Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-30T15:16:13.614Z Has data issue: false hasContentIssue false
  • English
  • Français

Phylogeography of Trichuris populations isolated from different Cricetidae rodents

Published online by Cambridge University Press:  20 August 2012

ROCÍO CALLEJÓN ,
MANUEL DE ROJAS ,
CARLOS FELIÚ ,
FRANCISCO BALAO ,
ÁNGELA MARRUGAL ,
HEIKKI HENTTONEN ,
DIEGO GUEVARA  and
CRISTINA CUTILLAS
ROCÍO CALLEJÓN
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
MANUEL DE ROJAS
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
CARLOS FELIÚ
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Barcelona, Barcelona, Spain
FRANCISCO BALAO
Affiliation:
Department of Plant Biology and Ecology, University of Seville, Apdo. 1095, E-41080 Seville, Spain
ÁNGELA MARRUGAL
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
HEIKKI HENTTONEN
Affiliation:
Finnish Forest Research Institute, Vantaa, Finland
DIEGO GUEVARA
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
CRISTINA CUTILLAS*
Affiliation:
Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Profesor García González 2, 41012 Seville, Spain
*
*Corresponding author: Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Seville, Prof. García González 2, 41012 Seville, Spain. Tel: +34954556773. Fax: +34954628162. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The phylogeography of Trichuris populations (Nematoda) collected from Cricetidae rodents (Muroidea) from different geographical regions was studied. Ribosomal DNA (Internal Transcribed Spacers 1 and 2, and mitochondrial DNA (cytochrome c- oxidase subunit 1 partial gene) have been used as molecular markers. The nuclear internal transcribed spacers (ITSs) 1 and 2 showed 2 clear-cut geographical and genetic lineages: one of the Nearctic region (Oregon), although the second was widespread throughout the Palaearctic region and appeared as a star-like structure in the minimum spanning network. The mitochondrial results revealed that T. arvicolae populations from the Palaearctic region were separated into 3 clear-cut geographical and genetic lineages: populations from Northern Europe, populations from Southern (Spain) and Eastern Europe (Croatia, Belarus, Kazahstan), and populations from Italy and France (Eastern Pyrénean Mountains). Phylogenetic analysis obtained on the basis of ITS1-5·8S-ITS2 rDNA sequences did not show a differential geographical structure; however, these markers suggest a new Trichuris species parasitizing Chionomys roberti and Cricetulus barabensis. The mitochondrial results revealed that Trichuris populations from arvicolinae rodents show signals of a post-glacial northward population expansion starting from the Pyrenees and Italy. Apparently, the Pyrenees and the Alps were not barriers to the dispersal of Trichuris populations.

Keywords

phylogeographyTrichuris arvicolaeNematodaribosomal DNAmitochondrial DNACricetidaerodents
Type
Research Article
Information
Parasitology , Volume 139 , Issue 13 , November 2012 , pp. 1795 - 1812
Copyright
Copyright © Cambridge University Press 2012

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, T. J. C., Blouin, M. S. and Beech, R. M. (1998). Population biology of parasitic nematodes: applications of genetic markers. Advances in Parasitology 41, 220–273.Google ScholarPubMed
Arrivillaga, J. C., Norris, D. E., Feliciangeli, M. D. and Lanzaro, G. C. (2002). Phylogeography of the neotropical sand fly Lutzomyia longipalpis inferred from mitochondrial DNA sequences. Infection, Genetics and Evolution 2, 83–95.CrossRefGoogle ScholarPubMed
