Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-12-01T01:15:29.403Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology

Published online by Cambridge University Press:  01 February 2011

STEVEN A. NADLER  and
GERARDO PÉREZ-PONCE DE LEÓN
STEVEN A. NADLER*
Affiliation:
Department of Nematology, University of California, One Shields Avenue, Davis, California, 95616-8668, USA
GERARDO PÉREZ-PONCE DE LEÓN
Affiliation:
Departamento de Zoologia. Instituto de Biología, Universidad Nacional Autónoma de México, Ap. Postal 70-153, C.P. 04510, México D.F.
*
*Corresponding author: Department of Nematology, University of California, One Shields Avenue, Davis, California, 95616-8668, USA. Tel: +530 7522121. Fax: +530-752-5674. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Herein we review theoretical and methodological considerations important for finding and delimiting cryptic species of parasites (species that are difficult to recognize using traditional systematic methods). Applications of molecular data in empirical investigations of cryptic species are discussed from an historical perspective, and we evaluate advantages and disadvantages of approaches that have been used to date. Developments concerning the theory and practice of species delimitation are emphasized because theory is critical to interpretation of data. The advantages and disadvantages of different molecular methodologies, including the number and kind of loci, are discussed relative to tree-based approaches for detecting and delimiting cryptic species. We conclude by discussing some implications that cryptic species have for research programmes in parasitology, emphasizing that careful attention to the theory and operational practices involved in finding, delimiting, and describing new species (including cryptic species) is essential, not only for fully characterizing parasite biodiversity and broader aspects of comparative biology such as systematics, evolution, ecology and biogeography, but to applied research efforts that strive to improve development and understanding of epidemiology, diagnostics, control and potential eradication of parasitic diseases.

Keywords

Biodiversitycryptic speciesspecies delimitationmolecular systematics
Type
Research Article
Information
Parasitology , Volume 138 , Special Issue 13: Systematics as a cornerstone of parasitology , November 2011 , pp. 1688 - 1709
Copyright
Copyright © Cambridge University Press 2011

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

Adams, B. J. (1998). Species concepts and the evolutionary paradigm in modern nematology. Journal of Nematology 30, 1–21.Google Scholar
Adams, B. J. (2002). The species delimitation uncertainty principle. Journal of Nematology 33, 153–160.Google Scholar
Aho, J. M., Mulvey, M., Jacobson, K. M. and Esch, G. W. (1992). Genetic differentiation among congeneric acanthocephalans in the yellow-bellied slider turtle. Journal of Parasitology 78, 974–981.CrossRefGoogle Scholar
Anderson, G. R. and Barker, S. C. (1993). Species differentiation in the didymozoidea (Digenea): Restriction fragment length differences in internal transcribed spacers 5·8S ribosomal DNA. International Journal for Parasitology 23, 133–136.CrossRefGoogle ScholarPubMed
Anderson, T. J. C., Blouin, M. S. and Beech, R. N. (1998). Population biology of parasitic nematodes: Applications of genetic markers. Advances in Parasitology 41, 219–283.CrossRefGoogle ScholarPubMed
Andrews, R. H., Beveridge, I., Adams, A. and Baverstock, P. R. (1988). Identification of life cycle stages of the nematode Echinocephalus overstreeti by allozyme electrophoresis. Journal of Helminthology 62, 153–157. doi: 10.1017/S0022149X0001141X.CrossRefGoogle ScholarPubMed
Andrews, R. H. and Chilton, N. B. (1999). Multilocus enzyme electrophoresis: a valuable technique for providing answers to problems in parasite systematics. International Journal for Parasitology 29, 213–253.Google ScholarPubMed
Andrews, R. H., Monis, P. T., Ey, P. L. and Mayrhofer, G. (1998). Comparison of the levels of intra-specific genetic variation within Giardia muris and Giardia intestinalis. International Journal for Parasitology 28, 1179–1185.CrossRefGoogle ScholarPubMed
Avise, J. C. (1994). Molecular Markers, Natural History and Evolution. Chapman and Hall, New York.CrossRefGoogle Scholar
Avise, J. C. (2000). Phylogeography: The History and Formation of Species. Cambridge, Harvard University Press.CrossRefGoogle Scholar
Ba, C. T., Wang, X. Q., Renaud, F., Euzet, L., Marchand, B. and De Meeûs, T. (1994). Diversity in the genera Avitellina and Thysaniezia (Cestoda: Cyclophylloidea): Genetic evidence. Journal of the Helminthological Society of Washington 61, 57–60.Google Scholar
