Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology

Trends in Parasitology

Volumn 29, Issue 9, 2013, Pages 449-459

  Brant, Sara V ^a   Loker, Eric S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Evolution; Life cycle; Parasite; Phylogeny; Schistosomatidae

Indexed keywords

INTERNAL TRANSCRIBED SPACER;

BIOMPHALARIA; BODY BUILD; CHARADRIIFORMES; CLADISTICS; DIOECY; EGG LAYING; FRESHWATER ENVIRONMENT; GENETIC VARIABILITY; HABITAT; HOST PARASITE INTERACTION; HOST RANGE; HOST RESISTANCE; IMMUNE RESPONSE; INTERMEDIATE HOST; LIFE CYCLE; MARINE ENVIRONMENT; MICROBIAL DIVERSITY; NONHUMAN; ONCOMELANIA; OOCYTE TRANSPORT; PARASITE TRANSMISSION; PATHOGENICITY; PHYLOGENETIC TREE; PHYLOGENY; REVIEW; SCHISTOSOMA; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; SEX DIFFERENCE; TREMATODIASIS;

AVES; GASTROPODA; SCHISTOSOMA; SCHISTOSOMATIDAE; VERTEBRATA;

EID: 84882883628     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2013.06.004     Document Type: Review

References (89)

1. Loker E.S., Brant S.V. Diversification, dioecy and dimorphism in schistosomes. Trends Parasitol. 2006, 22:521-528.
2. Gryseels B. Schistosomiasis. Infect. Dis. Clin. North Am. 2012, 26:383-397.
3. Kolářová L. Schistosomes causing cercarial dermatitis: a mini-review of current trends in systematics and a host specificity and pathogenicity. Folia Parasitol. (Praha) 2007, 54:81-87.
4. Soldánová M., et al. Swimmer's itch: etiology, impact, and risk factors in Europe. Trends Parasitol. 2013, 29:65-74.
5. Snyder S.D., Loker E.S. Evolutionary relationships among the Schistosomatidae (Platyhelminthes:Digenea) and an Asian origin for Schistosoma. J. Parasitol. 2000, 86:283-288.
6. Khalil L.F. Schistosomatoidea. Keys to the Trematoda 2002, 419-432. CABI Publishing. D.I. Gibson (Ed.).
7. Lockyer A.E., et al. The phylogeny of the Schistosomatidae based on three genes with emphasis on the interrelationships of Schistosoma Weinland, 1858. Parasitology 2003, 126:203-224.
8. McLaren D.J., Hockley D.J. Blood flukes have a double outer membrane. Nature 1977, 269:147-149.
9. Aldhoun J.A., Littlewood D.T.J. Orientobilharzia Dutt & Srivastava, 1955 (Trematoda: Schistosomatidae), a junior synonym of Schistosoma Weinland, 1858. Syst. Parasitol. 2012, 82:81-88.
10. Kolářová L., et al. Allobilharzia visceralis gen. nov., sp. nov. (Schistosomatidae-Trematoda) from Cygnus cygnus (L.) (Anatidae). Parasitol. Int. 2006, 55:179-186.
11. Brant S.V., et al. Anserobilharzia gen. n. (Digenea, Schistosomatidae) and redescription of A. brantae (Farr & Blankemeyer, 1956) comb. n. (syn. Trichobilharzia brantae), a parasite of geese (Anseriformes). Zootaxa 2013, 3670:193-206.
12. Al-Kandari W.Y., et al. Molecular identification of Austrobilharzia species parasitizing Cerithidea cingulata (Gastropoda: Potamididae) from Kuwait Bay. J. Helminthol. 2012, 86:470-478.
13. Brant S.V., et al. Cercarial dermatitis transmitted by an exotic marine snail. Emerg. Infect. Dis. 2010, 16:1357-1365.
14. Leigh W.H. The morphology of Gigantobilharzia huttoni (Leigh, 1953) an avian schistosome with marine dermatitis-producing cercariae. J. Parasitol. 1955, 44:262-269.
15. Ponder W.F., Linderg D.R. Towards a phylogeny of gastropod molluscs: an analysis using morphological features. Zool. J. Linn. Soc. 1997, 119:83-265.
16. Badger L.I., Oyerinde J.P.O. Effect of aestivation of Biomphalaria pfeifferi on the survival and infectivity of Schistosoma mansoni cercariae. Br. J. Biomed. Sci. 2004, 61:138-141.
17. Blair D., et al. Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 2001, 123:S229-S243.
18. Horák P., et al. Biology of the schistosome genus Trichobilharzia. Adv. Parasitol. 2002, 52:155-233.
19. Vogel H., Minning W. Bilharziose bei Elefanten. Arch. Schiff. Tropenhyg. 1940, 44:562-574.
