Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T12:02:50.603Z Has data issue: false hasContentIssue false
  • English
  • Français

Detecting hybridization in African schistosome species: does egg morphology complement molecular species identification?

Published online by Cambridge University Press:  20 February 2017

NELE A. M. BOON ,
WOUTER FANNES ,
SARA ROMBOUTS ,
KATJA POLMAN ,
FILIP A. M. VOLCKAERT  and
TINE HUYSE
NELE A. M. BOON*
Affiliation:
Laboratory of Biodiversity and Evolutionary Genomics, Biology, University of Leuven, Ch. Deberiotstraat 32, B-3000 Leuven, Belgium Unit of Medical Helminthology, Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp, Belgium
WOUTER FANNES
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
SARA ROMBOUTS
Affiliation:
Laboratory of Biodiversity and Evolutionary Genomics, Biology, University of Leuven, Ch. Deberiotstraat 32, B-3000 Leuven, Belgium
KATJA POLMAN
Affiliation:
Unit of Medical Helminthology, Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerp, Belgium
FILIP A. M. VOLCKAERT
Affiliation:
Laboratory of Biodiversity and Evolutionary Genomics, Biology, University of Leuven, Ch. Deberiotstraat 32, B-3000 Leuven, Belgium
TINE HUYSE
Affiliation:
Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium
*
*Corresponding author: Laboratory of Biodiversity and Evolutionary Genomics, Biology, University of Leuven, Ch. Deberiotstraat 32, B-3000 Leuven, Belgium. E-mail: Nele.boon@kuleuven.be
Get access Rights & Permissions [Opens in a new window]

Summary

Hybrid parasites may have an increased transmission potential and higher virulence compared to their parental species. Consequently, hybrid detection is critical for disease control. Previous crossing experiments showed that hybrid schistosome eggs have distinct morphotypes. We therefore compared the performance of egg morphology with molecular markers with regard to detecting hybridization in schistosomes. We studied the morphology of 303 terminal-spined eggs, originating from 19 individuals inhabiting a hybrid zone with natural crosses between the human parasite Schistosoma haematobium and the livestock parasite Schistosoma bovis in Senegal. The egg sizes showed a high variability and ranged between 92·4 and 176·4 µm in length and between 35·7 and 93·0 µm in width. No distinct morphotypes were found and all eggs resembled, to varying extent, the typical S. haematobium egg type. However, molecular analyses on the same eggs clearly showed the presence of two distinct partial mitochondrial cox1 profiles, namely S. bovis and S. haematobium, and only a single nuclear ITS rDNA profile (S. haematobium). Therefore, in these particular crosses, egg morphology appears not a good indicator of hybrid ancestry. We conclude by discussing strengths and limitations of molecular methods to detect hybrids in the context of high-throughput screening of field samples.

Keywords

hybridizationSchistosoma haematobiumSchistosoma bovisegg morphometricsbarcodingzoonosisSenegal
Type
Research Article
Information
Parasitology , Volume 144 , Issue 7 , June 2017 , pp. 954 - 964
Check for updates
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