Baldwin, J. G., Nadler, S. A. and Freckman, D. W. (1999). Nematodes – pervading the earth and linking all life. In Proceedings of the Second National Forum on Biodiversity, Nature and Human Society: The Quest for a Sustainable World (eds. Raven, P. H. and Williams, T.), pp. 176–191. National Academy Press.Google Scholar
Ballard, J. W. O. and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729–744.CrossRefGoogle ScholarPubMed
Baverstock, P. R., Adams, M. and Beveridge, I. (1985). Biochemical differentiation in bile duct cestodes and their marsupial hosts. Molecular Biology and Evolution 2, 321–337.Google ScholarPubMed
Bell, A. S. and Sommerville, C. (2002). Molecular evidence for the synonymy of two species of Apatemon Szidat, 1928, A. gracilis (Rudolphi, 1819) and A. annuligerum (von Nordmann, 1832) (Digenea: Strigeidae) parasitic as metacercariae in British fishes. Journal of Helminthology 76, 193–198. doi:10.1079/JOH2002120.CrossRefGoogle Scholar
Bensasson, D., Zhang, D., Hartl, D. L. and Hewitt, G. M. (2001). Mitochondrial pseudogenes: evolution's misplaced witnesses. Trends in Ecology and Evolution 16, 314–321.CrossRefGoogle ScholarPubMed
Bensch, S., Perez-Tris, J., Waldenstrom, J. and Hellgren, O. (2004). Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: Multiple cases of cryptic speciation? Evolution 58, 1617–1621.Google ScholarPubMed
Beveridge, I., Chilton, N. B. and Andrews, R. H. (1993). Sibling species within Macropostrongyloides baylisi (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology 23, 21–33.CrossRefGoogle ScholarPubMed
Bickford, D., Lohman, D. J., Sodhi, N. S., Ng, P. K. L., Meier, R., Winker, K., Ingram, K. K. and Das, I. (2007). Cryptic diversity as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148–155. doi:10.1016/j.tree.2006.11.004.CrossRefGoogle ScholarPubMed
Blasco-Costa, I., Balbuena, J. A., Raga, J. A., Kostadinova, A. and Olson, P. D. (2009). Molecules and morphology reveal cryptic variation among digeneans infecting sympatric mullets in the Mediterranean. Parasitology 137, 287–302. doi:10.1017/S0031182009991375.CrossRefGoogle ScholarPubMed
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. (1998). Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 1719–1727.CrossRefGoogle ScholarPubMed
Bouzid, W., Štefka, J., Hypša, V., Lek, S., Scholz, T., Legal, L., Kalthoum, O., Hassine, B. and Loot, G. (2008). Geography and host specificity: two forces behind the genetic structure of the freshwater fish parasite Ligula intestinalis (Cestoda: Diphyllobothriidae). International Journal for Parasitology 38, 1465–1479.CrossRefGoogle ScholarPubMed
Brooks, D. R. (1979). Testing the context and extent of host–parasite co-evolution. Systematic Zoology 28, 299–307.CrossRefGoogle Scholar
Brooks, D. R. (1981). Hennig's parasitological method: a proposed solution. Systematic Biology 30, 229–249.CrossRefGoogle Scholar
Brooks, D. R. and Hoberg, E. P. (2000). Triage for the biosphere: the need and rationale for taxonomic inventories and phylogenetic studies of parasites. Comparative Parasitology 67, 1–25.Google Scholar
Brooks, D. R. and McLennan, D. A. (1993). Parascript: Parasites and the Language of Evolution. Smithsonian Institution Press, Washington, D.C.Google Scholar
Bullini, L., Arduino, P., Cianchi, R., Nascetti, G., D'Amelio, S., Mattiucci, S., Paggi, L., Orecchia, P., Plotz, J., Berland, B., Smith, J. W. and Brattey, J. (1997). Genetic and ecological research on Anisakid endoparasites of fish and marine mammals in the Antarctic and Arctic-boreal regions. In Antarctic Communities: Species, Structure and Survival (eds. Battaglia, B., Valencia, J. and Walton, D. W. H.). pp. 39–44. Cambridge University Press, Cambridge, U.K.Google Scholar
Bullini, L., Nascetti, G., Ciafre, S., Rumore, F., Biocca, E., Montalenti, S. and Rita, G. (1978). Ricerche cariologiche ed elettroforetiche su Parascaris univalens e Parascaris equorum. Atti della Accademia Nazionale dei Lincei Rendiconti Classe di Scienze Fisiche Matematiche e Naturali 65, 151–156.Google Scholar
Bush, S. E., Price, R. D. and Clayton, D. H. (2009). Descriptions of eight new species of feather lice in the genus Columbicola (Phthiraptera: Philopteridae), with a comprehensive world checklist. Journal of Parasitology 95, 286–294. doi:10.1645/GE-1799.1.CrossRefGoogle ScholarPubMed