20. Miller H.M., Northup F.E. The seasonal infestations of Nassa obsoleta (Say) with larval trematodes. Biol. Bull. 1926, 50:490-509.
21. Penner L.R. The biology of a marine dermatitis producing schistosome cercaria from Batillaria minima. J. Parasitol. 1953, 39:19-20.
22. Chu G.W.T.C., Cutress C.E. Austrobilharzia variglandis (Miller and Northup, 1926) Penner, 1953, (Trematoda: Schistosomatidae) in Hawaii with notes on its biology. J. Parasitol. 1954, 40:515-524.
23. Karamian M., et al. Parasitological and molecular study of the furcocercariae from Melanoides tuberculata as a probable agent of cercarial dermatitis. Parasitol. Res. 2011, 108:955-962.
24. Leedom W.S., Short R.B. Cercaria pomaceae sp. n., a dermatitis-producing schistosome cercaria from Pomacea paludosa, the Florida apple snail. J. Parasitol. 1981, 67:257-261.
25. Szidat L. Investigaciones sobre Cercaria chascomusi n.sp. agente causal de una nueva enfermedad humana en la Argentina: 'La Dermatitis de los banistas de la laguna Chascomus'. Bol. Mus. Argent. Cienc. Nat. 1958, 18:1-13.
26. Ito J. Studies on the morphology and life cycle of Pseudobilharziella corvi Yamaguti, 1941 (Trematoda: Schistosomatidae). Jpn. J. Med. Sci. Biol. 1960, 13:53-58.
27. Aldhoun J.A., et al. Schistosomes in the north: a unique finding from a prosobranch snail using molecular tools. Parasitol. Int. 2009, 58:314-317.
28. Brant S.V., et al. An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. J. Parasitol. 2006, 92:77-88.
29. Brant S.V., Loker E.S. Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J. Parasitol. 2009, 95:941-963.
30. Martorelli S.R. Sobre una cercaria de la familia Schistosomatidae (Digenea) parasita de Chilina gibbosa Sowerby, 1841 en el Lago Pellegrini, Provincia de Rio Negro, Republica Argentina. Neotropica 1984, 30:97-106.
31. Ewers W.H. A new intermediate host of schistosome trematodes from New South Wales. Nature 1961, 190:283-284.
32. Brant S.V. The occurrence of the avian schistosome Allobilharzia visceralis Kolářová, Rudolfová, Hampl et Skírnisson, 2006 (Schistosomatidae) in the tundra swan, Cygnus columbianus (Anatidae), from North America. Folia Parasitol. (Praha) 2007, 54:99-104.
33. Brant S.V., Loker E.S. Schistosomes in the southwest United States and their potential for causing cercarial dermatitis or 'swimmer's itch. J. Helminthol. 2009, 83:191-198.
34. Brant S.V., et al. New intermediate host records for the avian schistosomes Dendritobilharzia pulverulenta, Gigantobilharzia huronensis and Trichobilharzia querquedulae from North America. J. Parasitol. 2011, 97:946-949.
35. Combes C. Atlas mondial des cercaires. Mem. Mus. Natl. d'Hist. Nat. Ser. A: Zool. 1980, 115:1-235.
36. Snyder S.D. Phylogeny and paraphyly among tetrapod blood flukes (Digenea: Schistosomatidae and Spirorchiidae). Int. J. Parasitol. 2004, 34:1385-1392.
37. Neuhaus W. Der Einfluss des Zwischenwirtes auf die Gestalt der Cercarie von Trichobilharzia szidati Neuhaus1951und ihre systematische Kennzeichnung. Zoologisch. Anzeig. 1952, 148:275-285.
38. Haas W. Parasitic worms: strategies of host finding, recognition and invasion. Zoology 2003, 106:349-364.
39. Prokofiev V.V., Galaktionov K.V. Strategies of search behaviour in trematode cercariae. Trudy Zool. Inst. 2009, 313:308-318.
40. McMullen D.B., Beaver P.C. Studies on schistosome dermatitis. IX. The life cycles of three dermatitis-producing schistosomes from birds and a discussion of the subfamily Bilharziellinae (Trematoda: Schistosomatidae). Am. J. Hyg. 1945, 42:128-154.
41. Theron A. Early and late shedding patterns of Schistosoma mansoni cercariae - ecological significance in transmission to human and murine hosts. J. Parasitol. 1984, 70:652-655.
42. Steinauer M.L., et al. Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: a molecular epidemiological approach. PLoS Negl. Trop. Dis. 2008, 2:e222.