Ås, S., Bengtsson, J. and Ebenhard, T. (1997). Archipelagoes and theories of insularity. Ecological Bulletins 46, 88–116.Google Scholar
Asmussen, M. A., Arnold, J. and Avise, J. C. (1987). Definition and properties of disequilibrium statics for associations between nuclear and cytoplasmic genotypes. Genetics 115, 755–768.CrossRefGoogle Scholar
Attwood, S. W. (2001). Schistosomiasis in the Mekong region: epidemiology and phylogeography. Advances in Parasitology 50, 87–152.CrossRefGoogle ScholarPubMed
Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Harvard University Press, Cambridge, MA, USA.CrossRefGoogle Scholar
Ballard, J. W. O. and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.CrossRefGoogle ScholarPubMed
Bandelt, H. J., Foster, P. and Röhl, A. (1999). Median-joining networks for inferring intraspecies phylogenies. Molecular Biology and Evolution 16, 37–48.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 ScholarPubMed
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1995). Host movement and genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.CrossRefGoogle ScholarPubMed
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. (1998). Substitution bias, rapid saturation and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 1719–27.CrossRefGoogle ScholarPubMed
Bowles, J. and McManus, D. P. (1993). Rapid discrimination of Echinococcus species and strains using a polymerase chain reaction-based RFLP method. Molecular and Biochemical Parasitology 57, 231–240.CrossRefGoogle ScholarPubMed
Burban, C., Petit, R. J., Carcreff, E. and Jactel, H. (1999). Rangewide variation of the maritime pine bast scale Matsucoccus feytaudi Duc. (Homoptera: Matsucoccidae) in relation to the genetic structure of its host. Molecular Ecology 8, 1593–1602.CrossRefGoogle Scholar
Callejón, R., de Rojas, M., Foronda, P., Feliú, C., Guevara, D. and Cutillas, C. (2010). Molecular evolution of Trichuris muris isolated from different Muridae hosts in Europe. Parasitology Research 107, 631–641.CrossRefGoogle ScholarPubMed
Cassens, I., Waerebeek, K., Best, P., Crespo, E., Reyes, J. and Milinkovitch, M. (2003). The phylogeography of dusky dolphins (Lagenorhynchus obscurus): a critical examination of network methods and rooting procedure. Molecular Ecology 12, 1781–1792.CrossRefGoogle Scholar
Chilton, N. B., Gasser, R. B. and Beveridge, I. (1995). Differences in a ribosomal DNA sequence of morphologically indistinguishable species within the Hypodontus macropi complex (Nematoda: Strongyloidea). International Journal for Parasitology 25, 647–651.CrossRefGoogle Scholar
Cutillas, C., Callejón, R., de Rojas, M., Tewes, B., Úbeda, J. M., Ariza, C. and Guevara, D. C. (2009). Trichuris suis and Trichuris trichiura are different nematode species. Acta Tropica 111, 299–307.CrossRefGoogle ScholarPubMed
Cutillas, C., de Rojas, M. and Ariza, C. (2007). Molecular identification of Trichuris vulpis and Trichuris suis isolated from different hosts. Parasitology Research 100, 383–389.CrossRefGoogle ScholarPubMed
Cutillas, C., Oliveros, R., de Rojas, M. and Guevara, D. (2002). Determination of Trichuris muris from murid hosts and T. arvicolae (Nematoda) from arvicolid rodents by amplification and sequentiation of the ITS1-5·8S-ITS2 segment of the ribosomal DNA. Parasitology Research 88, 574–582.CrossRefGoogle Scholar