Cantacessi, C., Riddell, S., Morris, G. M., Doran, T., Woods, W. G., Otranto, D. and Gasser, R. B. (2008). Genetic characterization of the three unique operational taxonomic units of Eimeria from chickens in Australia based on nuclear spacer ribosomal DNA. Veterinary Parasitology 152, 226–234. doi:10.1016/j.vetpar.2007.12.028.CrossRefGoogle ScholarPubMed
Cepicka, I., Kutišova, K., Tachezy, J., Kulda, J. and Flegr, J. (2005). Cryptic species within the Tetratrichomonas gallinarum species complex revealed by molecular polymorphism. Veterinary Parasitology 128, 11–21.CrossRefGoogle ScholarPubMed
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.Google ScholarPubMed
Chilton, N. B., Beveridge, I. and Andrews, R. H. (1992). Detection by allozyme electrophoresis of cryptic species Hypodontus macropi (Nematoda: Strongyloidea) from macropodid marsupials. International Journal for Parasitology 22, 271–279.CrossRefGoogle ScholarPubMed
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
Chilton, N. B., O'Callaghan, M. G., Beveridge, I. and Andrews, R. H. (2007). Genetic markers to distinguish Moniezia expansa from M. benedeni (Cestoda: Anoplocephalidae) and evidence of the existence of cryptic species in Australia. Parasitology Research 100, 1187–1192. doi:10.1007/s00436-006-0388-4.CrossRefGoogle Scholar
Christensen, C. M., Zarlenga, D. S. and Gasbarre, L. C. (1994). Ostertagia, Haemonchus, Cooperia and Oesophagostomum: construction and characterization of genus-specific DNA probes to differentiate important parasites of cattle. Experimental Parasitology 78, 93–100.CrossRefGoogle ScholarPubMed
Conn, J. E., Mitchell, S. E. and Cockburn, A. F. (1997). Mitochondrial DNA variation within and between two species of neotropical anopheline mosquitoes (Diptera: Culicidae). Journal of Heredity 88, 98–107.CrossRefGoogle ScholarPubMed
Corliss, J. O. (1999). Biodiversity, classification, and numbers of species of protists. In Proceedings of the Second National Forum on Biodiversity, Nature and Human Society: The Quest for a Sustainable World (eds. Raven, P. H. and Williams, T.), pp. 130–155. National Academy Press.Google Scholar
Criscione, C. D. and Blouin, M. S. (2004). Life cycles shape parasite evolution: Comparative population genetics of salmon trematodes. Evolution 58, 198–202. doi:10.1554/03-359.Google ScholarPubMed
Criscione, C. D. and Blouin, M. S. (2007). Parasite phylogeographical congruence with salmon host evolutionarily significant units: implications for salmon conservation. Molecular Ecology 16, 993–1005. doi:10.1111/j.1365-294X.2006.03220.x.CrossRefGoogle ScholarPubMed
Criscione, C. D., Poulin, R. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257. doi:10.1111/j.1365-294X.2005.02587.x.CrossRefGoogle ScholarPubMed
Dallas, J. F., Irvine, R. J. and Halvorsen, O. (2000). DNA evidence that Ostertagia gruehneri and O. arctica (Nematoda: Ostertagiinae) in reindeer from Norway and Svalbard are conspecific. International Journal for Parasitology 30, 655–658.CrossRefGoogle Scholar
Dame, J. B., Yowell, C. A., Courtney, C. H. and Lindren, W. G. (1991). Cloning and characterization of the ribosomal RNA repeat from Ostertagia ostertagi. Molecular and Biochemical Parasitology 45, 275–280.CrossRefGoogle ScholarPubMed
Davis, J. I. and Nixon, K. C. (1992). Populations, genetic variation, and the delimitation of phylogenetic species. Systematic Biology 41, 421–435.CrossRefGoogle Scholar
DeSalle, R., Egan, M. G. and Siddal, M. (2005). The unholy trinity: taxonomy, species delimitation and DNA barcoding. Philosophical Transactions of the Royal Society B 360, 1905–1926. doi:10.1098/rstb.2005.1722.CrossRefGoogle ScholarPubMed
Desdevises, Y., Jovelin, R., Jousson, O. and Morand, S. (2000). Comparison of ribosomal DNA sequences of Lamellodiscus spp. (Monogenea, Diplectanidae) parasitising Pagellus (Sparidae, Teleostei) in the North Mediterranean Sea: Species divergence and coevolutionary interactions. International Journal for Parasitology 30, 741–746.CrossRefGoogle ScholarPubMed
Donald, K. M., Kennedy, M., Poulin, R. and Spencer, H. G. (2004). Host specificity and molecular phylogeny of larval Digenea isolated from New Zealand and Australian topshells (Gastropoda: Trochidae). International Journal for Parasitology 34, 557–568.CrossRefGoogle ScholarPubMed
Donald, K. M., Sijnja, A. and Spencer, H. G. (2007). Species assignation amongst morphologically cryptic larval Digenea isolated from New Zealand topshells (Gastropoda: Trochidae). Parasitology Research 101, 433–441. doi:10.1007/s00436-007-0501-3.CrossRefGoogle ScholarPubMed
Doyle, J. (1995). The irrelevance of allele tree topologies for species delimitation, and a non-topological alternative. Systematic Botany 20, 574–588.CrossRefGoogle Scholar