43. Loker E.S. A comparative study of the life histories of mammalian schistosomes. Parasitology 1983, 87:343-369.
44. Rollinson D., Southgate V.R. The genus Schistosoma: a taxonomic appraisal. The Biology of Schistosomes: From Genes to Latrines 1987, 1-49. Academic Press. D. Rollinson, A.J.G. Simpson (Eds.).
45. Attwood S.W., et al. Schistosoma ovuncatum n. sp. (Digenea: Schistosomatidae) from northwest Thailand and the historical biogeography of southeast Asian Schistosoma Weinland, 1858. Syst. Parasitol. 2002, 51:1-19.
46. Hanelt B., et al. Schistosoma kisumuensis n. sp. (Digenea: Schistosomatidae) from murid rodents in the Lake Victoria Basin, Kenya and its phylogenetic position within the S. haematobium species group. Parasitology 2009, 136:987-1001.
47. Brant S.V., et al. Molecular phylogenetics of the elephant schistosome Bivitellobilharzia loxodontae (Trematoda: Schistosomatidae) from the Central African Republic. J. Helminthol. 2013, 87:102-107.
48. Webster B.L., Littlewood T.J. Mitochondrial gene order change in Schistosoma (Platyhelminthes: Digenea: Schistosomatidae. Int. J. Parasitol. 2012, 42:313-321.
49. Devkota R., et al. Sharing schistosomes: the elephant schistosome Bivitellobilharzia nairi also infects the greater one-horned rhinoceros (Rhinoceros unicornis) in Chitwan National Park, Nepal. J. Helminthol. 2013, 10.1017/S0022149X12000697.
50. Vande Vusse F.J. Host parasite relations of Dendritobilharzia pulverulenta (Trematoda: Schistosomatidae) and anatids. J. Parasitol. 1979, 65:894-897.
51. Vande Vusse F.J. A review of the genus Dendritobilharzia Skrjabin and Zakharow 1920 (Trematoda: Schistosomatidae). J. Parasitol. 1980, 66:814-822.
52. Najim A.T. Life history of Gigantobilharzia huronensis Najim, 1950 - a dermatitis producing bird blood fluke (Trematoda: Schistosomatidae). Parasitology 1956, 46:443-469.
53. Jouet D., et al. Avian schistosomes in French aquatic birds: molecular approach. J. Helminthol. 2009, 83:181-189.
54. Blair D., Islam K.S. The life cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Syst. Parasitol. 1983, 5:89-117.
55. Kolářová L., et al. Trichobilharzia mergi sp. nov. (Trematoda: Digenea: Schistosomatidae), a visceral schistosome of Mergus serrator (L.) (Aves: Anatidae). Parasitol. Int. 2013, 62:300-308.
56. Johnson K.J., Sorenson M.D. Phylogeny and biogeography of the dabbling ducks (Genus: Anas): a comparison of molecular and morphological evidence. Auk 1999, 116:792-805.
57. Basch P.F. Why do schistosomes have separate sexes?. Parasitol. Today 1990, 6:160-163.
58. Despres L., Maurice S. The evolution of dimorphism and separate sexes in schistosomes. Proc. R. Soc. Lond. B: Biol. Sci. 1995, 262:175-180.
59. Platt T.R., Brooks D.R. Evolution of the schistosomes (Digenea: Schistosomatoidea): the origin of dioecy and colonization of the venous system. J. Parasitol. 1997, 83:1035-1044.
60. Beltran S., Boissier J. Male-biased sex ratio: why and what consequences for the genus Schistosoma?. Trends Parasitol. 2010, 26:63-69.
61. Hrádková K., Horák P. Neurotropic behavior of Trichobilharzia regenti in ducks and mice. J. Helminthol. 2002, 76:137-141.
62. Chanová M., Horák P. Terminal phase of bird schistosomiasis caused by Trichobilharzia regenti (Schistosomatidae) in ducks (Anas platyrhynchos f. domestica). Folia Parasitol. (Praha) 2007, 54:105-107.
63. Horák P., et al. Penetration of Trichobilharzia cercariae into mammals: dangerous or negligible event?. Parasite 2008, 15:299-303.
64. Spakulová M., et al. The karyotype of Trichobilharzia regent Horák, Kolářová, and Dvořák, 1998 (Digenea: Schistosomatidae), a nasal schistosome in Central Europe. Parasitol. Res. 2001, 87:479-483.
