Distinct lineages of schistocephalus parasites in threespine and ninespine stickleback hosts revealed by DNA sequence analysis

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Nishimura, Nicole ^a   Heins, David C ^b   Andersen, Ryan O ^a   Barber, Iain ^c   Cresko, William A ^a  

^a UNIVERSITY OF OREGON   (United States)

^b Tulane University   (United States)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOOXYGENASE 1; MITOCHONDRIAL DNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE 1; UNCLASSIFIED DRUG; PROTEIN;

ANIMAL TISSUE; ARTICLE; BASE PAIRING; CESTODE; CESTODE LIFE CYCLE STAGE; CLADISTICS; DNA SEQUENCE; FISH; GENE STRUCTURE; GEOGRAPHIC DISTRIBUTION; HOST PARASITE INTERACTION; NONHUMAN; NORTHERN HEMISPHERE; PHENOTYPE; SCHISTOCEPHALUS; STICKLEBACK; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMAL; CHEMISTRY; GENETIC VARIABILITY; GENETICS; HAPLOTYPE; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PARASITE; PARASITOLOGY; PHYLOGENY; SEQUENCE ALIGNMENT; SMEGMAMORPHA;

AVES; CESTODA; GASTEROSTEUS; PUNGITIUS; SCHISTOCEPHALUS;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BASE SEQUENCE; CESTODA; CLONING, MOLECULAR; DNA, MITOCHONDRIAL; GENETIC VARIATION; HAPLOTYPES; HOST-PARASITE INTERACTIONS; MOLECULAR SEQUENCE DATA; PARASITES; PHYLOGENY; PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SMEGMAMORPHA;

EID: 79960440507     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022505     Document Type: Article

References (92)

1. Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM, (2003) Introduced species and their missing parasites. Nature 421: 628-630.
2. Lafferty KD, Dobson AP, Kuris AM, (2006) Parasites dominate food web links. Proc Natl Acad Sci U S A 103: 11211-11216.
3. Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, et al. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454: 515-518.
4. Lafferty KD, (2008) Ecosystem consequences of fish parasites. Journal of Fish Biology.
5. Lafferty KD, Kuris AM, (2009) Parasites reduce food web robustness because they are sensitive to secondary extinction as illustrated by an invasive estuarine snail. Philos Trans R Soc Lond B Biol Sci 364: 1659-1663.
6. Hudson PJ, Dobson AP, Lafferty KD, (2006) Is a healthy ecosystem one that is rich in parasites? Trends Ecol Evol 21: 381-385.
7. Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, et al. (2008) Parasites in food webs: the ultimate missing links. Ecol Lett 11: 533-546.
8. Thomas LJ, (1947) Notes on the life cycle of Schistocephalus sp., a tapeworm from gulls. J Parasitol 33: 10.
9. Wedekind C, Milinski M, (1996) Do three-spined sticklebacks avoid consuming copepods, the first intermediate host of Schistocephalus solidus? An experimental analysis of behavioural resistance. Parasitology 112: 371-383.
10. Barber I, Hoare D, Krause J, (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10: 131-165.
11. Moore J, (2000) Parasites and the behavior of animals Oxford, UK Oxford University Press.
12. Franz K, Kurtz J, (2002) Altered host behaviour: manipulation or energy depletion in tapeworm-infected copepods? Parasitology 125: 187-196.
13. Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR, (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet 32: 569-577.
14. Choisy M, Brown SP, Lafferty KD, Thomas F, (2003) Evolution of trophic transmission in parasites: why add intermediate hosts? Am Nat 162: 172-181.
15. Hammerschmidt K, Kurtz J, (2005) Evolutionary implications of the adaptation to different immune systems in a parasite with a complex life cycle. Proc R Soc Lond B Biol Sci 272: 2511-2518.
16. Hammerschmidt K, Koch K, Milinski M, Chubb JC, Parker GA, (2009) When to go: optimization of host switching in parasites with complex life cycles. Evolution 63: 1976-1986.
17. Blasco-Costa I, Balbuena JA, Raga JA, Kostadinova A, Olson PD, (2010) Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 137: 287-302.
18. Arme C, Owen RW, (1967) Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology 57: 301-314.
19. Barber I, Scharsack JP, (2010) The three-spined stickleback-Schistocephalus solidus system: an experimental model for investigating host-parasite interactions in fish. Parasitology 137: 411-424.
20. Bell MA, (1976) Evolution of phenotypic diversity in Gasterosteus aculeatus superspecies on the Pacific coast of North America. Syst Zool 25: 211-227.
21. Wootton RJ, (1976) The biology of the sticklebacks London; New York Academic Press pp. 387 p.
22. Wootton RJ, (1984) A functional biology of sticklebacks Berkeley, CA University of California Press pp. 265 p.
23. Bell MA, Foster SA, (1994) The evolutionary biology of the threespine stickleback Oxford; New York Oxford University Press pp. 571 p.
24. Schluter D, (2000) The ecology of adaptive radiations Oxford Oxford University Press pp. 288 p.
25. McKinnon JS, Rundle HD, (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17: 480-488.
26. Cresko WA, McGuigan KL, Phillips PC, Postlethwait JH, (2007) Studies of threespine stickleback developmental evolution: progress and promise. Genetica 129: 105-126.
27. Peichel CL, Nereng KS, Ohgi KA, Cole BL, Colosimo PF, et al. (2001) The genetic architecture of divergence between threespine stickleback species. Nature 414: 901-905.
28. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, et al. (2004) Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci U S A 101: 6050-6055.
29. Colosimo PF, Hosemann KE, Batabhadra S, Villarreal G Jr, Dickson M, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science 307: 1928-1933.
30. Kimmel CB, Ullmann B, Walker C, Wilson C, Currey M, et al. (2005) Evolution and development of facial bone morphology in threespine sticklebacks. Proc Natl Acad Sci U S A 102: 5791-5796.
31. Miller CT, Beleza S, Pollen AA, Schluter D, Kittles RA, et al. (2007) cis-Regulatory changes in Kit ligand expression and parallel evolution of pigmentation in sticklebacks and humans. Cell 131: 1179-1189.
32. Chan YF, Marks ME, Jones FC, Villarreal GJ, Shapiro MD, et al. (2010) Adaptive evolution of pelvic reduction in sticklebacks by recurrent deletion of a Pitx1 enhancer. Science 327: 302-305.
33. Hohenlohe PA, Bassham S, Etter PD, Stiffler N, Johnson EA, et al. (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS Genet 6: e1000862.