Farris, J. S., Källersjö, A., Kluge, A. R. and Bult, C. (1994). Testing significance of incongruence. Cladistics 10, 315–319.CrossRefGoogle Scholar
Felsenstein, J. (1988). Phylogenies from molecular sequences: Inference and reliability. Annual Review of Genetics 22, 521–565.CrossRefGoogle ScholarPubMed
Felsenstein, J. (2004). Inferring Phylogenies. Sinauer Associates, Inc. Sunderland, Massachusetts.Google Scholar
Ferri, E., Barbuto, M., Bain, O., Galimberti, A. Shigehiko, Guerrero, R., Ferté, H., Bandi, C., Martin, C. and Casiraghi, M. (2009). Integrated taxonomy: Traditional approach and DNA barcoding for the identification of filarioid worms and related parasites (Nematoda). Frontiers in Zoology 6, 1. doi:10.1186/1742-9994-6-1.CrossRefGoogle ScholarPubMed
Flockhart, A. and Denham, A. (1984). Differentiation of species and life cycle stages of Brugia spp. by isoenzyme analysis. Journal of Parasitology 70, 378–384.CrossRefGoogle ScholarPubMed
Gasser, R. B. and Hoste, H. (1995). Genetic markers for closely-related parasitic nematodes. Molecular and Cellular Probes 9, 315–320.CrossRefGoogle ScholarPubMed
Glennon, V., Perkins, E. M., Chisholm, L. A. and Whittington, I. (2008). Comparative phylogeography reveals host generalists, specialists and cryptic diversity: Hexabothriid, microbothriid and monocotylid monogeneans from rhinobatid rays in southern Australia. International Journal for Parasitology 38, 1599–1612. doi:10.1016/j.ijpara.2008.05.017.CrossRefGoogle ScholarPubMed
Goater, T. M., Mulvey, M and Esch, G. W. (1990). Electrophoretic differentiation of two Halipegus species (Trematoda: Hemiuridae) congeners in an amphibian population. Journal of Parasitology 76, 431–434.CrossRefGoogle Scholar
Goldstein, P. Z., DeSalle, R., Amato, G. and Vogler, A. P. (2000). Conservation genetics at the species boundary. Conservation Biology 14, 120–131. doi:10.1046/j.1523-1739.2000.98122.x.CrossRefGoogle Scholar
Good, D. A. and Wake, D. B. (1992). Geographic variation and speciation in the torrent salamanders of the genus Rhyacotriton (Caudata: Rhyacotritonidae). University of California Publications in Zoology 126, 1–91.Google Scholar
Grillo, V., Jackson, F., Cabaret, J. and Gilleard, J. S. (2007). Population genetic analysis of the ovine parasitic nematode Teladorsagia circumcincta and evidence for a cryptic species. International Journal for Parasitology 37, 435–447. doi:10.1016/j.ijpara.2006.11.014.CrossRefGoogle ScholarPubMed
Hansen, H., Bakke, T. A. and Bachmann, L. (2007). DNA taxonomy and barcoding of monogenean parasites: lessons from Gyrodactylus. Trends in Parasitology 23, 363–367. doi:10.1016/j.pt.2007.06.007.CrossRefGoogle ScholarPubMed
Hebert, P. D., Cywinska, A., Ball, S. L. and deWaard, J. R. (2003). Biological identifications through DNA barcodes. Proceedings of the Royal Society (Biological Sciences Series) 270, 313–321. doi: 10.1098/rspb.2002.2218.Google ScholarPubMed
Hebert, P. D., Stoeckle, M. Y., Zemlak, T. S. and Francis, C. M. (2004). Identification of Birds through DNA Barcodes. PLoS Biol 2, e312. doi:10.1371/journal.pbio.0020312.CrossRefGoogle ScholarPubMed
Hennig, W. (1966). Phylogenetic Systematics. University of Illinois Press, Urbana, IL.Google Scholar
Henry, C. S. (1985). Sibling species, call differences, and speciation in green lacewings (Neuroptera: Chrysopidae: Chrysoperla). Evolution 39, 965–984.Google ScholarPubMed
Hoberg, E. P. (2002). Foundations for an integrative parasitology: Collections, archives and biodiversity informatics. Comparative Parasitology 69, 124–131.CrossRefGoogle Scholar
Hoberg, E. P. and Brooks, D. R. (2008). A macroevolutionary mosaic: Episodic host-switching, geographical colonization and diversification in complex host–parasite systems. Journal of Biogeography 35, 1533–1550. doi:10.1111/j.1365-2699.2008.01951.x.CrossRefGoogle Scholar
Hoberg, E. P., Pilitt, P. A. and Galbreath, K. E. (2009). Why museums matter: A tale of pinworms (Oxyuroidea: Heteroxynematidae) among pikas (Ochotona princeps and O. collaris) in the American West. Journal of Parasitology 95, 490–501. doi:10.1645/GE-1823.1.CrossRefGoogle Scholar
Hoelzer, G. A. (1997). Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51, 622–626.CrossRefGoogle ScholarPubMed
Hung, G. C., Chilton, N. B., Beveridge, I., McDonnell, A., Lichtenfels, J. R. and Gasser, R. B. (1997). Molecular delineation of Cylicocyclus nassatus and C. ashworthi (Nematoda: Strongylidae). International Journal for Parasitology 27, 601–605.CrossRefGoogle Scholar