65. Morand S., Muller-Graf C.D. Muscles or testes? Comparative evidence for sexual competition among dioecious blood parasites (Schistosomatidae) of vertebrates. Parasitology 2000, 120:45-56.
66. Bourns T.K.R., et al. Migration and development of Trichobilharzia ocellata (Trematoda: Schistosomatidae) in its duck hosts. Can. J. Zool. 1973, 51:1021-1030.
67. Ozumba N.A., et al. Endemicity, focality and seasonality of transmission of human schistosomiasis in Amagunze village, eastern Nigeria. J. Helminthol. 1989, 63:206-212.
68. Agbolade O.M., et al. Human urinary schistosomiasis transmission foci and period in an endemic town of Liebu North, southwest Nigeria. Trop. Biomed. 2004, 21:15-22.
69. Hassan A.O., et al. Human water contact activities and urinary schistosomiasis around Erinle and Eko-ende dams. Global Adv. Res. J. Med. Med. Sci. 2012, 1:77-84.
70. Aldhoun J.A., et al. Bird schistosomes in planorbid snails in the Czech Republic. Parasitol. Int. 2012, 61:250-259.
71. Rollinson D. Natural history, ecology and schistosome transmission. Biomphalaria Snails and Larval Trematodes 2011, 57-79. Springer. R. Toledo, B. Fried (Eds.).
72. Lie K.J. Survival of Schistosoma mansoni and other trematode larvae in the snail Biomphalaria glabrata - a discussion of the interference theory. Trop. Geogr. Med. 1982, 34:111-122.
73. Chouikha I., Hinnebusch J.B. Yersinia-flea interactions and the evolution of the arthropod-bourne transmission route of plague. Curr. Opin. Microbiol. 2012, 15:239-246.
74. Wright C.A. Snail susceptibility or trematode infectivity?. J. Nat. Hist. 1974, 8:545-548.
75. Fan P.C., Lin L.H. Hybridization of Schistosoma mansoni and Schistosoma japonicum in mice. Southeast Asian J. Trop. Med. Public Health 2005, 36:89-96.
76. Tsangaras K., et al. Museums and disease: using tissue archive and museum samples to study pathogens. Ann. Anat. 2012, 194:58-73.
77. Hartigan A., et al. Museum material reveals frog parasite emergence after the invasion of the cane toad in Australia. Parasit. Vectors 2010, 3:50.
78. Hoberg E.P., et al. Why museums matter: a tale of pinworms (Oxyuroidea: Heteroxynematidae) among Pikas (Ochotona princeps and O. collaris) in the American West. J. Parasitol. 2009, 95:490-501.
79. Hunova K., et al. Radix spp.: identification of trematode intermediate hosts in the Czech Republic. Acta Parasitol. 2012, 57:273-284.
80. Platt T.R., et al. Griphobilharzia amoena n. gen., n. sp. (Digenea: Schistosomatidae), a parasite of the freshwater crocodile Crocodylus johnstoni (Reptilia: Crocodylia) from Australia, with the erection of a new subfamily, Griphobilharziinae. J. Parasitol. 1991, 77:65-68.
81. Jouet D. Molecular diversity of Trichobilharzia franki in two intermediate hosts (Radix auricularia and Radix peregra): a complex of species. Infect. Genet. Evol. 2010, 10:1218-1227.
82. Lui Z., Bai G. On bird schistosomes from Jilin Province: Jilinobilharzia crecci gen. nov., sp. nov. (Schistodomatidae: Bilharziellinae) with a discussion on the taxonomy of the subfamily Bilharziellinae. Acta Zool. Sin. 1976, 22:385-392.
83. Santoferrara L., et al. Utility of genetic markers and morphology for species discrimination within the order Tintinnida (Ciliophora, Spirotrichea). Protist 2013, 164:24-36.
84. Rudolfová J.A., et al. Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol. Res. 2005, 95:79-89.
85. Vilas R., et al. A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 2005, 131:839-846.
86. Detwiler J.T., et al. Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. J. Parasitol. 2012, 98:1148-1155.
87. Huelsenbeck J.P., Ronquist F. MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 2001, 17:754-755.
88. Berriman M., et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358.
89. Young N.D., et al. Whole-genome sequence of Schistosoma haematobium. Nat. Genet. 2012, 44:221-225.