REFERENCES

Almeda, J., Ascaso, C., Marçal, G. A., Corachan, M., Southgate, V. R. and Rollinson, D. (1996). Morphometric variability of Schistosoma intercalatum eggs: a diagnostic dilemma. Journal of Helminthology 70, 97–102.Google Scholar
Alves, W. (1949). The eggs of Schistosoma bovis, S. mattheei and S. haematobium . Journal of Helminthology 23, 127.Google Scholar
Barber, K. E., Mkoji, G. M. and Loker, E. S. (2000). PCR-RFLP analysis of the ITS2 region to identify Schistosoma haematobium and S. bovis from Kenya. American Journal of Tropical Medicine and Hygiene 62, 434–440.Google Scholar
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Boissier, J., Moné, H., Mitta, G., Bargues, M. D., Molyneux, D. and Mas-Coma, S. (2015). Schistosomiasis reaches Europe. The Lancet Infectious Diseases 15, 757–758.Google Scholar
Bowles, J., Blair, D. and McManus, D. P. (1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.Google Scholar
Brémond, P., Sellin, B., Sellin, E., Nameoua, B., Labbo, R., Theron, A. and Combes, C. (1993). Arguments for the modification of the genome (introgression) of the human parasite Schistosoma haematobium by genes from S. bovis, in Niger. Comptes-Rendus de l'Académie des Sciences.Série III: Sciences de la Vie 316, 667–670.Google Scholar
Brindley, P. J. and Hotez, P. J. (2013). Break out: urogenital schistosomiasis and Schistosoma haematobium infection in the post-genomic era. PLoS Neglected Tropical Diseases 7, 2–4.Google Scholar
De Clercq, D., Rollinson, D., Diarra, A., Sacko, M., Coulibaly, G., Landouré, A., Traoré, M., Southgate, V. R., Kaukas, A. and Vercruysse, J. (1994). Schistosomiasis in Dogon country, Mali: identification and prevalence of the species responsible for infection in the local community. Transactions of the Royal Society of Tropical Medicine and Hygiene 88, 653–656.Google Scholar
Fuertes Aguilar, J., Rosselló, J. A. and Nieto Feliner, G. (1999). Nuclear ribosomal DNA (nrDNA) concerted evolution in natural and artificial hybrids of Armeria (Plumbaginaceae). Molecular Ecology 8, 1341–1346.Google Scholar
Garcia, M. G., Silva, R. S., Carniello, M. A., Veldman, J. W., Rossi, A. A. B. and de Oliveira, L. O. (2011). Molecular evidence of cryptic speciation, historical range expansion, and recent intraspecific hybridization in the Neotropical seasonal forest tree Cedrela fissilis (Meliaceae). Molecular Phylogenetics and Evolution 61, 639–649.Google Scholar
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. The Lancet 368, 1106–1118.Google Scholar
Husting, E. L. (1965). Comments on “the routes of schistosome egg passage…”. The Central African Journal of Medicine 11, 250–254.Google Scholar
Huyse, T., Webster, B. L., Geldof, S., Stothard, J. R., Diaw, O. T., Polman, K. and Rollinson, D. (2009). Bidirectional introgressive hybridization between a cattle and human schistosome species. PLoS Pathogens 5, e1000571.Google Scholar
Huyse, T., Van den Broeck, F., Hellemans, B., Volckaert, F. A. M. and Polman, K. (2013). Hybridisation between the two major African schistosome species of humans. International Journal for Parasitology 43, 687–689.Google Scholar
Katz, N., Chaves, A. and Pellegrino, J. (1972). A simple device for quantitative stool thick-smear tecnique in Schistosoma mansoni . Revista do Instituto de Medicina Tropical de São Paulo 14, 397–400.Google Scholar
Khalil, M. (1924). On the morphology of Schistosoma bovis . Journal of Helminthology 2, 81.Google Scholar
King, K. C., Stelkens, R. B., Webster, J. P., Smith, D. F. and Brockhurst, M. A. (2015). Hybridization in parasites: consequences for adaptive evolution, pathogenesis, and public health in a changing world. PLoS Pathogens 11, e1005098.Google Scholar
Leger, E. and Webster, J. P. (2016). Hybridizations within the genus Schistosoma: implications for evolution, epidemiology and control. Parasitology 144, 1–16. doi:10.1017/S0031182016001190.Google Scholar
Loker, E. S. (1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87(Pt 2), 343–369.CrossRefGoogle ScholarPubMed
MacHattie, C., Mills, E. A. and Chadwick, M. C. R. (1933). Can sheep and cattle act as reservoirs of human schistosomiasis? Transactions of the Royal Society of Tropical Medicine and Hygiene 27, 173–184.Google Scholar
Meurs, L., Mbow, M., Vereecken, K., Menten, J., Mboup, S. and Polman, K. (2012). Epidemiology of mixed Schistosoma mansoni and Schistosoma haematobium infections in northern Senegal. International Journal for Parasitology 42, 305–311.Google Scholar
Meurs, L., Brienen, E., Mbow, M., Ochola, E. A., Mboup, S., Karanja, D. M. S., Secor, W. E., Polman, K. and van Lieshout, L. (2015). Is PCR the next reference standard for the diagnosis of Schistosoma in stool? A comparison with microscopy in Senegal and Kenya. PLOS Neglected Tropical Diseases 9, e0003959.Google Scholar
Moné, H., Holtfreter, M. C., Allienne, J.-F., Mintsa-Nguéma, R., Ibikounlé, M., Boissier, J., Berry, A., Mitta, G., Richter, J. and Mouahid, G. (2015). Introgressive hybridizations of Schistosoma haematobium by Schistosoma bovis at the origin of the first case report of schistosomiasis in Corsica (France, Europe). Parasitology Research 114, 4127–4133.Google Scholar
