Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-15T11:14:45.389Z Has data issue: false hasContentIssue false
  • English
  • Français

A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites

Published online by Cambridge University Press:  27 July 2005

R. VILAS ,
C. D. CRISCIONE  and
M. S. BLOUIN
R. VILAS
Affiliation:
Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, Oregon 97331, USA
C. D. CRISCIONE
Affiliation:
Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, Oregon 97331, USA
M. S. BLOUIN
Affiliation:
Department of Zoology, Oregon State University, 3029 Cordley Hall, Corvallis, Oregon 97331, USA
Get access Rights & Permissions [Opens in a new window]

Abstract

We examined the relative merits of mitochondrial DNA loci and ribosomal DNA internal transcribed spacers for their use in prospecting for cryptic species of platyhelminth parasites. Sequence divergence at ITS1 and ITS2 was compared with divergence at 2 mtDNA loci (NADH dehydrogenase-1 and cytochrome c oxidase I) between closely related species of trematodes and cestodes. Both spacers accumulated substitutions substantially more slowly than mtDNA, which clearly shows a higher level of divergence among species relative to intra-specific variation. Besides a slow rate of substitution, other caveats that may be encountered when using ITS sequences as a prospecting marker are discussed. In particular, we note recent studies that suggest the existence of substantial levels of intra-individual variation in ITS sequences of flatworms. Because it is likely that closely related species share this phenomenon, it may confound the detection of cryptic species, especially if small sample sizes are studied. Although potential limitations of mtDNA are also recognized, the higher rate of evolution and smaller effective population size of this marker increases the probability of detecting diagnostic characters between cryptic species.

