Skip to main content Accessibility help
×
Home

Barcoding hybrids: heterogeneous distribution of Schistosoma haematobium × Schistosoma bovis hybrids across the Senegal River Basin

  • NELE A. M. BOON (a1) (a2), FREDERIK VAN DEN BROECK (a3), DJIBY FAYE (a4), FILIP A. M. VOLCKAERT (a1), SOULEYMANE MBOUP (a5), KATJA POLMAN (a2) and TINE HUYSE (a6)...

Abstract

Hybridization events between Schistosoma species (Digenea, Platyhelminthes) are reported with increasing frequency, largely due to improved access to molecular tools. Nevertheless, little is known about the distribution and frequency of hybrid schistosomes in nature. Screening for hybrids on a large scale is complicated by the need for nuclear and mitochondrial sequence information, precluding a ‘simple’ barcoding approach. Here we aimed to determine and understand the spatiotemporal distribution of Schistosoma haematobium × Schistosoma bovis hybrids in the Senegal River Basin. From ten villages, distributed over the four main water basins, we genotyped a total of 1236 schistosome larvae collected from human urine samples using a partial mitochondrial cox1 fragment; a subset of 268 parasites was also genotyped using ITS rDNA. Hybrid schistosomes were unevenly distributed, with substantially higher numbers in villages bordering Lac de Guiers than in villages from the Lampsar River and the Middle Valley of the Senegal River. The frequency of hybrids per village was not linked with the prevalence of urinary schistosomiasis in that village. However, we did find a significant positive association between the frequency of hybrids per village and the prevalence of Schistosoma mansoni. We discuss the potential consequences of adopting a barcoding approach when studying hybrids in nature.

Copyright

Corresponding author

*Corresponding author: Tine Huyse, Department of Biology, Royal Museum for Central Africa, Leuvensesteenweg 13, B-3080 Tervuren, Belgium. E-mail: Tine.Huyse@africamuseum.be

