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

  • NELE A. M. BOON (a1) (a2), WOUTER FANNES (a3), SARA ROMBOUTS (a1), KATJA POLMAN (a2), FILIP A. M. VOLCKAERT (a1) and TINE HUYSE (a3)...

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.

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Corresponding author

*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

References

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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, 97102.
Alves, W. (1949). The eggs of Schistosoma bovis, S. mattheei and S. haematobium . Journal of Helminthology 23, 127.
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, 434440.
Bates, D., Mächler, M., Bolker, B. and Walker, S. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 148.
Boissier, J., Moné, H., Mitta, G., Bargues, M. D., Molyneux, D. and Mas-Coma, S. (2015). Schistosomiasis reaches Europe. The Lancet Infectious Diseases 15, 757758.
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, 165173.
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, 667670.
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, 24.
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, 653656.
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, 13411346.
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, 639649.
Gryseels, B., Polman, K., Clerinx, J. and Kestens, L. (2006). Human schistosomiasis. The Lancet 368, 11061118.
Husting, E. L. (1965). Comments on “the routes of schistosome egg passage…”. The Central African Journal of Medicine 11, 250254.
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.
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, 687689.
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, 397400.
Khalil, M. (1924). On the morphology of Schistosoma bovis . Journal of Helminthology 2, 81.
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.
Leger, E. and Webster, J. P. (2016). Hybridizations within the genus Schistosoma: implications for evolution, epidemiology and control. Parasitology 144, 116. doi:10.1017/S0031182016001190.
Loker, E. S. (1983). A comparative study of the life-histories of mammalian schistosomes. Parasitology 87(Pt 2), 343369.
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, 173184.
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, 305311.
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.
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, 41274133.
Pitchford, R. J. (1959). Cattle schistosomiasis in man in the eastern Transvaal. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 286290.
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, 105120.
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, 318322.
R Development Core Team (2015). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
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, 348351.
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, 101114.
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, 68136817.
Smyth, J. D. and Clegg, J. A. (1959). Egg-shell formation in trematodes and cestodes. Experimental Parasitology 8, 286323.
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 haematobiumSchistosoma bovis hybrid infection in a cluster of travelers returning from Mali. Clinical Infectious Diseases 63, doi:10.1093/cid/ciw493.
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, 12491267.
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, 11591172.
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, 50625074.
Taylor, M. G. (1970). Hybridisation experiments on five species of African schistosomes. Journal of Helminthology 44, 253314.
Touassem, R. (1987). Egg polymorphism of Schistosoma bovis . Veterinary Parasitology 23, 185191.
Twyford, A. D. and Ennos, R. A. (2012). Next-generation hybridization and introgression. Heredity 108, 179189.
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, 14131418.
Vercruysse, J., Southgate, V. R. and Rollinson, D. (1984). Schistosoma curassoni Brumpt, 1931 in sheep and goats in Senegal. Journal of Natural History 18, 969976.
Webster, B. L. and Southgate, V. R. (2003). Mating interactions of Schistosoma haematobium and S. intercalatum with their hybrid offspring. Parasitology 126, 327338.
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, 947955.
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, 739745.
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, 107114.
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.
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, 939967.

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