Cutillas, C., Oliveros, R., de Rojas, M. and Guevara, D. C. (2004). Determination of Trichuris skrjabini by sequencing of the ITS1-5·8S-ITS2 segment of the ribosomal DNA: comparative molecular study of different species of trichurids. Journal of Parasitology 90, 648–652.CrossRefGoogle ScholarPubMed
Delicado, D., Ramos, M. and Machordom, A. (2010). Preliminary data on morphological VS molecular divergences between islands and iberian populations of freshwater genus Pseudamnicola Paulucci 1878 (Mollusca: Gastropoda: Hydrobiidae). In Islands and Evolution (ed. Perez–Mellado, V. and Ramon, C.). pp. 255–260.Google Scholar
Derycke, S., Backeljau, T., Vlaeminck, C., Vierstraete, A., Vanfleteren, J., Vincx, M. and Moens, T. (2007). Spatiotemporal analysis of population genetic structure in Geomonhystera disjuncta (Nematoda, Monhysteridae) reveals high levels of molecular diversity. Marine Biology 151, 1799–1812.CrossRefGoogle Scholar
Excoffier, L. and Lischer, H. E. L. (2010). Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564–567.CrossRefGoogle ScholarPubMed
Feliú, C., Spakulova, M., Casanova, J. C., Renaud, F., Morand, S., Hugot, J. P., Santalla, F. and Durand, P. (2000). Genetic and morphological heterogeneity in small rodent whipworms in Southwestern Europe: characterization of Trichuris muris and description of Trichuris arvicolae n. sp. (Nematoda: Trichuridae). Journal of Parasitology 86, 442–449.CrossRefGoogle Scholar
Fernández-Palacios, J. (2010). Why Islands? In Islands and Evolution (ed. Pérez-Mellado, V. and Ramón, C.), pp. 85–109. Institut Menorquí dÉstudis, Menorca, Spain.Google Scholar
Folinsbee, K. E. and Brooks, D. R. (2007). Miocene hominoid biogeography: pulses of dispersal and differentiation. Journal of Biogeography 34, 383–397.CrossRefGoogle Scholar
Gasser, R. B., Nansen, P. and Guldberg, P. (1996). Fingerprinting sequence variation in ribosomal DNA of parasites by DGGE. Molecular and Cellular Probes, 10, 99–105.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Haukisalmi, V., Hardman, L. M., Foronda, P., Feliu, C., Laakkonen, J., Niemimaa, J., Lehtonen, J. T. and Henttonen, H. (2010 b). Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from sequences of 28S ribosomal RNA. Zoologica Scripta 39, 631–641.CrossRefGoogle Scholar
Haukisalmi, V., Hardman, L. M., Hardman, M., Laakkonen, J., Niemimaa, J. and Henttonen, H. (2007). Morphological and molecular characterisation of Paranoplocephala buryatiensis n. sp. and P. longivaginata Chechulin & Gulyaev, 1998 (Cestoda: Anoplocephalidae) in Clethrionomys voles. Systematic Parasitology 66, 55–71.CrossRefGoogle Scholar
Haukisalmi, V., Hardman, L. M., Hardman, M., Rausch, R. L. and Henttonen, H. (2008). Molecular systematics of the Holarctic Anoplocephaloides variabilis (Douthitt, 1915) complex, with the proposal of Microcephaloides n. g. (Cestoda: Anoplocephalidae). Systematic Parasitology 70, 15–26.CrossRefGoogle Scholar
Haukisalmi, V., Hardman, L. M. and Henttonen, H. (2010 a). Taxonomic review of cestodes of the genus Catenotaenia Janicki, 1904 in Eurasia and molecular phylogeny of Catenotaeniidae (Cyclophyllidea). Zootaxa 2489, 1–33.CrossRefGoogle Scholar
Haukisalmi, V., Hardman, L. M., Henttonen, H., Laakkonen, J., Niemimaa, J., Hardman, M. and Gubányi, A. (2009). Molecular systematics and morphometrics of Anoplocephaloides dentata (Cestoda, Anoplocephalidae) and related species in voles and lemmings. Zoologica Scripta 38, 199–220.CrossRefGoogle Scholar