34. Cresko WA, (2008) Armor development and fitness. Science 322: 204-206.
35. Gibson G, (2005) The synthesis and evolution of a supermodel. Science 307: 1890-1891.
36. Barber I, (2007) Host-parasite interactions of the three-spined stickleback. In: Östlund-Nilsson S, Mayer I, Huntingford FA, editors. Biology of the three-spined stickleback Boca Raton, FL CRC Press pp. 271-318.
37. Heins DC, Ulinski B, Johnson J, Baker JA, (2004) Effect of the cestode macroparasite Schistocephalus pungitii on the reproductive success of ninespine stickleback, Pungitius pungitius. Can J Zool 82: 1731-1737.
38. Shapiro MD, Bell MA, Kingsley DM, (2006) Parallel genetic origins of pelvic reduction in vertebrates. Proc Natl Acad Sci U S A 103: 13753-13758.
39. Harmon LJ, Matthews B, Des Roches S, Chase JM, Shurin JB, et al. (2009) Evolutionary diversification in stickleback affects ecosystem functioning. Nature 458: 1167-1170.
40. Ross JA, Urton JR, Boland J, Shapiro MD, Peichel CL, (2009) Turnover of sex chromosomes in the stickleback fishes (Gasterosteidae). PLoS Genet 5: e1000391.
41. Shapiro MD, Summers BR, Balabhadra S, Aldenhoven JT, Miller AL, et al. (2009) The genetic architecture of skeletal convergence and sex determination in ninespine sticklebacks. Curr Biol 19: 1140-1145.
42. Heins DC, Baker JA, (2010) Castration of female ninespine stickleback by the pseudophyllidean cestode Schistocephalus pungitii: evolutionary significance and underlying mechanism. J Parasitol 96: 206-208.
43. Wheeler A, (1969) The fishes of the British Isles and North-West Europe Michigan State University Press pp. 613 p.
44. Marcogliese DJ, (1992) Metazoan parasites of sticklebacks on Sable Island, Northwest Atlantic Ocean: Biogeographic considerations. J Fish Biol 41: 399-407.
45. Dubinina M, (1959) The natural system of the genus Schistocephalus Creplin (Cestoda, Ligulidae) (in Russian). Zool Zh 38: 1498-1517.
46. Barber I, Wright HA, Arnott SA, Wootton RJ, (2008) Growth and energetics in the stickleback-Schistocephalus host-parasite system: a review of experimental infection studies. Behaviour 145: 647-668.
47. Heins DC, Baker JA, (2008) The stickleback-Schistocephalus host-parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145: 625-645.
48. Scharsack JP, Kalbe M, Derner R, Kurtz J, Milinski M, (2004) Modulation of granulocyte responses in three-spined sticklebacks Gasterosteus aculeatus infected with the tapeworm Schistocephalus solidus. Dis Aquat Organ 59: 141-150.
49. Scharsack JP, Kalbe M, Harrod C, Rauch G, (2007) Habitat-specific adaptation of immune responses of stickleback (Gasterosteus aculeatus) lake and river ecotypes. Proc R Soc Lond B Biol Sci 274: 1523-1532.
50. Scharsack JP, Koch K, Hammerschmidt K, (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proc R Soc Lond B Biol Sci 274: 3151-3158.
51. Smyth JD, (1946) Studies on tapeworm physiology, the cultivation of Schistocephalus solidus in vitro. J Exp Biol 23: 47-70.
52. Smyth JD, (1950) Studies on tapeworm physiology. V. Further observations on the maturation of Schistocephalus solidus (Diphyllobothriidae) under sterile conditions in vitro. J Parasitol 36: 371-383.
53. Smyth JD, (1954) Studies on tapeworm physiology. VII. Fertilization of Schistocephalus solidus in vitro. Exp Parasitol 3: 64-67.
54. Smyth JD, (1956) Studies on tapeworm physiology. IX. A histochemical study of egg-shell formation in Schistocephalus solidus (Pseudophyllidea). Exp Parasitol 5: 519-540.
55. Dartnall HJ, (1973) Parasites of 9-spined stickleback Pungitius pungitius (L). J Fish Biol 5: 505-509.
56. Hyslop EJ, Chubb JC, (1983) Schistocephalus pungitii Dubinina, 1959 (Cestoda) in Britain. Parasitology 87: R30-R30.
57. Hoffman GL, (1999) Parasites of North American freshwater fishes Ithaca, NY Cornell University Press.
58. Smyth JD, (1990) Parasitological serendipity: from Schistocephalus to Echinococcus. Int J Parasitol 20: 411-423.
59. Smyth JD, (1994) An introduction to animal parasitology Cambridge, UK Cambridge University Press.
60. Copp GH, Kovac V, (2003) Sympatry between threespine Gasterosteus aculeatus and ninespine Pungitius pungitius sticklebacks in English lowland streams. Ann Zool Fennici 40: 341-355.
61. Braten T, (1966) Host specificity in Schistocephalus solidus. Parasitology 56: 657-664.
62. Orr TSC, Hopkins CA, Charles GH, (1969) Host specificity and rejection of Schistocephalus solidus. Parasitology 59: 683-690.
63. Chubb JC, Seppala T, Luscher A, Milinski M, Valtonen ET, (2006) Schistocephalus cotti n. sp. (Cestoda: Pseudophyllidea) plerocercoids from bullheads Cottus gobio L. in an Arctic river in Finland, with a key to the plerocercoids of the Palaearctic species of the genus. Syst Parasitol 65: 161-170.