References

Hide All
Abdellahi, M., Ndir, O. and Niang, S. (2016). Évaluation de la prévalence des bilharzioses auprès des enfants de 5 à 14 ans après plusieurs années de traitement de masse dans le bassin du fleuve Sénégal. Santé Publique 28, 535540.
Alizon, S., de Roode, J. C. and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology letters 16, 556567.
Anderson, T. M., Bridgett, M., Candille, S. I., Musiani, M., Stahler, D. R., Smith, D. W., Padhukasahasram, B., Randi, E., Leonard, J. A., Bustamante, C. D., Ostrander, E. A., Tang, H., Robert, K. and Barsh, G. S. (2009). Molecular and evolutionary history of melanism in north American gray wolves. Science 323, 13391343.
Ballard, J. W. O. and Melvin, R. G. (2010). Linking the mitochondrial genotype to the organismal phenotype: invited review. Molecular Ecology 19, 15231539.
Ballard, J. W. O. and Whitlock, M. C. (2004). The incomplete natural history of mitochondria. Molecular Ecology 13, 729744.
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.
Boissier, J., Grech-Angelini, S., Webster, B. L., Allienne, J.-F., Huyse, T., Mas-Coma, S., Toulza, E., Barré-Cardi, H., Rollinson, D., Kincaid-Smith, J., Oleaga, A., Galinier, R., Foata, J., Rognon, A., Berry, A., Mouahid, G., Henneron, R., Moné, H., Noel, H. and Mitta, G. (2016). Outbreak of urogenital schistosomiasis in Corsica (France): an epidemiological case study. The Lancet Infectious Diseases 3099, 19.
Boon, N. A. M., Fannes, W., Rombouts, S., Polman, K., Volckaert, F. A. M. and Huyse, T. (2017). Detecting hybridization in African schistosome species: does egg morphology complement molecular species identification? Parasitology 144, 954964.
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.
Brant, S. V. and Loker, E. S. (2013). Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends in Parasitology 29, 449459.
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.
Currat, M., Ruedi, M., Petit, R. J. and Excoffier, L. (2008). The hidden side of invasions: massive introgression by local genes. Evolution 62, 19081920.
Detwiler, J. T. and Criscione, C. D. (2010). An infectious topic in reticulate evolution: introgression and hybridization in animal parasites. Genes 1, 102123.
Diaw, O., Vassiliades, G., Thiongane, Y., Seye, M., Sanrr, Y. and Diouf, A. (1998). Extension des trématodoses du bétail après la construction des barrages dans le bassin du fleuve Sénégal. Revue d'élevage et de médecinevétérinaire des pays tropicaux 51, 113120.
Dinno, A. (2016). Dunn's test of multiple comparisons using rank sums.
Dray, S. and Dufour, A. B. (2007). The ade4 package: implementing the duality diagram for ecologists. Journal of Statistical Software 22, 120.
Dunn, O. J. (1964). Multiple comparisons using rank sums. Technometrics 6, 241252.
Emery, A. M., Allan, F. E., Rabone, M. E. and Rollinson, D. (2012). Schistosomiasis collection at NHM (SCAN). Parasites & Vectors 5, 185.
Gagneux, S., DeRiemer, K., Van, T., Kato-Maeda, M., de Jong, B. C., Narayanan, S., Nicol, M., Niemann, S., Kremer, K., Gutierrez, M. C., Hilty, M., Hopewell, P. C. and Small, P. M. (2006). Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proceedings of the National Academy of Sciences 103, 28692873.
Good, J. M., Vanderpool, D., Keeble, S. and Bi, K. (2015). Negligible nuclear introgression despite complete mitochondrial capture between two species of chipmunks. Evolution 69, 19611972.
Harrison, R. G. and Larson, E. L. (2014). Hybridization, introgression, and the nature of species boundaries. Journal of Heredity 105, 795809.
Hedrick, P. W. (2013). Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology 22, 46064618.
Hill, G. E. (2015). Mitonuclear ecology. Molecular Biology and Evolution 32, 19171927.
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.
Irwin, D. E. (2002). Phylogeographic breaks without geographic barriers to gene flow. Evolution 56, 23832394.
Kane, R. A., Stothard, J. R., Emery, A. M. and Rollinson, D. (2008). Molecular characterization of freshwater snails in the genus Bulinus: a role for barcodes? Parasites & Vectors 1, 15.
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.
Kazancioǧlu, E. and Arnqvist, G. (2014). The maintenance of mitochondrial genetic variation by negative frequency-dependent selection. Ecology Letters 17, 2227.
Kruskal, W. H. and Wallis, W. A. (1952). Use of ranks in one-criterion variance analysis. Journal of the American Statistical Association 47, 583621.
Leger, E. and Webster, J. P. (2016). Hybridizations within the genus Schistosoma: implications for evolution, epidemiology and control. Parasitology 144, 116.
Loker, E. S. and Brant, S. V. (2006). Diversification, dioecy and dimorphism in schistosomes. Trends in Parasitology 22, 521528.
McSorley, H. J. and Maizels, R. M. (2012). Helminth infections and host immune regulation. Clinical Microbiology Reviews 25, 585608.
