Evidence for extensive cryptic speciation in trematodes of butterflyfishes (Chaetodontidae) of the tropical Indo-West Pacific

International Journal for Parasitology

Volumn 44, Issue 1, 2014, Pages 37-48

  McNamara, M K A ^a   Miller, T L ^b   Cribb, T H ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b JAMES COOK UNIVERSITY   (Australia)

Author keywords

Chaetodontidae; Cryptic species; Hurleytrematoides; Monorchiidae; Parasites

Indexed keywords

INTERNAL TRANSCRIBED SPACER 2; MITOCHONDRIAL DNA;

FISH; FLATWORM; MITOCHONDRIAL DNA; MORPHOLOGY; PARASITE; SPECIATION (BIOLOGY); TAXONOMY;

ARTICLE; CONTROLLED STUDY; COX1 GENE; FISH; GENE; GENETIC MARKER; GENETIC VARIABILITY; HAPLOTYPE; HURLEYTREMATOIDES CORONATUM; HURLEYTREMATOIDES DEBLOCKI; HURLEYTREMATOIDES FALIEXAE; HURLEYTREMATOIDES LOI; HURLEYTREMATOIDES MORANDI; HURLEYTREMATOIDES SASALI; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE IDENTIFICATION; PLATYHELMINTH; SEQUENCE ANALYSIS; SPECIES COMPARISON; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION; TREMATODE;

AUSTRALIA; CAROLINE ISLANDS; CORAL SEA; GREAT BARRIER REEF; HERON ISLAND; LIZARD ISLAND; MOOREA; NEW CALEDONIA [MELANESIA]; NINGALOO REEF; PACIFIC OCEAN; PALAU; QUEENSLAND; SOCIETY ISLANDS; WESTERN AUSTRALIA; WINDWARD ISLANDS [SOCIETY ISLANDS];

CHAETODONTIDAE; HURLEYTREMATOIDES; MONORCHIIDAE; PISCES; SQUAMATA; TETRAODONTIDAE; TREMATODA;

CHAETODONTIDAE; CRYPTIC SPECIES; HURLEYTREMATOIDES; MONORCHIIDAE; PARASITES;

ANIMALS; AQUATIC ORGANISMS; AUSTRALASIA; CHORDATA; CLUSTER ANALYSIS; DNA, MITOCHONDRIAL; DNA, RIBOSOMAL SPACER; ELECTRON TRANSPORT COMPLEX IV; FISH DISEASES; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PACIFIC OCEAN; PHYLOGENY; SEQUENCE ANALYSIS, DNA; TREMATODA; TREMATODE INFECTIONS;

EID: 84892372911     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.09.005     Document Type: Article

References (94)