Haukisalmi, V. and Henttonen, H. (2001). Biogeography of helminth parasitism in Lemmus Link (Arvicolinae), with the description of Paranoplocephala fellmani n.sp. (Cestoda: Anoplocephalidae) from the Norwegian lemming L. lemmus (Linnaeus). Systematic Parasitology 49, 7–22.CrossRefGoogle Scholar
Haukisalmi, V., Henttonen, H. and Hardman, L. M. (2006). Taxonomy, diversity and zoogeography of Paranoplocephala spp. (Cestoda: Anoplocephalidae) in voles and lemmings of Beringia, with a description of three new species. Biological Journal of the Linnean Society 89, 277–299.CrossRefGoogle Scholar
Haukisalmi, V., Wickström, L. M., Hantula, J. and Henttonen, H. (2001). Taxonomy, genetic differentation and Holarctic biogeography of Paranoplocephala (Cestoda: Anoplocephalidae) in collared lemmings (Dicrostonyx; Arvicolinae). Biological Journal of the Linnean Society 74, 171–196.CrossRefGoogle Scholar
Haukisalmi, V., Wickström, L. M., Henttonen, H., Hantula, J. and Gubányi, A. (2004). Molecular and morphological evidence for multiple species within Paranoplocephala omphalodes (Hermann, 1783) (Cestoda: Anoplocephalidae) in Microtus-voles (Arvicolinae). Zoologica Scripta 33, 277–290.CrossRefGoogle Scholar
Hewitt, G. (1999). Postglacial recolonization of European Biota. Biological Journal of the Linnean Society 68, 87–112.CrossRefGoogle Scholar
Hu, M., Chilton, N. B., Abs El-Osta, Y. G. and Gasser, R. B. (2003). Comparative analysis of mitochondrial genome data for Necator americanus from two endemic regions reveals substantial genetic variation. International Journal for Parasitology 33, 955–963.CrossRefGoogle ScholarPubMed
Hu, M., Chilton, N. B., Zhu, X. and Gasser, R. B. (2002). Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase populations. Electrophoresis 23, 27–34.3.0.CO;2-7>CrossRefGoogle ScholarPubMed
Huang, W. F., Jiang, J. H., Chen, Y. W. and Wang, C. H. (2007). A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38, 30–37.CrossRefGoogle Scholar
Huelsenbeck, J. P. and Rannala, B. (1997). Phylogenetic methods come of age: Testing hypotheses in an evolutionary context. Science 276, 227–232.CrossRefGoogle Scholar
Huyse, T., Poulin, R. and Theron, A. (2005). Speciation in parasites: a population genetics approach. TRENDS in Parasitology 21, 469–475.CrossRefGoogle ScholarPubMed
Jaarola, M. and Searle, J. B. (2002). Phylogeography of field voles (Microtus agrestis) in Eurasia inferred from mitochondrial DNA sequences. Molecular Ecology 11, 2613–2621. info:pmid/12453244CrossRefGoogle ScholarPubMed
Jaarola, M. and Searle, J. B. (2004). A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe. Heredity 92, 228–234.CrossRefGoogle ScholarPubMed
Järvingen, O. and Ranta, E. (1987). Patterns and processes in species assemblages on Northern Baltic islands. Annales Zoologici Fennici 24, 249–411.Google Scholar
Kumazawa, Y. and Nishida, M. (1993). Sequence evolution of mitochondrial tRNA genes and deep-branch animal phylogenetics. Journal of Molecular Evolution 37, 380–398.CrossRefGoogle ScholarPubMed
Larkin, M. A., Blackshields, G. and Brown, N. P. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.CrossRefGoogle ScholarPubMed
Liu, F., Lu, J., Hu, W., Wang, S. Y., Cui, S. J., Chi, M., Yan, Q., Wang, X. R., Song, H. D. and Xu, X. N. (2006). New perspectives on host-parasite interplay by comparative transcriptomic and proteomic analyses of Schistosoma japonicum. PloS Pathogens 2, e29.CrossRefGoogle ScholarPubMed
Mas-Coma, S. and Bargues, M. D. (2009). Populations, hybrids and the systematic concepts of species and subspecies in Chagas disease triatomine vectors inferred from nuclear ribosomal and mitochondrial DNA. Acta Tropica 110, 112–136.CrossRefGoogle ScholarPubMed