Hung, C. G., Chilton, N. B., Beveridge, I., Zhu, Q. L., Lichtenfels, J. R. and Gasser, R. B. (1999). Molecular evidence for cryptic species within Cylicostephanus minutus (Nematoda: Strongylidae). International Journal for Parasitology 29, 285–291.CrossRefGoogle ScholarPubMed
Jackson, J., Chilton, N. B., Beveridge, I., Morris, M. and Andrews, R. H. (1998). An electrophoretic comparison of the Australian paralysis tick, Ixodes holocyclus Neumann, 1899, with I. cornuatus Roberts, 1960 (Acari: Ixididae). Australian Journal of Zoology 46, 109–117. doi:0004-959X/98/02010.CrossRefGoogle Scholar
Johnson, K. P., Reed, D. L., Parker, S. L. H., Kim, D. and Clayton, D. H. (2007). Phylogenetic analysis of nuclear and mitochondrial genes supports species groups for Columbicola (Insecta: Phthiraptera). Molecular Phylogenetics and Evolution 45, 506–518. doi:10.1016/j.ympev.2007.07.005.CrossRefGoogle ScholarPubMed
Koehler, A. V., Hoberg, E. P., Dokuchaev, N. E. and Cook, J. A. (2007). Geographic and host range of the nematode Soboliphyme baturini across Beringia. Journal of Parasitology 93, 1070–1083. doi:10.1645/GE-1182R.1.CrossRefGoogle ScholarPubMed
Knapp, S. (2008). Taxonomy as a team sport. In The New Taxonomy (ed. Wheeler, Q. W.), pp. 95–127. CRC Press, Boca Raton, Florida.Google Scholar
Knowlton, N. (1986). Cryptic and sibling species among the decapod crustaceans. Journal of Crustacean Biology 6, 356–363.CrossRefGoogle Scholar
Krone, O., Friedrich, D. and Honisch, M. (2007). Specific status and pathogenicity of syngamid nematodes in bird species (Ciconiformes, Falconiformes, Gruiformes) from Germany. Journal of Helminthology 81, 67–73. doi:10.1017/S0022149X07214129.CrossRefGoogle ScholarPubMed
La Rosa, G., Pozio, E., Rossi, P. and Murrell, K. D. (1992). Allozyme analysis of Trichinella isolates from various host species and geographical regions. Journal of Parasitology 78, 641–646.CrossRefGoogle ScholarPubMed
Lavikainen, A., Haukisalmi, V., Lehtinen, M. J., Laaksonen, S., Holmström, S., Isomursu, M., Oksanen, A. and Meri, S. (2010). Mitochondrial DNA data reveal cryptic species within Taenia krabbei. Parasitology International 59, 290–293. doi:10.1016/j.parint.2010.03.003.CrossRefGoogle ScholarPubMed
León-Règagnon, V., Guillén-Hernández, S. and Arizmendi-Espinosa, M. A. (2005). Intraspecific variation of Haematoloechus floedae Harwood, 1932 (Digenea: Plagiorchiidae), from Rana spp. in North and Central America. Journal of Parasitology 91, 915–921. doi:10.1645/GE-430R.1.CrossRefGoogle ScholarPubMed
Leung, T. L. F., Keeney, D. B. and Poulin, R. (2009). Cryptic species complexes in manipulative echinostomatid trematodes: When two become six. Parasitology 136, 241–252. doi:10.1017/S0031182008005374.CrossRefGoogle ScholarPubMed
Lewontin, R. C. and Hubby, J. L. (1966). A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54, 595–609.CrossRefGoogle Scholar
Li, J. and Liao, X. (2003). The taxonomic status of Diagramma (Pseudophyllidea: Ligulidae) inferred from DNA sequences. Journal of Parasitology 89, 792–799. doi:10.1645/GE-3078.CrossRefGoogle Scholar
Light, J. E. and Hafner, M. S. (2007). Cophylogeny and disparate rates of evolution in sympatric lineages of chewing lice on pocket gophers. Molecular Phylogenetics and Evolution 45, 997–1013. doi:10.1016/j.ympev.2007.09.001.CrossRefGoogle ScholarPubMed
Littlewood, D. T. J., Rohde, K. and Clough, K. A. (1997). Parasite speciation within or between host species? Phylogenetic evidence from site-specific polystome monogeneans. International Journal for Parasitology 27, 1289–1297.CrossRefGoogle ScholarPubMed
Locke, S., Mclaughlin, J. D. and Marcogliese, D. J. (2010). 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, Canada. Molecular Ecology 19, 2813–2827. doi:10.1111/j.1365-294X.2010.04713.x.CrossRefGoogle Scholar
Malenke, J. R., Johnson, K. P. and Clayton, D. H. (2009). Host specialization differentiates cryptic species of feather-feeding lice. Evolution 63, 1427–1438.CrossRefGoogle ScholarPubMed
Martínez-Aquino, A., Reyna-Fabián, M. E., Rosas-Valdez, R., Razo-Mendivil, U., Pérez-Ponce de León, G. and García-Varela, M. (2009). Detecting a complex of cryptic species within Neoechynorhynchus golvani (Acanthocephala: Neoechynorhynchidae) inferred from ITS and LSU rDNA gene sequences. Journal of Parasitology 95, 1040–1047. doi:10.1645/GE-1926.1.CrossRefGoogle Scholar
Mattiucci, S. and Nascetti, G. (2008). Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.CrossRefGoogle ScholarPubMed
Mattiucci, S., Nascetti, G., Bullini, L., Orecchia, P. and Paggi, L. (1986). Genetic structure of Anisakis physeteris, and its differentiation from the Anisakis simplex complex (Ascaridida, Anisakidae). Parasitology 93, 383–387.CrossRefGoogle ScholarPubMed