1. Abbott R.J., Ritchie M.G., Hollingsworth P.M. Speciation in plants and animals: pattern and process - introduction. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:2965-2969.
2. Aiken H.M., Bott N.J., Mladineo I., Montero F.E., Nowak B.F., Hayward C.J. Molecular evidence for cosmopolitan distribution of platyhelminth parasites of tunas (Thunnus spp.). Fish Fish. 2007, 8:167-180.
3. Barber P.H., Bellwood D.R. Biodiversity hotspots: evolutionary origins of biodiversity in wrasses (Halichoeres: Labridae) in the Indo-Pacific and new world tropics. Mol. Phylogenet. Evol. 2005, 35:235-253.
4. Bartoli P. Lasiotocus longicystis n. sp. (Trematoda, Digenea, Monorchiidae), metacercaire parasite de lamellibranches marins; recherches experimentales sur son developpement. B. Soc. Zool. Fr. 1965, 90:119-129.
5. Bartoli P., Jousson O., Russel-Pinto F. The life cycle of Monorchis parvus (Digenea: Monorchiidae) demonstrated by developmental and molecular data. J. Parasitol. 2000, 86:479-489.
6. Bay L.K., Caley M.J.M., Crozier R.H. Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation. BMC Evol. Biol. 2008, 8:248.
7. Bickford D., Lohman D.J., Sodhi N.S., Ng P.K.L., Meier R., Winker K., Ingram K.K., Das I. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 2007, 22:148-155.
8. Blasco-Costa I., Balbuena J.A., Raga J.A., Kostadinova A., Olson P.D. Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 2010, 137:287-302.
9. Blouin M.S. Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. Int. J. Parasitol. 2002, 32:527-531.
10. Bowles J., Hope M., Tiu W.U., Liu X., McManus D.P. Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum. Acta Trop. 1993, 55:217-229.
11. Brower A.V.Z. Alleviating the taxonomic impediment of DNA barcoding and setting a bad precedent: names for ten species of 'Astraptes fulgerator' (Lepidoptera: Hesperiidae: Eudaminae) with DNA-based diagnoses. Syst. Biodivers. 2010, 8:485-491.
12. Chambers C.B., Cribb T.H. Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Syst. Parasitol. 2006, 63:61-82.
13. Cook L.G., Edwards R.D., Crisp M.D., Hardy N.B. Need morphology always be required for new species descriptionsα. Invertebr. Syst. 2010, 24:322-326.
14. Cribb T.H., Anderson G.R., Adlard R.D., Bray R.A. A DNA-based demonstration of a three-host life-cycle for the Bivesiculidae (Platyhelminthes: Digenea). Int. J. Parasitol. 1998, 28:1791-1795.
15. Cribb T.H., Bray R.A. Gut wash, body soak, blender and heat-fixation: approaches to the effective collection, fixation and preservation of trematodes of fishes. Syst. Parasitol. 2010, 76:1-7.
16. Cribb T.H., Bray R.A., Barker S.C., Adlard R.D., Anderson G.R. Ecology and diversity of digenean trematodes of reef and inshore fishes of Queensland. Int. J. Parasitol. 1994, 24:851-860.
17. Cribb T.H., Pichelin S., Dufour V., Bray R.A., Chauvet C., Faliex E., Galzin R., Lo C.M., Lo-Yat A., Morand S., Rigby M.C., Sasal P. Parasites of recruiting coral reef fish larvae in New Caledonia. Int. J. Parasitol. 2000, 30:1445-1451.
18. Criscione C.D., Poulin R., Blouin M.S. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol. Ecol. 2005, 14:2247-2257.
19. de Queiroz K. The general lineage concept of species, species criteria, and the process of speciation - A conceptual unification and terminological recommendations. Endless Forms 1998, 57-75. Oxford University Press, New York. D.J. Howard, S.H. Berlocher (Eds.).
20. DeMartini J.D., Pratt I. The life cycle of Telolecithus pugetensis Lloyd and Guberlet, 1932 (Trematoda: Monorchidae). J. Parasitol. 1964, 50:101-105.
21. Detwiler J.T., Bos D.H., Minchella D.J. Revealing the secret lives of cryptic species: examining the phylogenetic relationships of echinostome parasites in North America. Mol. Phylogenet. Evol. 2010, 55:611-620.
22. Donald K.M., Kennedy M., Poulin R., Spencer H.G. Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). Int. J. Parasitol. 2004, 34:557-568.
