoda) parasitic in the Australian fur seal Arctocephalus pusillus doriferus (Schreber), with notes on hookworms in three other pinniped hosts. Syst. Parasitol. 2013, 85:65-78.
45. SAS Institute Inc. 2010. SAS/STAT® 9.22 User's Guide. SAS Institute Inc., Cary, NC.
46. Sepúlveda M.D. Hookworms (Uncinaria sp.) in Juan Fernandez fur seal pups (Arctocephalus philippi) from Alejandro Selkirk Island, Chil. J. Parasitol. 1998, 84:1305-1307.
47. Spraker T.R., Lyons E.T., DeLong R.L., Zink R.R. Penetration of the small intestine of a California sea lion (Zalophus californianus) pup by adult hookworms (Uncinaria spp). Parasitol. Res. 2004, 92:436-438.
48. Spraker T.R., DeLong R.L., Lyons E.T., Melin S.R. Hookworm enteritis with bacteremia in California sea lion pups on San Miguel Island. J. Wildl. Dis. 2007, 43:179-188.
49. Stiles C.W. Uncinariasis (Anchylostomiasis) in man and animals in the United States. Texas Med. News 1901, 10:523-532.
50. *and Other Methods) 1998, Sinauer Associates, Sunderland. 4 ed.
51. Thomas W.K., Wilson A.C. Mode and tempo of molecular evolution in the nematode Caenorhabditis: cytochrome oxidase II and calmodulin sequences. Genetics 1991, 128:269-279.
52. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25:4876-4882.
53. Vilas R., Criscione C.D., Blouin M.S. A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 2005, 131:1-8.