Mayden, R. L. (1997). A hierarchy of species concepts: the denouement in the saga of the species problem. In Species: The Units of Biodiversity (ed. Claridge, M. F., Dawah, H. A. and Wilson, M. R), pp. 381–424. Chapman and Hall, London & New York.Google Scholar
Mayr, E. (1963). Animal Species and Evolution. Harvard University Press. Cambridge, Massachusetts.CrossRefGoogle Scholar
Mayxay, M., Pukrittayakamee, S., Newton, P. and White, N. J. (2004). Mixed-species malaria infections in humans. Trends in Parasitology 20, 233–240.CrossRefGoogle ScholarPubMed
McManus, D. P. (1990). Characterisation of taeniid cestodes by DNA analysis. Revue Scientifique et Technique de I'Office International des Epizooties 9, 489–510.CrossRefGoogle ScholarPubMed
McManus, D. P. and Bowles, J. (1996). Molecular genetic approaches to parasite identification: their value in diagnostic parasitology and systematic. International Journal for Parasitology 26, 687–704.CrossRefGoogle Scholar
Meier, R. (2008). DNA sequences in taxonomy: Opportunities and challenges. In The New Taxonomy (ed. Wheeler, Q. W.), pp. 95–127. CRC Press, Boca Raton, Florida.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. doi:10.1016/j.vetpar.2007.09.027.CrossRefGoogle ScholarPubMed
Miura, O., Kuris, A. M., Torchin, M. E., Hechinger, R. F., Dunham, E. J. and Chiba, D. S. (2005). Molecular-genetic analyses reveal cryptic species of trematodes in the intertidal gastropod, Batillaria cumingi (Crosse). International Journal for Parasitology 35, 793–801. doi:10.1016/j.ijpara.2005.02.014.CrossRefGoogle ScholarPubMed
Moszczynska, A., Locke, S. A., McLaughlin, D. N., Marcogliese, D. J. and Crease, T. J. (2009). Development of primers for the mitochondrial cytocherome c oxidase I gene in digenetic trematodes (Platyhelminthes) illustrates the challenge of barcoding parasitic helminths. Molecular Ecology Resources 9 (suppl. 1), 75–82. doi:10.1111/j.1755–0998.2009.02634.x.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1987 a). Biochemical and immunological systematics of some ascaridoid nematodes: genetic divergence between congeners. Journal of Parasitology 73, 811–816.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1987 b). Genetic variability in endoparasitic helminths. Parasitology Today 3, 154–155.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1990). Molecular approaches to studying helminth population genetics and phylogeny. International Journal for Parasitology 20, 11–29.CrossRefGoogle ScholarPubMed
Nadler, S. A. (1995). Microevolution and the genetic structure of parasite populations. Journal of Parasitology 81, 395–403.CrossRefGoogle ScholarPubMed
Nadler, S. A. (2002). Species delimitation and nematode biodiversity: Phylogenies rule. Nematology 4, 615–625.CrossRefGoogle Scholar
Nadler, S. A., Adams, B. J., Lyons, E. T., DeLong, R. L. and Melin, S. R. (2000). Molecular and morphometric evidence for separate species of Uncinaria (Nematoda: Ancylostomatidae) in California sea lions and northern fur seals: Hypothesis testing supplants verification. Journal of Parasitology 86, 1099–1106. doi:10.1645/0022-3395.CrossRefGoogle ScholarPubMed
Nadler, S. A., De Ley, P., Mundo-Ocampo, M., Smythe, A., Stock, P., Bumbarger, D., Adams, B. J., De Ley, I. T., Holovachov, O. and Baldwin, J. G. (2006). Phylogeny of Cephalobina (Nematoda): Molecular evidence for recurrent evolution of probolae and incongruence with traditional classification. Molecular Phylogenetics and Evolution 40, 696–711. doi: 10.1016/j.ympev.2006.04.005.CrossRefGoogle Scholar
Nascetti, G., Cianchi, R., Mattiucci, S., D´Amelio, S., Orecchia, P., Paggi, L., Brattey, J., Berland, B., Smith, J. W. and Bullini, B. (1993). Three sibling species within Contracecum osculatum (Nematoda: Ascaridida: Ascaridoidea) from the Atlantic Arctic-Boreal region: Reproductive isolation and host preferences. International Journal for Parasitology 23, 105–120.CrossRefGoogle Scholar
Nascetti, G., Grappelli, C., Bullini, L. and Montalenti, S. G. (1979). Ricerche sul differenziamento genetico di Ascaris lumbricoides e Ascaris suum. Atti della Accademia Nazionale dei Lincei Rendiconti Classe di Scienze Fisiche Matematiche e Naturali 67, 457–465.Google Scholar
Nascetti, G., Paggi, L., Orecchia, P., Smith, J. W., Mattiucci, S. and Bullini, L. (1986). Electrophoretic studies on the Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North-east Atlantic. International Journal for Parasitology 16, 633–640.CrossRefGoogle ScholarPubMed
Nichols, R. (2001). Gene trees and species trees are not the same. Trends in Ecology and Evolution 16, 358–364.CrossRefGoogle Scholar