Keywords

cytochrome c oxidase INADH dehydrogenase-1rDNA internal transcribed spacerplatyhelminth parasitescryptic speciesmolecular prospecting
Type
Research Article
Information
Parasitology , Volume 131 , Issue 6 , December 2005 , pp. 839 - 846
Copyright
© 2005 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, G. R. and Barker, S. C. ( 1998). Inference of phylogeny and taxonomy within the didymozoidae (Digenea) from the second internal transcribed spacer ITS2 of ribosomal DNA. Systematic Parasitology 41, 87–94.CrossRefGoogle Scholar
Avise, J. C. ( 2000). Phylogeography: the History and Formation of Species. Harvard University Press, Cambridge, MA. USA.
Ballard, J. W. O. and Whitlock, M. C. ( 2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.CrossRefGoogle Scholar
Bell, A. S. and Sommerville, C. ( 2002). Molecular evidence for a synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. anuligerum (von Nordman, 1832) (Digenea: Strigeidae) parasitic as metacercariae in British fishes. Journal of Helminthology 76, 193–198.Google Scholar
Benasson, D., Zhang, D. X., Hartl, D. L. and Hewitt, G. M. ( 2001). Mitochondrial pseudogenes: Evolution′s misplaced witnesses. Trends in Ecology and Evolution 16, 314–321.CrossRefGoogle Scholar
Bieberich, A. A. and Minchella, D. J. ( 2001). Mitochondrial inheritance in Schistosoma mansoni: mitochondrial variable number tandem repeat mutation produces noise on top of the signal. Journal of Parasitology 87, 1011–1015.CrossRefGoogle Scholar
Blair, D., Agatsuma, T., Watanobe, T., Okamoto, M. and Ito, A. ( 1997). Geographical genetic structure within the human lung fluke, Paragonimus westermani, detected from DNA sequences. Parasitology 115, 411–417.CrossRefGoogle Scholar
Blair, D., Chang, Z., Chen, M., Cui, A., Wu, B., Agatsuma, T., Iwagami, M., Corlis, D., Fu, C. and Zhan, X. ( 2005). Paragonimus skrjabini Chen, 1959 (Digenea: Paragonimidae) and related species in eastern Asia: a combined molecular and morphological approach to identification and taxonomy. Systematic Parasitology 60, 1–21.CrossRefGoogle Scholar
Blouin, M. S. ( 2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle Scholar
Bowles, J., Blair, D. and McManus, D. P. ( 1995). A molecular phylogeny of the genus Echinococcus. Parasitology 110, 317–328.CrossRefGoogle Scholar
Chan, K. M. A. and Levin, S. A. ( 2005). Leaky prezygotic isolation and porous genomes: rapid introgression of maternally inherited DNA. Evolution 59, 720–729.CrossRefGoogle Scholar
Criscione, C. D. and Blouin, M. S. ( 2004). Life cycles shape parasite evolution: comparative population genetics of salmon trematodes. Evolution 58, 198–202.CrossRefGoogle Scholar
Criscione, C. D., Poulin, R. and Blouin, M. S. ( 2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.CrossRefGoogle Scholar
Després, L., Imbert-Establet, D., Combes, C. and Bonhomme, F. ( 1992). Molecular evidence linking hominid evolution to recent radiation of Schistosomes (Platyhelminthes: Trematoda). Molecular Phylogenetics and Evolution 1, 295–304.CrossRefGoogle Scholar
Dover, G. A. ( 1982). Molecular drive: a cohesive mode of species evolution. Nature, London 299, 111–117.CrossRefGoogle Scholar
Dvorák, J., Vanácová, S., Hampl, V., Flegr, J. and Horák, P. ( 2002). Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124, 307–313.CrossRefGoogle Scholar
Galazzo, D. E., Dayanandan, S., Marcogliese, D. J. and McLaughlin, J. D. ( 2002). Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
Gasser, R. B., Zhu, X. and McManus, D. P. ( 1999). NADH dehydrogenase subunit 1 and cytochrome c oxidase subunit I sequences compared for members of the genus Taenia (Cestoda). International Journal for Parasitology 29, 1965–1970.CrossRefGoogle Scholar
Harris, D. J. and Crandall, K. A. ( 2000). Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Molecular Biology and Evolution 17, 284–291.CrossRefGoogle Scholar
Haukisalmi, V., Wickström, L. M., Hantula, J. and Henttonen, H. ( 2001). Taxonomy, genetic differentiation and Holartic biogeography of Paranoplocephala spp. (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx: Arvicolinae). Biological Journal of the Linnean Society 74, 171–196.Google Scholar