23. Downie A.J., Bray R.A., Jones B.E., Cribb T.H. Taxonomy, host-specificity and biogeography of Symmetrovesicula Yamaguti, 1938 (Digenea: Fellodistomidae) from chaetodontids (Teleostei: Perciformes) in the tropical Indo-west Pacific region. Syst. Parasitol. 2011, 78:1-18.
24. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
25. Frezal L., Leblois R. Four years of DNA barcoding: current advances and prospects. Infect. Genet. Evol. 2008, 8:727-736.
26. Georgieva S., Selbach C., Faltýnková A., Soldánová M., Sures B., Skírnisson K., Kostadinova A. New cryptic species of the 'revolutum' group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasite Vectors 2013, 6:64.
27. Georgieva S., Soldánová M., Pérez-del-Olmo A., Dangel R.D., Sitko J., Sures B., Kostadinova A. Molecular prospecting for European Diplostomum (Digenea: Diplostomidae) reveals cryptic diversity. Int. J. Parasitol. 2013, 43:57-72.
28. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
29. Hall K.A., Cribb T.H. Ptychogyliauchen, a new genus of Gyliauchenidae (Platyhelminthes: Digenea) from siganid fishes of the Indo-West Pacific. Invertebr. Syst. 2004, 18:607-625.
30. Halt M.N., Kupriyanova E.K., Cooper S.J.B., Rouse G.W. Naming species with no morphological indicators: species status of Galeolaria caespitosa (Annelida: Serpulidae) inferred from nuclear and mitochondrial gene sequences and morphology. Invertebr. Syst. 2009, 23:205-222.
31. Hammer Ø., Harper D.A.T., Ryan P.D. PAST: paleontological statistics software package for education and data analysis. Palaeontol. Electronica 2001, 4:1-9.
32. Holmes J.C. The structure of helminth communities. Int. J. Parasitol. 1987, 17:203-208.
33. Hubert N., Meyer C.P., Bruggemann H.J., Guerin F., Komeno R.J.L., Espiau B., Causse R., Williams J.T., Planes S. Cryptic diversity in Indo-Pacific coral-reef fishes revealed by DNA-barcoding provides new support to the centre-of-overlap hypothesis. PLoS ONE 2012, 7.
34. Hunter J.A., Cribb T.H. A cryptic complex of species related to Transversotrema licinum Manter, 1970 from fishes of the Indo-West Pacific, including descriptions of ten new species of Transversotrema Witenberg, 1944 (Digenea: Transversotrematidae). Zootaxa 2012, 3176:1-44.
35. Hunter J.A., Ingram E., Adlard R.D., Bray R.A., Cribb T.H. A cryptic complex of Transversotrema species (Digenea: Transversotrematidae) on labroid, haemulid and lethrinid fishes in the Indo-West Pacific Region, including the description of three new species. Zootaxa 2010, 17-32.
36. Hutson K., Styan C.A., Beveridge I., Keough M.J., Zhu X., Abs EL-Osta Y.G., Gasser R.B. Elucidating the ecology of bucephalid parasites using a mutation scanning approach. Mol. Cell. Probes 2004, 18:139-146.
37. Jones D.B., Jerry D.R., McCormick M.I., Bay L.K. The population genetic structure of a common tropical damselfish on the Great Barrier Reef and eastern Papua New Guinea. Coral Reefs 2010, 29:455-467.
38. Jousson O., Bartoli P. Species diversity among the genus Monorchis (Digenea: Monorchiidae) parasitic in marine teleosts: molecular, morphological and morphometrical studies with a description of Monorchis blennii m. sp. Parasitol. Res. 2002, 88:230-241.
39. Jousson O., Bartoli P., Pawlowski J. Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). J. Evol. Biol. 2000, 13:778-785.
40. Justine J.L. Parasites of coral reef fish: how much do we knowα With a bibliography of fish parasites in New Caledonia. Belg. J. Zool. 2010, 140:155-190.
41. Kearn G. The eggs of monogeneans. Adv. Parasitol. 1986, 25:175-273.
42. Knowlton N. Molecular genetic analyses of species boundaries in the sea. Hydrobiologica 2000, 420:73-90.
43. Kon T., Yoshino T., Nishida M. Cryptic species of the gobioid paedomorphic genus Schindleria from Palau, Western Pacific Ocean. Ichthyol. Res. 2011, 58:62-66.
44. Kritsky D.C., Stephens F. Haliotrema abaddon n. sp. (Monogenoidea: Dactylogyridae) from the gills of wild and maricultured West Australian dhufish Glaucosoma hebraicum (Teleostei: Glaucosomatidae), in Australia. J. Parasitol. 2001, 87:749-754.