Nicolalde-Morejón, F., Vergara-Silva, F., González-Astorga, J., Vovides, A. P. and Espinosa de los, Monteros A. (2009). Reciprocal illumination of morphological characters upon a molecular hypothesis supports the proposal of a new species of cycad from Mexico. Systematics and Biodiversity 7, 73–79. doi:10.1017/S1477200008002879.CrossRefGoogle Scholar
Nixon, K. C. and Wheeler, Q. D. (1990). An amplification of the phylogenetic species concept. Cladistics 6, 211–224.CrossRefGoogle Scholar
Nolan, M. J. and Cribb, T. H. (2005). The use and implications of ribosomal DNA sequencing for the discrimination of digenean species. Advances in Parasitology 60, 102–163. doi:10.1017/S1477200008002879.Google ScholarPubMed
Orecchia, P., Paggi, L., Mattiucci, S., Smith, J. W., Nascetti, G. and Bullini, L. (1986). Electrophoretic identification of larvae and adults of Anisakis (Ascaridida: Anisakidae). Journal of Helminthology 60, 331–339.CrossRefGoogle ScholarPubMed
Padial, J. S., Miralles, A., De la Riva, I. and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology 7, 16. doi: 10.1186/1742-9994-7-16.CrossRefGoogle ScholarPubMed
Page, R. D. M. (1993). Genes, organisms, and areas: the problem of multiple lineages. Systematic Biology 42, 77–84.CrossRefGoogle Scholar
Page, R. D. M. (1996). Temporal congruence revisited: comparison of mitochondrial DNA sequence divergence in cospeciating pocket gophers and their chewing lice. Systematic Biology 45, 151–167.CrossRefGoogle Scholar
Paggi, L. and Bullini, L. (1994). Molecular taxonomy in anisakids. Bulletin of the Scandinavian Society of Parasitology 4, 25–39.Google Scholar
Palm, H. W., Damriyasa, I. M. and Oka, I. B. M. (2008). Molecular genotyping of Anisakis Dujardin, 1845 (Nematoda: Ascaridoidea: Anisakidae) larvae from marine fish of Balinese and Javanese waters, Indonesia. Helminthologia 45, 3–12. doi: 10.2478/s11687-008-0001-8.CrossRefGoogle Scholar
Pérez-Ponce de León, G. and Choudhury, A. (2010). Parasite inventories and DNA-based taxonomy: lessons from helminths of freshwater fishes in a megadiverse country. Journal of Parasitology 96, 236–244. doi:10.1645/GE-2239.1.CrossRefGoogle Scholar
Pérez-Ponce de León, G. and Nadler, S. A. (2010). What we don't recognize can hurt us: A plea for awareness about cryptic species. Journal of Parasitology 96, 453–464. doi:10.1645/GE-2260.1.CrossRefGoogle Scholar
Porter, A. H. (1990). Testing nominal species boundaries using gene flow statistics: taxonomy of two hybridizing admiral butterflies (Limenitis: Nymphalidae). Systematic Zoology 39, 131–147.CrossRefGoogle Scholar
Poulin, R. (2010). Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters. doi:10.1098/rsbl.2010.0640.Google ScholarPubMed
Poulin, R. and Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology 75, 277–293.CrossRefGoogle ScholarPubMed
Poulin, R. and Morand, S. (2004). Parasite Biodiversity. Smithsonian Institution, Washington.Google Scholar
Pozio, E., La Rosa, G., Murrell, K. D. and Lichtenfels, J. R. (1992). Taxonomic revision of the genus Trichinella. Journal of Parasitology 78, 654–659.CrossRefGoogle ScholarPubMed
Rannala, B. H. (1990). Electrophoretic evidence concerning the relationship between Haplometrana and Glypthelmins (Digenea: Plagiorchiformes). Journal of Parasitology 76, 746–748.CrossRefGoogle Scholar
Razo-Mendivil, U., Vázquez-Domínguez, E., Rosas-Valdez, R., Pérez-Ponce de León, G. and Nadler, S. A. (2010). Phylogenetic analysis of nuclear and mitochondrial DNA reveals a complex of cryptic species in Crassicutis cichlasomae (Digenea), a parasite of middle-American cichlids. International Journal for Parasitology 40, 471–486. doi:10.1016/j.ijpara.2009.10.004.CrossRefGoogle ScholarPubMed
Romstad, A., Gasser, R. B., Nansen, P., Polderman, A. M. and Chilton, N. B. (1998). Necator americanus (Nematoda: Ancylostomatidae) from Africa and Malaysia have different ITS-2 rDNA. International Journal for Parasitology 28, 611–615.CrossRefGoogle ScholarPubMed
Sáez, A. G. and Lozano, E. (2005). Body doubles. Nature 433, 111.CrossRefGoogle ScholarPubMed
Saijuntha, W., Sithithaworn, P., Wongkham, S., Laha, T., Pipitgool, V., Tesana, V., Chilton, N. B., Petney, T. N. and Andrews, R. H. (2007). Evidence of a species complex within the food-borne trematode Opisthorchis viverrini and possible co-evolution with their first intermediate hosts. International Journal for Parasitology 37, 695–703. doi:10.1016/j.ijpara.2006.12.008.CrossRefGoogle ScholarPubMed