Hu, M., Gasser, R. B., Chilton, N. B. and Beveridge, I. ( 2005). Genetic variation in the mitochondrial cytochrome c oxidase subunit 1 within three species of Progamotaenia (Cestoda: Anoplocephalidae) from macropodid marsupials. Parasitology 130, 117–129.CrossRefGoogle Scholar
Huang, W. Y., He, B., Wang, C. R. and Zhu, X. Q. ( 2004). Characterization of Fasciola species from Mailand China by ITS-2 ribosomal DNA sequence. Veterinary Parasitology 120, 75–83.CrossRefGoogle Scholar
Hugall, A., Stanton, J. and Moritz, C. ( 1999). Reticulate evolution and the origins of ribosomal internal transcribed spacer diversity in apomictic Meloidogyne. Molecular Biology and Evolution 16, 157–164.CrossRefGoogle Scholar
Janotti-Passos, L. K., Souza, C. P., Parra, J. C. and Simpson, A. J. G. ( 2001). Biparental mitochondrial DNA inheritance in the parasitic trematode Schistosoma mansoni. Journal of Parasitology 87, 79–82.CrossRefGoogle Scholar
Jousson, O. and Bartoli, P. ( 2000). The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n.comb. (Digenea, Opecoelidae): evidence from molecules and morphology. International Journal for Parasitology 30, 747–760.Google Scholar
Jousson, O., Bartoli, P. and Pawlowki, J. ( 2000). Cryptic speciation among intestinal parasites (Trematoda: Digenea) infecting sympatric host fishes (Sparidae). Journal of Evolutionary Biology 13, 773–775.CrossRefGoogle Scholar
Kane, R. A. and Rollinson, D. ( 1994). Repetitive sequences in the ribosomal DNA internal transcribed spacer of Schistosoma haematobium, Schistosoma intercalatum and Schistosoma mattheei. Molecular and Biochemical Parasitology 63, 153–156.CrossRefGoogle Scholar
Kane, R. A., Ridgers, I. L., Johnston, D. A. and Rollinson, D. ( 1996). Repetitive sequences within the first internal transcribed spacer of ribosomal DNA in schistosomes contain a Chi-like site. Molecular and Biochemical Parasitology 75, 265–269.CrossRefGoogle Scholar
Kostadinova, A., Herniou, E. A., Barrett, J. and Littlewood, D. T. ( 2003). Phylogenetic relationships of Echinostoma rudolphi, 1809 (Digenea: Echinostomatidae) and related genera re-assessed via DNA and morphological analysis. Systematic Parasitology 54, 159–176.CrossRefGoogle Scholar
Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. ( 2001). MEGA2: Molecular Evolutionary Genetics Analysis software, Arizona State University, Tempe, Arizona, USA.
León-Règagnon, V., Brooks, D. R. and Pérez-Ponce De León, G. ( 1999). Differentiation of Mexican species of Haematoloechus loos, 1899 (Digenea: Plagiorchiformes): molecular and morphological evidence. Journal of Parasitology 85, 935–946.CrossRefGoogle Scholar
Luo, H., Nie, P., Zhang, Y. A., Wang, G. T. and Yao, W. J. ( 2002). Molecular variation of Bothriocephalus acheilognathi Yamaguti, 1934 (Cestoda: Pseudophyllidea) in different fish host species based on ITS rDNA sequences. Systematic Parasitology 52, 159–166.CrossRefGoogle Scholar
Luton, K., Walker, D. and Blair, D. ( 1992). Comparisons of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323–327.CrossRefGoogle Scholar
Macnish, M. G., Morgan-Ryan, U. M., Monis, P. T., Behnke, J. M. and Thompson, R. C. A. ( 2002). A molecular phylogeny of nuclear and mitochondrial sequences in Hymenolepis nana (Cestoda) supports the existence of a cryptic species. Parasitology 125, 567–575.CrossRefGoogle Scholar
Morgan, J. A. T. and Blair, D. ( 1995). Nuclear rDNA ITS sequence variation in the trematode genus Echinostoma: an aid to establishing relationships within the 37-collar spine group. Parasitology 111, 609–615.CrossRefGoogle Scholar
Morgan, J. A. T. and Blair, D. ( 1998). Relative merits of nuclear ribosomal internal transcribed spacer and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297.CrossRefGoogle Scholar
Morgan, J. A. T., DeJong, J., Lwambo, J. S., Mungai, B. N., Mkoji, G. M. and Loker, E. S. ( 2003). First report of a natural hybrid between Schistosoma mansoni and S. rodhaini. Journal of Parasitology 89, 416–418.CrossRefGoogle Scholar
