Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T07:57:20.120Z Has data issue: false hasContentIssue false
  • English
  • Français

Evolutionary diversity in polystomatids infecting tetraploid and octoploid Xenopus in East African highlands: biological and molecular evidence

Published online by Cambridge University Press:  12 April 2007

J. A. JACKSON  and
R. C. TINSLEY
J. A. JACKSON*
Affiliation:
School of Biology, University of Nottingham, Nottingham NG7 2RD, UK
R. C. TINSLEY
Affiliation:
School of Biological Sciences, University of Bristol, Bristol BS8 1UG, UK
*
*Corresponding author: School of Biology, University of Nottingham, Nottingham NG7 2RD, UK. Tel: +44 115 9513188. Fax: +44 115 9513188. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Species of Protopolystoma are monogenean flukes that only infect allopolyploid hosts in the anuran genus Xenopus. Multivariate analyses of morphometric sclerite characters in the nominal species Protopolystoma simplicis suggest that morphologically distinguishable populations occur in the tetraploid host, Xenopus laevis victorianus, and in each of the octoploid hosts, X. vestitus and X. wittei. The species-level divergence of a lineage specific to X. laevis is supported by sequence variation in the mitochondrial cytochrome c oxidase subunit 1 (cox1) gene. Protopolystoma simplicis from X. laevis is redesignated P. microsclera n. sp., with P. simplicis being retained for populations in octoploid hosts. This division is consistent with large differences in egg hatching schedule, fixed differences at the mannose-6-phosphate isomerase and fumarate hydratase loci, and host-specificity in experimental analyses. Although the respective P. simplicis populations in X. vestitus and X. wittei also show significant diversity in allozyme expression, morphometrics and egg hatching schedule, they are retained in the same species because their level of mitochondrial DNA divergence is similar to that found within other Protopolystoma species. The consequences of splitting P. simplicis for a recent interpretation of the origin of Protopolystoma faunas in octoploid Xenopus spp. is discussed.

Keywords

allopolyploidyhost-specificityresistancesusceptibilityvertebratemonogeneanProtopolystomamitochondrial DNAallozymemorphometrics
Type
Research Article
Information
Parasitology , Volume 134 , Issue 9 , August 2007 , pp. 1223 - 1235
Copyright
Copyright © Cambridge University Press 2007

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

Combes, C. (2001). Parasitism: The Ecology and Evolution of Intimate Interactions. The University of Chicago Press, Chicago.Google Scholar
Evans, B. J., Kelley, D. B., Melnick, D. J. and Cannatella, D. C. (2005). Evolution of RAG-1 in polyploid clawed frogs. Molecular Biology and Evolution 22, 1193–1207.CrossRefGoogle ScholarPubMed
Evans, B. J., Kelley, D. B., Tinsley, R. C., Melnick, D. J. and Cannatella, D. C. (2004). A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. Molecular Phylogenetics and Evolution 33, 197–213.CrossRefGoogle ScholarPubMed
Hebert, P. D. N. and Beaton, M. J. (1993). Methodologies for Allozyme Analysis using Cellulose Acetate Electrophoresis: A Practical Handbook. Helena Laboratories, Beaumont, Texas.Google Scholar
Hebert, P. D. N., Cywinska, A., Ball, S. L. and DeWaard, J. R. (2003 a). Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, B 270, 313–321.Google Scholar
Hebert, P. D. N., Ratnasingham, S. and DeWaard, J. R. (2003 b). Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, B 270, S96–S99.CrossRefGoogle ScholarPubMed
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle ScholarPubMed
Jackson, J. A., Pleass, R. J., Cable, J., Bradley, J. E. and Tinsley, R. C. (2006). Heterogenous interspecific interactions in a host-parasite system. International Journal for Parasitology 36, 1341–1349.Google Scholar
Jackson, J. A. and Tinsley, R. C. (1995). Sclerite growth and morphometric variation in Gyrdicotylus gallieni Vercammen-Grandjean, 1960 (Monogenea, Gyrodactylidae) from Xenopus laevis laevis (Anura). Systematic Parasitology 31, 1–9.CrossRefGoogle Scholar
Jackson, J. A. and Tinsley, R. C. (2001). Protopolystoma xenopodis (Monogenea) primary and secondary infections in Xenopus laevis. Parasitology 123, 455–463.CrossRefGoogle ScholarPubMed
Jackson, J. A. and Tinsley, R. C. (2002). Effects of environmental temperature on the susceptibility of Xenopus laevis and X. wittei (Anura) to Protopolystoma xenopodis (Monogenea). Parasitology Research 88, 632–638.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2003). Parasite infectivity to hybridising host species: a link between hybrid resistance and allopolyploid speciation? International Journal for Parasitology 33, 137–144.CrossRefGoogle ScholarPubMed
Jackson, J. A. and Tinsley, R. C. (2005). Geographic and within-population structure in variable resistance to parasite species and strains in a vertebrate host. International Journal for Parasitology 35, 29–37.CrossRefGoogle Scholar
Jackson, J. A., Tinsley, R. C. and Du Preez, L. H. (2001). Differentiation of two locally sympatric Protopolystoma (Monogenea: Polystomatidae) species by temperature-dependent larval development and survival. International Journal for Parasitology 31, 815–821.Google Scholar
Jackson, J. A., Tinsley, R. C. and Kigoolo, S. (1998). Polyploidy and parasitic infection in Xenopus species from western Uganda. Herpetological Journal 8, 19–22.Google Scholar
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
Posada, D. and Crandall, K. A. (1998). MODELTEST: testing the model of DNA substitution. Bioinformatics 14, 817–818.CrossRefGoogle ScholarPubMed
Richardson, B. J., Baverstock, P. R. and Adams, M. (1986). Allozyme Electrophoresis. Academic Press, Sydney, Australia.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis using Parsimony (*and other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle ScholarPubMed
Tinsley, R. C. and Jackson, J. A. (1998 a). Correlation of parasite speciation and specificity with host evolutionary relationships. International Journal for Parasitology 28, 1573–1582.Google Scholar
Tinsley, R. C. and Jackson, J. A. (1998 b). Speciation of Protopolystoma Bychowsky, 1957 (Monogenea: Polystomatidae) in hosts of the genus Xenopus (Anura: Pipidae). Systematic Parasitology 40, 93–141.Google Scholar
Tymowska, J. (1991). Polyploidy and cytogenetic variation in frogs of the genus Xenopus. In Amphibian Cytogenetics and Evolution (ed. Green, D. M. and Sessions, S. K.), pp. 259–297. Academic Press, London.CrossRefGoogle Scholar
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, 839–846.CrossRefGoogle ScholarPubMed