Merkusheva, Y. V. and Bobkova, A. F. (1981). Helminths of domestic and wild animals of Bielorussia. Nauk Tech Minsk 118 pp.Google Scholar
Michaux, J. R., Magnanou, E., Paradis, E., Nieberding, C. and Libois, R. (2003). Mitochondrial phylogeography of the wood mouse (Apodemus sylvaticus) in the western Palaearctic region. Molecular Ecology 12, 685–697.CrossRefGoogle Scholar
Miranda, R. R., Tennessen, J. A., Blouin, M. S. and Rabelo, E. M. (2008). Mitochondrial DNA variation of the dog hookworm Ancylostoma caninum in Brazilian populations. Veterinary Parasitology 151, 61–67.CrossRefGoogle ScholarPubMed
Morgan, J. A. T. and Blair, D. (1998). Relative merits of nuclear ribosomal internal transcribed spacers and mitochondrial CO1 and ND1 genes for distinguishing among Echinostoma species (Trematoda). Parasitology 116, 289–297.CrossRefGoogle ScholarPubMed
Nadler, S. A., Lindquist, R. L. and Near, T. J. (1995). Genetic structure of midwestern Ascaris suum populations: a comparison of isoenzyme and RAPD markers. Journal of Parasitology 81, 385–394.CrossRefGoogle ScholarPubMed
Nagano, I., Wu, Z., Matsuo, A., Pozio, E. and Takahashi, Y. (1999). Identification of Trichinella isolates by polymerase chain reaction-restriction fragment length polymorphism of the mitochondrial cytochrome c-oxidase subunit I gene. International Journal for Parasitology 29, 1113–1120.CrossRefGoogle ScholarPubMed
Nieberding, C., Libois, R., Douady, C. J., Morand, S. and Michaux, J. R. (2005). Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palaearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology 14, 765–779.CrossRefGoogle Scholar
Nieberding, C., Morand, S., Libois, R. and Michaux, J. R. (2004). A parasite reveals cryptic phylogeographic history of its host. Proceedings of the Royal Entomological Society of London, Series B 271, 2559–2568.CrossRefGoogle ScholarPubMed
Niemelä, J., Ranta, E. and Haila, Y. (1985). Carabid beetles in lush forest patches on the Åland Islands, south-west Finland: an island-mainland comparison. Journal of Biogeography 12, 109–120.CrossRefGoogle Scholar
Nieminen, M. and Hanski, I. (1998). Metapopulations of moths on islands: a test of two contrasting models. Journal of Animal Ecology 67, 149–160.CrossRefGoogle Scholar
Nylander, J. A. A. (2008). MrModeltest 2·3 README. http://www.abc.se/∼nylander/mrmodeltest2/mrmodeltest2.html. Accessed 22 May 2008.Google Scholar
Otranto, D., Testini, G., de Luca, F., Hu, M., Shamsi, S. and Gasser, R. B. (2005). Analysis of genetic variability within Thezalia callipaeda (Nematoda: Thelazioidea) from Europe and Asia by sequencing and mutation scanning of mitocondrial cytochrome c oxidase subunit 1 gene. Molecular and Cellular Probes 19, 306–313.CrossRefGoogle Scholar
Page, R. D. M. and Holmes, E. C. (1998). Molecular Evolution: A phylogenetic Approach. Blackwell Science, Oxford, UK.Google Scholar
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.CrossRefGoogle ScholarPubMed
Posada, D. and Buckley, T. R. (2004). Model selection and model averaging in phylogenetics: Advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Systems Biology 53, 793–808.CrossRefGoogle ScholarPubMed
Price, P. W. (1980). Evolutionary Biology of Parasites. Princeton University Press, Princeton, NJ, USA.Google ScholarPubMed
Rambaut, A. and Drummond, A. (2007). Tracer v1·4. Available from http://beast.bio.ed.ac.uk/.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.CrossRefGoogle ScholarPubMed