Pitchford, R. J. (1959). Cattle schistosomiasis in man in the eastern Transvaal. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 286–290.Google Scholar
Pitchford, R. J. (1965). Differences in the egg morphology and certain biological characteristics of some African and Middle Eastern Schistosomes, genus Schistosoma, with terminal-spined eggs. Bulletin of the World Health Organization 32, 105–120.Google Scholar
Pitchford, R. J. and Visser, P. S. (1975). A simple and rapid technique for quantitative estimation of helminth eggs in human and animal excreta with special reference to Schistosoma sp. Transactions of the Royal Society of Tropical Medicine and Hygiene 69, 318–322.Google Scholar
R Development Core Team (2015). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ratard, R. C., Ndamkou, C. N., Kouemeni, L. E. and Ekani Bessala, M. M. (1991). Schistosoma mansoni eggs in urine. Journal of Tropical Medicine and Hygiene 94, 348–351.Google Scholar
Rollinson, D., Southgate, V. R., Vercruysse, J. and Moore, P. J. (1990). Observations on natural and experimental interactions between Schistosoma bovis and S. curassoni from West Africa. Acta Tropica 47, 101–114.Google Scholar
Sang, T., Crawford, D. J. and Stuessy, T. F. (1995). Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. Proceedings of the National Academy of Sciences of the United States of America 92, 6813–6817.Google Scholar
Smyth, J. D. and Clegg, J. A. (1959). Egg-shell formation in trematodes and cestodes. Experimental Parasitology 8, 286–323.Google Scholar
Soentjens, P., Cnops, L., Huyse, T., Yansouni, C., De Vos, D., Bottieau, E., Clerinx, J. and Van Esbroeck, M. (2016). Diagnosis and clinical management of Schistosoma haematobium – Schistosoma bovis hybrid infection in a cluster of travelers returning from Mali. Clinical Infectious Diseases 63, doi:10.1093/cid/ciw493.Google Scholar
Southgate, V. R., Rollinson, D., Ross, G. C., Knowles, R. J. and Vercruysse, J. (1985). On Schistosoma curassoni, S. haematobium and S. bovis from Senegal: development in Mesocricetus auratus, compatibility with species of Bulinus and their enzymes. Journal of Natural History 19, 1249–1267.Google Scholar
Southgate, V. R., Jourdane, J. and Tchuem Tchuenté, L. (1998). Recent studies on the reproductive biology of the schistosomes and their relevance to speciation in the Digenea. International Journal for Parasitology 28, 1159–1172.Google Scholar
Steinauer, M. L., Hanelt, B., Mwangi, I. N., Maina, G. M., Agola, L. E., Kinuthia, J. M., Mutuku, M. W., Mungai, B. N., Wilson, W. D., Mkoji, G. M. and Loker, E. S. (2008). Introgressive hybridization of human and rodent schistosome parasites in western Kenya. Molecular Ecology 17, 5062–5074.Google Scholar
Taylor, M. G. (1970). Hybridisation experiments on five species of African schistosomes. Journal of Helminthology 44, 253–314.Google Scholar
Touassem, R. (1987). Egg polymorphism of Schistosoma bovis . Veterinary Parasitology 23, 185–191.CrossRefGoogle ScholarPubMed
Twyford, A. D. and Ennos, R. A. (2012). Next-generation hybridization and introgression. Heredity 108, 179–189.Google Scholar
Van den Broeck, F., Geldof, S., Polman, K., Volckaert, F. A. M. and Huyse, T. (2011). Optimal sample storage and extraction procotols for reliable multilocus genotyping of the human parasite Schistosoma mansoni . Infection, Genetics and Evolution 11, 1413–1418.Google Scholar
Vercruysse, J., Southgate, V. R. and Rollinson, D. (1984). Schistosoma curassoni Brumpt, 1931 in sheep and goats in Senegal. Journal of Natural History 18, 969–976.CrossRefGoogle Scholar
Webster, B. L. and Southgate, V. R. (2003). Mating interactions of Schistosoma haematobium and S. intercalatum with their hybrid offspring. Parasitology 126, 327–338.Google Scholar
Webster, B. L., Southgate, V. R. and Littlewood, D. T. J. (2006). A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis . International Journal for Parasitology 36, 947–955.Google Scholar
Webster, B. L., Tchuem Tchuenté, L. A. and Southgate, V. R. (2007). A single-strand conformation polymorphism (SSCP) approach for investigating genetic interactions of Schistosoma haematobium and Schistosoma guineensis in Loum, Cameroon. Parasitology Research 100, 739–745.Google Scholar
Webster, B. L., Rollinson, D., Stothard, J. R. and Huyse, T. (2010). Rapid diagnostic multiplex PCR (RD-PCR) to discriminate Schistosoma haematobium and S. bovis . Journal of Helminthology 84, 107–114.Google Scholar
Webster, B. L., Diaw, O. T., Seye, M. M., Webster, J. P. and Rollinson, D. (2013). Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Neglected Tropical Diseases 7, e2110.Google Scholar
Weerakoon, K. G. A. D., Gobert, G. N., Cai, P. and McManus, D. P. (2015). Advances in the diagnosis of human schistosomiasis. Clinical Microbiology Reviews 28, 939–967.Google Scholar
Supplementary material: File

Boon supplementary material

Table S1

Download Boon supplementary material(File)
File 16.2 KB