64. Olson PD, Littlewood DT, Griffiths D, Kennedy CR, Arme C, (2002) Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J Helminthol 76: 171-174.
65. Logan FJ, Horak A, Stefka J, Aydogdu A, Scholz T, (2004) The phylogeny of diphyllobothriid tapeworms (Cestoda: Pseudophyllidea) based on ITS-2 rDNA sequences. Parasitol Res 94: 10-15.
66. Bouzid W, Stefka J, Hypsa V, Lek S, Scholz T, et al. (2008) Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). Int J Parasitol 38: 1465-1479.
67. Stefka J, Hypsa V, Scholz T, (2009) Interplay of host specificity and biogeography in the population structure of a cosmopolitan endoparasite: microsatellite study of Ligula intestinalis (Cestoda). Mol Ecol 18: 1187-1206.
68. Orti G, Bell MA, Reimchen TE, Meyer A, (1994) Global survey of mitochondrial-DNA sequences In the threespine stickleback- evidence for recent migrations. Evolution 48: 608-622.
69. Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG, et al. (2003) Major patterns of higher teleostean phylogenies: a new perspective based on 100 complete mitochondrial DNA sequences. Mol Phylogenet Evol 26: 121-138.
70. Hunt G, Bell MA, Travis MP, (2008) Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage. Evolution 62: 700-710.
71. Wegner KM, Reusch TB, Kalbe M, (2003) Multiple parasites are driving major histocompatibility complex polymorphism in the wild. J Evol Biol 16: 224-232.
72. Kurtz J, Kalbe M, Aeschlimann PB, Haberli MA, Wegner KM, et al. (2004) Major histocompatibility complex diversity influences parasite resistance and innate immunity in sticklebacks. Proc R Soc Lond B Biol Sci 271: 197-204.
73. Kurtz J, Hammerschmidt K, (2006) Resistance against heterogeneous sequential infections: experimental studies with a tapeworm and its copepod host. J Helminthol 80: 199-206.
74. Wegner KM, Kalbe M, Rauch G, Kurtz J, Schaschl H, et al. (2006) Genetic variation in MHC class II expression and interactions with MHC sequence polymorphism in three-spined sticklebacks. Mol Ecol 15: 1153-1164.
75. Sage RD, Whitney JB, Wilson AC, (1986) Genetic analysis of a hybrid zone between domesticus and musculus mice (Mus musculus complex): hemoglobin polymorphisms. Curr Top Microbiol Immunol 127: 75-85.
76. Sage RD, Heyneman D, Lim KC, Wilson AC, (1986) Wormy mice in a hybrid zone. Nature 324: 60-63.
77. Moulia C, Le Brun N, Dallas J, Orth A, Renaud F, (1993) Experimental evidence of genetic determinism in high susceptibility to intestinal pinworm infection in mice: a hybrid zone model. Parasitology 106: 387-393.
78. Moulia C, Le Brun N, Loubes C, Marin R, Renaud F, (1995) Hybrid vigour against parasites in interspecific crosses between two mice species. Heredity 74: 48-52.
79. Milinski M, (1990) Parasites and host decision-making. In: Barnard CJ, Behnke JM, editors. Parasitism and host behaviour London Taylor and Francis pp. 95-116.
80. Lester RJG, (1971) Influence of Schistocephalus plerocercoids on respiration of Gasterosteus and a possible resulting effect on behavior of fish. Can J Zool 49: 361-366.
81. Giles N, (1983) Behavioural effects of the parasite Schistocephalus solidus (Cestoda) on an intermediate host, the three-spined stickleback, Gasterosteus aculeatus L. Anim Behav 31: 1192-1194.
82. Ness JH, Foster SA, (1999) Parasite-associated phenotype modifications in threespine stickleback. Oikos 85: 127-134.
83. Barber J, Walker P, Svensson PA, (2004) Behavioural responses to simulated avian predation in female three spined sticklebacks: The effect of experimental schistocephalus solidus infections. Behaviour 141: 1425-1440.
84. Lobue CP, Bell MA, (1993) Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the threespine stickleback. Am Nat 142: 725-735.
85. Øverli O, Páll M, Borg B, Jobling M, Winberg S, (2001) Effects of Schistocephalus solidus infection on brain monoaminergic activity in female three-spined sticklebacks Gasterosteus aculeatus. Proc R Soc Lond B Biol Sci 268: 1411-1415.
86. McManus DP, Bowles J, (1996) Molecular genetic approaches to parasite identification: Their value in diagnostic parasitology and systematics. Int J Parasitol 26: 687-704.
87. Hung GC, Chilton NB, Beveridge I, Zhu XQ, Lichtenfels JR, et al. (1999) Molecular evidence for cryptic species within Cylicostephanus minutus (Nematoda: Strongylidae). Int J Parasitol 29: 285-291.
88. Miura O, Kuris AM, Torchin ME, Hechinger RF, Dunham EJ, et al. (2005) Molecular genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int J Parasitol 35: 793-801.
89. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792-1797.
90. Excoffier L, Laval G, Schneider S, (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47-50.
91. Guindon S, Gascuel O, (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
92. Posada D, (2008) jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25: 1253-1256.