45. Lanave C., Preparata G., Sacconefl C., Serio G. A new method for calculating evolutionary substitution rates. J. Mol. Evol. 1984, 20:86-93.
46. Leung T.L.F., Keeney D.B., Poulin R. Cryptic species complexes in manipulative echinostomatid trematodes: when two become six. Parasitology 2009, 136:241-252.
47. Locke S.A., McLaughlin J.D., Marcogliese D.J. DNA barcodes show cryptic diversity and a potential physiological basis for host specificity among Diplostomoidea (Platyhelminthes: Digenea) parasitizing freshwater fishes in the St. Lawrence River. Can. Mol. Ecol. 2010, 19:2813-2827.
48. Louhi K.R., Karvonen A., Rellstab C., Jokela J. Is the population genetic structure of complex life cycle parasites determined by the geographic range of the most motile hostα. Infect. Genet. Evol. 2010, 10:1271-1277.
49. Luton K., Walker D., Blair D. Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Mol. Biochem. Parasitol. 1992, 56:323-328.
50. Madhavi R. Checklist of digenean trematodes reported from Indian marine fishes. Syst. Parasitol. 2011, 78:163-232.
51. Mallet J. Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2008, 363:2971-2986.
52. Martin W.E. Studies on the trematodes of Woods Hole. III. The life cycle of Monorcheides cumingiae (Martin) with special reference to its effect on the invertebrate host. Biol. Bull. 1940, 79:131-144.
53. Mayr E. Systematics and the Origin of Species from the Viewpoint of a Zoologist 1964, Dover Publications, New York.
54. Mayr E. Populations, Species, and Evolution: An Abridgment of Animal Species and Evolution 1970, Harvard University Press, Cambridge.
55. McMillan W.O., Palumbi S.R. Concordant evolutionary patterns among Indo-west Pacific butterflyfishes. Proc. R. Soc. Lond. B Biol. Sci. B 1995, 260:229-236.
56. McNamara M.K.A., Adlard R.D., Bray R.A., Sasal P., Cribb T.H. Monorchiids (Platyhelminthes: Digenea) of chaetodontid fishes (Perciformes): biogeographical patterns in the tropical Indo-West Pacific. Parasitol. Int. 2012, 61:288-306.
57. McNamara M.K.A., Cribb T.H. Hurleytrematoides justinei n. sp. (Digenea: Monorchiidae) from Canthigaster valentini (Bleeker, 1853) (Tetraodontiformes: Tetraodontidae) from Heron Island, Queensland, Australia. Zootaxa 2009, 2027:63-68.
58. McNamara M.K.A., Cribb T.H. Taxonomy, host specificity and dietary implications of Hurleytrematoides (Digenea: Monorchiidae) from chaetodontid fishes on the Great Barrier Reef. Parasitol. Int. 2011, 60:255-269.
59. Meyer C.P., Geller J.B., Paulay G. Fine scale endemism on coral reefs: archipelagic differentiation in turbinid gastropods. Evolution 2005, 59:113-125.
60. Miller T.L., Adlard R.D., Bray R.A., Justine J.L., Cribb T.H. Cryptic species of Euryakaina n. g. (Digenea: Cryptogonimidae) from sympatric lutjanids in the Indo-West Pacific. Syst. Parasitol. 2010, 77:185-204.
61. Miller T.L., Bray R.A., Cribb T.H. Taxonomic approaches to and interpretation of host-specificity of trematodes of fishes: lessons from the Great Barrier Reef. Parasitology 2011, 138:1710-1722.
62. Miller T.L., Cribb T.H. Coevolution of Retrovarium n. gen. (Digenea: Cryptogonimidae) in Lutjanidae and Haemulidae (Perciformes) in the Indo-West Pacific. Int. J. Parasitol. 2007, 37:1023-1045.
63. Miller T.L., Cribb T.H. 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. 2007, 52:104-113.
64. Miller T.L., Cribb T.H. Eight new species of Siphoderina Manter, 1934 (Digenea, Cryptogonimidae) infecting Lutjanidae and Haemulidae (Perciformes) off Australia. Acta Parasitol. 2008, 53:344-364.
65. Miura O., Kuris A.M., Torchin M.E., Hechinger R.F., Dunham E.J., Chiba S. Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). Int. J. Parasitol. 2005, 35:793-801.
66. Nadler S.A., Perez-Ponce De Leon G. Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 2011, 138:1688-1709.
