Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-26T06:22:20.905Z Has data issue: false hasContentIssue false

An updated look at the uneven distribution of cryptic diversity among parasitic helminths

Published online by Cambridge University Press:  06 March 2017

G. Pérez-Ponce de León
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, Ciudad Universitaria, México D.F., México
R. Poulin*
Affiliation:
Department of Zoology, University of Otago, Dunedin, New Zealand

Abstract

Cryptic parasite diversity is a major issue for taxonomy and systematics, and for attempts to control diseases of humans, domestic animals and wildlife. Here, we re-examine an earlier report that, after correcting for sampling effort, more cryptic species of trematodes are found per published study than for other helminth taxa. We performed a meta-analysis of 110 studies that used DNA sequences to search for cryptic species in parasitic helminth taxa. After correcting for study effort and accounting for the biogeographical region of origins, we found that more cryptic species tend to be uncovered among trematodes, and fewer among cestodes and animal-parasitic nematodes, than in other helminth groups. However, this pattern was only apparent when we included only studies using nuclear markers in the analysis; it was not seen in a separate analysis based only on mitochondrial markers. We propose that the greater occurrence of cryptic diversity among trematodes may be due to some of their unique features, such as their mode of reproduction or frequent lack of hard morphological structures, or to the way in which trematode species are described. Whatever the reason, the high frequency of cryptic species among trematodes has huge implications for estimates of parasite diversity and for future taxonomic research.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2017 

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

Bickford, D., Lohman, D.J., Sodhi, N.S., Ng, P.K.L., Meier, R., Winker, K., Ingram, K.K. & Das, I. (2007) Cryptic species as a window on diversity and conservation. Trends in Ecology and Evolution 22, 148155.Google Scholar
Blasco-Costa, I., Cutmore, S.C., Miller, T.L. & Nolan, M.J. (2016) Molecular approaches to trematode systematics: ‘best practice’ and implications for future study. Systematic Parasitology 93, 295306.Google Scholar
Blouin, M.S. (2002) Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527531.Google Scholar
Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology 22, 43694383.Google Scholar
Detwiler, J.T., Zajac, A.M., Minchella, D.J. & Belden, L.K. (2012) Revealing cryptic parasite diversity in a definitive host: echinostomes in muskrats. Journal of Parasitology 98, 11481155.CrossRefGoogle Scholar
Flot, J.F. (2015) Species delimitation's coming of age. Systematic Biology 64, 897899.Google Scholar
Galtier, N., Nabholz, B., Glemin, S. & Hurst, G.D.D. (2009) Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Molecular Ecology 18, 45414550.CrossRefGoogle ScholarPubMed
Georgieva, S., Selbach, C., Faltýnková, A., Soldánová, M., Sures, B., Skírnisson, K. & Kostadinova, A. (2013) New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites & Vectors 6, 64.Google Scholar
Haverkost, T.R. & Gardner, S.L. (2008) A review of species in the genus Rhopalias (Rudolphi, 1819). Journal of Parasitology 94, 716726.CrossRefGoogle ScholarPubMed
Locke, S., McLaughlin, J.D. & 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, 28132827.Google Scholar
Nadler, S.A. & Pérez-Ponce de León, G. (2011) Integrating molecular and morphological approaches for characterizing parasite cryptic species: implications for parasitology. Parasitology 138, 16881709.Google Scholar
Pérez-Ponce de León, G. & Nadler, S.A. (2010) What we don't recognize can hurt us: a plea for awareness about cryptic species. Journal of Parasitology 96, 453464.Google Scholar
Pérez-Ponce de León, G. & Poulin, R. (2016) Taxonomic distribution of cryptic diversity among metazoans: not so homogeneous after all. Biology Letters 12, 20160371.Google Scholar
Pfenninger, M. & Schwenk, K. (2007) Cryptic animal species are homogeneously distributed among taxa and biogeographical regions. BMC Evolutionary Biology 7, 121.CrossRefGoogle ScholarPubMed
Poulin, R. (2007) Evolutionary ecology of parasites. 2nd edn. Princeton, Princeton University Press.Google Scholar
Poulin, R. (2011) Uneven distribution of cryptic diversity among higher taxa of parasitic worms. Biology Letters 7, 241244.CrossRefGoogle ScholarPubMed
Poulin, R. & Keeney, D.B. (2008) Host specificity under molecular and experimental scrutiny. Trends in Parasitology 24, 2428.Google Scholar
Poulin, R. & Pérez-Ponce de León, G. (2017) Global analysis reveals that cryptic diversity is linked with habitat but not mode of life. Journal of Evolutionary Biology, in press.CrossRefGoogle Scholar
Poulin, R. & Presswell, B. (2016) Taxonomic quality of species descriptions varies over time and with the number of authors, but unevenly among parasitic taxa. Systematic Biology 65, 11071116.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 18641877.Google Scholar
Razo-Mendivil, U., Rosas-Valdez, R., Rubio-Godoy, M. & Pérez-Ponce de León, G. (2015) The use of mitochondrial and nuclear sequences in prospecting for cryptic species in Tabascotrema verai (Digenea: Cryptogonimidae), a parasite of Petenia splendida (Cichlidae) in Middle America. Parasitology International 64, 173181.Google Scholar
Rosas-Valdez, R., Choudhury, A. & Pérez-Ponce de León, G. (2011) Molecular prospecting for cryptic species in Phyllodistomum lacustri (Platyhelminthes, Gorgoderidae). Zoologica Scripta 40, 296305.Google Scholar
Vignon, M. & Sasal, P. (2010) The use of geometric morphometrics in understanding shape variability of sclerotized haptoral structures of monogeneans (Platyhelminthes) with insights into biogeographic variability. Parasitology International 59, 183191.Google Scholar
Vilas, R., Criscione, C.D. & 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, 839846.Google Scholar
Walther, B.A., Cotgreave, P., Price, R.D., Gregory, R.D. & Clayton, D.H. (1995) Sampling effort and parasite species richness. Parasitology Today 11, 306310.Google Scholar
Wayland, M.T. (2010) Proboscis profiler: a tool for detecting acanthocephalan morphotypes. Systematic Parasitology 76, 159167.Google Scholar
Yin, M., Hu, W., Mo, X., Wang, S., Brindley, P.J., McManus, D.P., Davis, G.M., Feng, Z. & Blair, D. (2008) Multiple near-identical genotypes of Schistosoma japonicum can occur in snails and have implications for population-genetic analyses. International Journal for Parasitology 38, 16811691.Google Scholar
Supplementary material: File

Pérez-Ponce de León and Poulin supplementary material

Pérez-Ponce de León and Poulin supplementary material 1

Download Pérez-Ponce de León and Poulin supplementary material(File)
File 43.2 KB