Schlick-Sateiner, B. C., Seifert, B., Stauffer, C., Christian, E., Crozier, R. H. and Steiner, F. M. (2007). Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology and Evolution 22, 391–392. doi:10.1016/j.tree.2007.05.004.CrossRefGoogle Scholar
Sehgal, R. N. M., Hull, A. C., Anderson, N. L., Valkiunas, G., Markovets, M. J., Kawamura, S. and Tell, L. A. (2006). Evidence for cryptic speciation of Leucocytozoon spp. (Haemosporidea, Leucocytozidae) in diurnal raptors. Journal of Parasitology 92, 375–379. doi:10.1645/GE-656R.1.CrossRefGoogle Scholar
Singh, B. (1997). Molecular methods for diagnoses and epidemiological studies of parasitic infections. International Journal for Parasitology 10, 1135–1145.CrossRefGoogle Scholar
Sites, J. W. Jr. and Marshall, J. C. (2003). Delimiting species: A Renaissance issue in systematic biology. Trends in Ecology and Evolution 18, 462–470. doi:10.1016/S0169-5347(03)00184-8.CrossRefGoogle Scholar
St-Onge, M., LaRue, B. and Charpentier, G. (2008). A molecular revision of the taxonomic status of mermithid parasites of black flies from Quebec (Canada). Journal of Invertebrate Pathology 98, 299–306. doi:10.1016/j.jip.2008.04.001.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Parham, J. E. and Nickol, B. B. (2006). Geographic analysis of host use, development, and habitat use of an acanthocephalan species, Leptorhynchoides thecatus. Journal of Parasitology 92, 464–472. doi:10.1645/GE-708R.1.CrossRefGoogle ScholarPubMed
Steinauer, M. L., Nickol, B. B. and Ortí, G. (2007). Cryptic speciation and patterns of phenotypic variation of variable acanthocephalan parasite. Molecular Ecology 16, 4097–4109. doi:10.1111/j.1365-294X.2007.03462.x.CrossRefGoogle ScholarPubMed
Stevenson, L. A., Gasser, R. B. and Chilton, N. B. (1996). The ITS-2 rDNA of Teladorsagia circumcincta, T. trifurcata and T. davtiani (Nematoda: Trichostrongylidae) indicates that these taxa are one species. International Journal for Parasitology 26, 1123–1126.CrossRefGoogle Scholar
Tautz, D., Arctander, P., Minelli, A., Thomas, R. H. and Volger, A. P. (2003). A plea for DNA taxonomy. Trends in Ecology and Evolution 18, 70–74. S0169-5347(02)00041-1.CrossRefGoogle Scholar
Tibayrenc, M. (1993). Entamoeba, Giardia, and Toxoplasma – Clones or cryptic species. Parasitology Today 9, 102–105.CrossRefGoogle ScholarPubMed
Tibayrenc, M. (1995). Population genetics of parasitic protozoa and other microorganisms. Advances in Parasitology 36, 47–115.CrossRefGoogle ScholarPubMed
Vieites, D. R., Walenberg, K. C., Andreone, F., Kölher, J., Glaw, F. and Vences, M. (2009). Vast underestimation of Madagascar biodiversity evidenced by an integrative amphibian inventory. Proceedings of The National Academy of Sciences, USA 106, 8267–8272. doi:10.1073pnas.0810821106.CrossRefGoogle ScholarPubMed
Vilas, R., Sanmartin, M. L. and Paniagua, E. (2004). Genetic variability of natural populations of trematodes of the genus Lecithochirium parasites of eels. Parasitology 129, 191–201. doi:10.1017/S0031182004005402.CrossRefGoogle ScholarPubMed
Vilas, R., Criscione, C. D. and Blouin, M. S. (2005). A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology 131, 1–8. doi:10.1017/S0031182005008437.CrossRefGoogle ScholarPubMed
Wheeler, Q. D. (1999). Why the phylogenetic species concept? Elementary. Journal of Nematology 31, 134–141.Google ScholarPubMed
Wheeler, Q. D. (2008). The New Taxonomy. CRC Press, Boca Raton, Florida.CrossRefGoogle Scholar
Wheeler, Q. D. and Meier, R. (2000) Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press: New York.Google Scholar
Wheeler, Q. D., Raven, P. H. and Wilson, E. O. (2004). Taxonomy: impediment or expedient? Science 303, 285. doi:10.1126/science.303.5656.285.CrossRefGoogle ScholarPubMed
Wiemers, M. and Fiedler, K. (2007). Does the DNA barcoding gap exist? – a case study in blue butterflies (Lepidoptera: Lycaenidae). Frontiers in Zoology 4, 8. doi:10.1186/1742-9994-4-8.CrossRefGoogle ScholarPubMed
Zarlenga, D. S., McManus, D. E., Fan, P. C. and Cross, J. H. (1991). Characterization and detection of a newly described Asian taeniid using cloned ribosomal DNA fragments and sequence amplification by polymerase chain reaction. Experimental Parasitology 72, 174–183.CrossRefGoogle ScholarPubMed
Zietara, M. S. and Lumme, J. (2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea: Gyrodactylidae). International Journal of Organismal Evolution 56, 2445–2458.Google Scholar
Zhu, X., Gasser, R. B., Chilton, N. B. and Jacobs, D. E. (2001). Molecular approaches for studying ascaridoid nematodes with zoonotic potential, with an emphasis on Toxocara species. Journal of Helminthology 75, 101–108. doi:10.1079/JOH200175.Google ScholarPubMed