Obwaller, A., Schneider, R., Walochnik, J., Gollackner, B., Deutz, A., Janitschke, K., Aspöck, H. and Auer, H. ( 2004). Echinococcus granulosus strain differentiation based on sequence heterogeneity in mitochondrial genes of cytochrome c oxidase-1 and NADH dehydrogenase-1. Parasitology 128, 569–575.CrossRefGoogle Scholar
Parkin, E. J. and Butlin, R. K. ( 2004). Within and between-individual sequence variation among ITS1 copies in the meadow grasshopper Chorthippus parallelus indicates frequent intrachromosomal gene conversion. Molecular Biology and Evolution 21, 1595–1601.CrossRefGoogle Scholar
Polanco, C., González, A. I. and Dover, G. A. ( 1998). Multigene family of ribosomal DNA in Drosophila melanogaster reveals contrasting patterns of homogenization for IGS and ITS spacer regions. A possible mechanism to resolve this paradox. Genetics 149, 243–256.Google Scholar
Pena, H. B., de Souza, C. P., Simpson, A. J. G. and Pena, S. D. J. ( 1995). Intracellular promiscuity in Schistosoma mansoni: Nuclear transcribed nuclear sequences are part of a mitochondrial minisatellite region. Proceedings of the National Academy of Sciences, USA 92, 915–919.CrossRefGoogle Scholar
Rollinson, D., Walker, T. K., Knowles, R. J. and Simpson, A. J. G. ( 1990). Identification of schistosome hybrids and larval parasites using rRNA probes. Systematic Parasitology 15, 65–73.CrossRefGoogle Scholar
Scholz, T., Skeríková, A., Shimazu, T. and Grygier, M. J. ( 2004). A taxonomic study of species of Bothriocephalus Rudolphi, 1808 (Cestoda: Pseudophyllidea) from eels in Japan: morphological and molecular evidence for the occurrence of B. claviceps (Goeze, 1782) and confirmation of the validity of B. japonicus Yamaguti, 1934. Systematic Parasitology 57, 87–96.Google Scholar
Thompson, R. C. A. and McManus, D. P. ( 2002). Towards a taxonomic revision of the genus Echinoccocus. Trends in Parasitology 18, 452–457.CrossRefGoogle Scholar
Tkach, V. V., Pawlowski, J. and Sharpilo, V. P. ( 2000). Molecular and morphological differentiation between species of the Plagiorchis vespertilionis group (Digenea, Plagiorchiidae) occurring in European bats, with a re-description of P. vespertilionis (Müller, 1780). Systematic Parasitology 47, 9–22.CrossRefGoogle Scholar
van Herwerden, L., Blair, D. and Agatsuma, T. ( 1998). Intra- and inter-specific variation in nuclear ribosomal internal transcribed spacer 1 of the Schistosoma japonicum species complex. Parasitology 116, 311–317.CrossRefGoogle Scholar
van Herwerden, L., Blair, D. and Agatsuma, T. ( 1999). Intra- and interindividual variation in ITS1 of Paragonimus westermani (Trematoda: Digenea) and related species: implications for phylogenetic studies. Molecular Phylogenetics and Evolution 12, 67–73.CrossRefGoogle Scholar
van Herwerden, L., Blair, D. and Agatsuma, T. ( 2000). Multiple lineages of the mitochondrial gene NADH dehydrogenase subunit 1 (ND1) in parasitic helminthes: implications for molecular evolutionary studies of facultatively anaerobic eukaryotes. Journal of Molecular Evolution 51, 339–352.CrossRefGoogle Scholar
Vogler, A. P. and DeSalle, R. ( 1994). Evolution and phylogenetic information content of the ITS-1 region in the tiger beetle Cincindela dorsalis. Molecular Biology and Evolution 11, 393–405.Google Scholar
von der Schulenburg, J. H., Hancock, J. M., Pagnamenta, A., Slogett, J. J., Majerus, M. E. and Hurst, G. D. ( 2001). Extreme length and length variation in the first ribosomal internal transcribed spacer of ladybird beetles (Coleoptera: Coccinellidae). Molecular Biology and Evolution 18, 648–660.CrossRefGoogle Scholar
Wu, X. Y., Chilton, N. B., Zhu, X. Q., Xie, M. Q. and Li, A. X. ( 2005). Molecular and morphological evidence indicates that Pseudorhabdosynochus lantauensis (Monogenea: Diplectanidae) represents two species. Parasitology 130, 669–677.CrossRefGoogle Scholar
Xiao, N., Qiu, J., Nakao, M., Li, T., Yang, W., Chen, X., Schantz, P. M., Craig, P. S. and Ito, A. ( 2005). Echinococcus shiquicus n.sp., a taeniid cestode from Tibetan fox and plateau pika in China. International Journal for Parasitology 35, 693–701.Google Scholar