67. Nolan M.J., Cribb T.H. Cardicola Short, 1953 and Braya n. gen. (Digenea: Sanguinicolidae) from five families of tropical Indo-Pacific fishes. Zootaxa 2006, 1265:1-80.
68. Nolan M.J., Cribb T.H. An exceptionally rich complex of Sanguinicolidae von Graff, 1907 (Platyhelminthes: Trematoda) from Siganidae, Labridae and Mullidae (Teleostei: Perciformes) from the Indo-west Pacific Region. Zootaxa 2006, 1218:1-80.
69. Palumbi S.R. Molecular biogeography of the Pacific. Coral Reefs 1997, 16:S47-S52.
70. Perez-Ponce de Leon 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.
71. Plaisance L., Rousset V., Morand.S., Littlewood D.T.J. Colonization of Pacific islands by parasites of low dispersal ability: phylogeography of two monogenean species parasitizing butterflyfishes in the South Pacific Ocean. J. Biogeogr. 2008, 35:76-87.
72. Pleijel F., Jondelius U., Norlinder E., Nygren A., Oxelman B., Schander C., Sundberg P., Thollesson M. Phylogenies without rootsα A plea for the use of vouchers in molecular phylogenetic studies. Mol. Phylogenet. Evol. 2008, 48:369-371.
73. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
74. Poulin R. Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biol. Lett. 2011, 7:241-244.
75. Prevot G. Metacercariae sp. Prevot, 1966 d' Antedon mediterranea Lmk. (Echinoderme), forme larvaire de Monorchis monorchis (M. Stossich) A. Looss, 1902 (Trematoda: Digenea). Ann. Parasit. Hum. Comp. 1967, 42:367-369.
76. Puillandre N., Sysoev A.V., Olivera B.M., Couloux A., Bouchet P. Loss of planktotrophy and speciation: geographical fragmentation in the deep-water gastropod genus Bathytoma (Gastropoda, Conoidea) in the western Pacific. Syst. Biodivers. 2010, 8:371-394.
77. Randall J.E. Zoogeography of shore fishes of the Indo-Pacific region. Zool. Stud. 1998, 37:227-268.
78. Razo-Mendivil U., Vazquez-Dominguez E., Rosas-Valdez R., Perez-Ponce de Leon G., Nadler S.A. Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea: Apocreadiidae), a parasite of Middle-American cichlids. Int. J. Parasitol. 2010, 40:471-486.
79. Rohde K. Species diversity of parasites on the Great Barrier Reef. Parasitol. Res. 1976, 50:93-94.
80. Rohner C.A., Cribb T.H. Opecoelidae (Digenea: Trematoda) in northern Great Barrier Reef goatfishes (Perciformes: Mullidae). Syst. Parasitol. 2013, 84:237-253.
81. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
82. Rosas-Valdez R., Choudhury A., De Leon G.P.P. Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zool. Scr. 2011, 40:296-305.
83. Russell-Pinto F., Goncalves J.F., Bowers E. Digenean larvae parasitizing Cerastoderma edule (Bivalvia) and Nassarius reticulatus (Gastropoda) from Ria de Aveiro, Portugal. J. Parasitol. 2006, 92:319-332.
84. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York. 3rd ed.
85. San Mauro D., Agorreta A. Molecular systematics: a synthesis of the common methods and the state of knowledge. Cell. Mol. Biol. Lett. 2010, 15:311-341.
86. Stunkard H.W. The morphology, life history, and systematic relations of Lasiotocus elongatus (Manter, 1931) Thomas, 1959 (Trematoda: Digenea). Biol. Bull. 1981, 160:155-160.
87. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
88. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
89. 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, 131:839-846.
90. Wilkins J.S. Species: A History of the Idea 2009, University of California Press, Berkeley.
91. Williams S.T., Jara J., Gomez E., Knowlton N. The marine Indo-West Pacific break: contrasting the resolving power of mitochondrial and nuclear genes. Integr. Comp. Biol. 2002, 42:941-952.
92. Yamaguti S. Digenetic Trematodes of Hawaiian Fishes 1970, Keigaku Publishing Co., Tokyo.
93. Yao H., Song J., Liu C., Luo K., Han J. Use of ITS2 region as the universal DNA barcode for plants and animals. PLoS One 2010, 5:e13102. doi:13110.11371/journal.pone.0013102.
94. Zink R.M. Methods in comparative phylogeography, and their application to studying evolution in the North American aridlands. Integr. Comp. Biol. 2002, 42:953-959.