Rozas, J. and Rozas, R. (1997). DNASP (version 2.0): a novel software package for extensive molecular population genetic analysis. Computer Applications in the Biosciensce 13, 307–311.Google Scholar
Seddon, N., Tobias, J. A., Yount, J. W., Butchart, S. H. M., Ramanampamonjy, J. R. and Randrianizahana, H. (2001). Conservation issues and priorities in the Mikea Forest of south-west Madagascar. Oryx 34, 287–304.CrossRefGoogle Scholar
Slatkin, M. and Hudson, R. R. (1991). Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129, 555–562.CrossRefGoogle ScholarPubMed
Stevenson, L. A., Chilton, N. B. and Gasser, R. B. (1995). Differentiation of Haemonchus placei from H. contortus (Nematoda: Trichostrongylidae) by the ribosomal DNA second internal transcribed spacer. International Journal for Parasitology 25, 483–488.CrossRefGoogle Scholar
Subbotin, S. A., Vierstraete, A., de Ley, P., Rowe, J., Waeyenberge, L., Moens, M. and Vanfleteren, J. R. (2001). Phylogenetic relationships within the cyst-forming nematodes (Nematoda, Heteroderidae) based on analysis of sequences from the ITS region of ribosomal DNA. Molecular Phylogenetics and Evolution 21, 1–16.CrossRefGoogle ScholarPubMed
Sukhdeo, S. C., Sukhdeo, M. V. K., Black, M. B. and Vrijenhoek, R. C. (1997). The evolution of tissue migration in parasitic nematodes (Nematoda: Strongylida) inferred from a protein-coding mitochondrial gene. Biological Journal of the Linnean Society 61, 281–298.CrossRefGoogle Scholar
Taberlet, P., Fumagalli, L., Wust-Saucy, A. G. and Cosson, J-F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453–464.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, doi: 10.1093/molbev/msr121.CrossRefGoogle ScholarPubMed
Tenora, F. (1967). The helminthfauna of small rodents of the Rohacskadolina Valley (Liptovske Hole Mts., Slovakia). Acta Scientiarum Naturalium Academiae Brno 1, 29–68.Google Scholar
Traversa, D., Kuzmina, T., Kharchenko, V. A., Iorio, R., Klei, T. R. and Otranto, D. (2008). Haplotypic variability within the mitochondrial gene encoding for the cytochrome c oxidase 1 (cox1) of Cylicocyclus nassatus (Nematoda, Strongylida): evidence for an affiliation between parasitic populations and domestic and wild equid hosts. Veterinary Parasitology 156, 241–247.CrossRefGoogle ScholarPubMed
Turner, T. F., Trexler, J. C., Harris, J. L. and Haynes, J. L. (2000). Nested cladistic analysis indicates population fragmentation shapes genetic diversity in a freshwater mussel. Genetics 154, 777–785.CrossRefGoogle Scholar
Wikstrom, N., Savolainen, V. and Chase, M. W. (2003). Angiosperm divergence times: congruence and incongruence between fossils and sequence divergence estimates. In Telling the Evolutionary Time: Molecular Clocks and the Fossil Record (ed. Donoghue, P. C. J. and Smith, M. P.), pp.142–165. Taylor & Francis, London, UK.Google Scholar
Wilson, D. E. and Reeder, D. M. (2005). Mammal Species of the World, a Taxonomic and Geographic Reference, 3rd Edn.The Johns Hopkins University Press, Baltimore, MD, USA.CrossRefGoogle Scholar
Wu, S. G., Wang, G. T., Xi, B. W., Xiong, F., Liu, T. and Nie, P. (2009). Population genetic structure of parasitic nematode Camallanus cotti inferred form DNA sequences of ITS1 rDNA and mitochondrial COI gene. Veterinary Parasitology 164, 248–256.CrossRefGoogle Scholar
Zhou, C., Li, M., Yuan, K., Hu, N. and Peng, W. (2011). Phylogeography of Ascaris lumbricoides and A. Suum from China. Parasitology Research 2, 329–338.CrossRefGoogle Scholar