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.
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.
Morgan, J. A T., Dejong, R. J., Adeoye, G. O., Ansa, E. D. O., Barbosa, C. S., Brémond, P., Cesari, I. M., Charbonnel, N., Corrêa, L. R., Coulibaly, G., D'Andrea, P. S., De Souza, C. P., Doenhoff, M. J., File, S., Idris, M. A., Incani, R. N., Jarne, P., Karanja, D. M. S., Kazibwe, F., Kpikpi, J., Lwambo, N. J. S., Mabaye, A., Magalhães, L. A., Makundi, A., Moné, H., Mouahid, G., Muchemi, G. M., Mungai, B. N., Séne, M., Southgate, V. et al. (2005). Origin and diversification of the human parasite Schistosoma mansoni. Molecular Ecology 14, 38893902.
Norton, A. J., Webster, J. P., Kane, R. A. and Rollinson, D. (2008). Inter-specific parasite competition: mixed infections of Schistosoma mansoni and S. rodhaini in the definitive host. Parasitology 135, 473484.
Picquet, M., Ernould, J. C., Vercruysse, J., Southgate, V. R., Mbaye, A., Sambou, B., Niang, M. and Rollinson, D. (1996). The epidemiology of human schistosomiasis in the Senegal river basin. Transactions of the Royal Society of Tropical Medicine and Hygiene 90, 340346.
R Development Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing Vienna Austria. doi: 10.1038/sj.hdy.6800737.
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.
Sène, M., Southgate, V. R. and Vercruysse, J. (2004). Bulinus truncatus, intermediate host of Schistosoma haematobium in the Senegal river basin. Bulletin de la Societe de Pathologie Exotique 97, 2932.
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, 16261629.
Southgate, V., de Clercq, D., Séne, M., Rollinson, D., LY, A. and Vercruysse, J. (2000). Observations on compatibility between Bulinus truncatus and Schistosoma haematobium in the Senegal river basin. Annals of Tropical Medicine And Parasitology 91, 371378.
Southgate, V., Tchuem Tchuenté, L., Sène, M., De Clercq, D., Théron, A., Jourdane, J., Webster, B. L., Rollinson, D., Gryseels, B. and Vercruysse, J. (2001). Studies on the biology of schistosomiasis with emphasis on the Senegal river basin. Memórias do Instituto Oswaldo Cruz 96 (Suppl.), 7578.
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.
Tchuem Tchuenté, L. A., Southgate, V. R., Combes, C. and Jourdane, J. (1996). Mating behaviour in schistosomes: are paired worms always faithful? Parasitology Today 12, 231236.
Theron, A., Rognon, A., Gourbal, B. and Mitta, G. (2014). Multi-parasite host susceptibility and multi-host parasite infectivity: a new approach of the Biomphalaria glabrata/Schistosoma mansoni compatibility polymorphism. Infection, Genetics and Evolution 26, 8088.
Toews, D. P. L. and Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 39073930.
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). Compatibility of Schistosoma haematobium, S. intercalatum and their hybrids with Bulinus truncatus and B. forskalii. Parasitology 127, 231242.
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., 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., Emery, A. M., Webster, J. P., Gouvras, A., Garba, A., Diaw, O., Seye, M. M., Tchuente, L. A. T., Simoonga, C., Mwanga, J., Lange, C., Kariuki, C., Mohammed, K. A., Stothard, J. R. and Rollinson, D. (2012). Genetic diversity within Schistosoma haematobium: DNA barcoding reveals Two distinct groups. PLoS Neglected Tropical Diseases 6, e1882.
Webster, B. L., Webster, J. P., Gouvras, A. N., Garba, A., Lamine, M. S., Diaw, O. T., Seye, M. M., Tchuem Tchuenté, L. A., Simoonga, C., Mubila, L., Mwanga, J. R., Lwambo, N. J. S., Kabatereine, N. B., Lange, C. N., Kariuki, C., Mkoji, G. M., Rollinson, D. and Stothard, J. R. (2013 a). DNA “barcoding” of Schistosoma mansoni across sub-Saharan Africa supports substantial within locality diversity and geographical separation of genotypes. Acta Tropica 128, 250260.
Webster, B. L., Diaw, O. T., Seye, M. M., Webster, J. P. and Rollinson, D. (2013 b). Introgressive hybridization of Schistosoma haematobium group species in Senegal: species barrier break down between ruminant and human schistosomes. PLoS Neglected Tropical Diseases 7, e2110.
WHO (2006). Preventive chemotherapy in human helminthiasis – Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. World Health Organization 62.

Keywords

Related content

Powered by UNSILO
Type Description Title
WORD
Supplementary materials

Boon et al. supplementary material
Figures S1-S2

 Word (11.9 MB)
11.9 MB

Barcoding hybrids: heterogeneous distribution of Schistosoma haematobium × Schistosoma bovis hybrids across the Senegal River Basin

  • NELE A. M. BOON (a1) (a2), FREDERIK VAN DEN BROECK (a3), DJIBY FAYE (a4), FILIP A. M. VOLCKAERT (a1), SOULEYMANE MBOUP (a5), KATJA POLMAN (a2) and TINE HUYSE (a6)...

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.