Skip to main content Accessibility help
×
Home

Signatures of mito-nuclear discordance in Schistosoma turkestanicum indicate a complex evolutionary history of emergence in Europe

  • SCOTT P. LAWTON (a1), LAUREN I. BOWEN (a1), AIDAN M. EMERY (a2) and GÁBOR MAJOROS (a3)

Summary

High levels of molecular diversity were identified in mitochondrial cytochrome c oxidase (cox1) gene sequences of Schistosoma turkestanicum from Hungary. These cox1 sequences were all specific to Hungary which contrasted with the low levels of diversity seen in the nuclear internal transcribed spacer region (ITS) sequences, the majority of which were shared between China and Iran isolates. Measures of within and between host molecular variation within S. turkestanicum showed there to be substantial differences in molecular diversity, with cox1 being significantly more diverse than the ITS. Measures of haplotype frequencies revealed that each host contained its own subpopulation of genetically unique parasites with significant levels of differentiation. Pairwise mismatch analysis of cox1 sequences indicated S. turkestanicum populations to have a bimodal pairwise difference distribution and to be stable unlike the ITS sequences, which appeared to have undergone a recent population expansion event. Positive selection was also detected in the cox1 sequences, and biochemical modelling of the resulting protein illustrated significant mutational events causing an alteration to the isoelectric point of the cox1 protein, potentially altering metabolism. The evolutionary signature from the cox1 indicates local adaptation and long establishment of S. turkestanicum in Hungary with continual introgression of nuclear genes from Asian isolates. These processes have led to the occurrence of mito-nuclear discordance in a schistosome population

Copyright

Corresponding author

*Corresponding author: Molecular Parasitology Laboratory, School of Life Sciences, Pharmacy and Chemistry, Kingston University, Kingston upon Thames, Surrey KT1 2EE, UK. E-mail: s.p.lawton@kingston.ac.uk

References

Hide All
Attwood, S. W., Fatih, F. A. and Upatham, E. S. (2008). DNA-sequence variation among Schistosoma mekongi populations and related taxa; phylogeography and the current distribution of Asian schistosomiasis. PLoS Neglected Tropical Diseases 2, e200.
Brusentsov, I. J., Katokhin, A. V., Brusentsova, I. V., Shekhovtsov, S. V., Borovikov, S. N., Goncharenko, G. G., Lider, L. A., Romashov, B. V., Rusinek, O. T., Shibitov, S. K., Suleymanov, M. M., Yevtushenko, A. V. and Mordvinov, V. A. (2013). Low genetic diversity in Wide spread Eurasian liver fluke Opisthorchis felineus suggest special demographic history of this trematode species. PLoS ONE 8, e62453.
Chamot, E., Tiscani, L. and Rougemont, A. (1998). Public health importance and risk factors for cercarial dermatitis associated with swimming in Lake Leman at Geneva, Switzerland. Epidemiolology & Infection 120, 305314.
Cheviron, Z. A. and Brumfield, R. T. (2009). Migration-selection balance and local adaptation of mitochondrial haplotypes in rufous collard sparrows (Zonotrichia capensis) along an elevational gradient. Evolution 63, 15931605.
Clement, M., Posada, D. and Crandall, K. A. (2000). TCS: a computer program to estimate gene genealogies. Molecular Ecology 9, 16571660.
Criscione, C. D., Poulin, R. P. and Blouin, M. S. (2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 22472257.
Curtis, J. and Minchella, D. J. (2000). Schistosome genetic structure: when clumping worms isn't just splitting hairs. Parasitology Today 16, 6871.
Curtis, J., Sorensen, R. E. and Minchella, D. J. (2002). Schistosome genetic diversity: the implications of population structure as detected with microsatellite markers. Parasitology 125 (Suppl.), S51S59.
Denton, R. D., Kenyon, L. J., Greenwald, K. R. and Lisle, H. (2014). Evolutionary basis of mito-nuclear discordance between sister species of mole salamanders (Ambystoma sp.). Molecular Ecology 23, 28112824.
Excoffer, L. and Lischer, H. E. L. (2010). Arliquin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10, 564567.
Gompert, Z., Forister, M. L., Fordyces, J. A. and Nice, C. C. (2008). Widespread mito-nuclear discordance with evidence for introgressive hybridization and selective sweeps in Lycaeides . Molecular Ecology 17, 52315244.
Goulding, T. C. and Cohen, C. S. (2014). Phylogeography of marine acanthocephalan: lack of cryptic diversity in a cosmopolitan parasite of mole crabs. Journal of Biogeography 41, 965976.
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hanelt, B., Mwangi, I. N., Kinuthia, J. M., Maina, G. M., Agola, L. E., Mutuku, M. W., Steinauer, M. L., Agwanda, B. R., Kigo, L., Mungai, B. N., Loker, E. S. and Mkoji, G. M. (2010). Schistosomes of small mammals from the Lake Victoria Basin, Kenya: new species, familiar species, and implications for schistosomiasis control. Parasitology 137, 11091118.
Horák, P. and Kolárová, L. (2010). Snails, waterfowl and cercarial dermatitis. Freshwater Biology 56, 779790.
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.
Katewa, S. D. and Ballard, J. W. O. (2007). Sympatric Drosophila simulans flies with distinct mtDNA show difference in mitochondrial respiration and electron transport. Insect Biochemistry and Molecular Biology 37, 213222.
Kodandaramaiah, U., Simonsen, T., Bromilow, S., Wahlberg, N. and Sperling, F. (2013). Deceptive single locus taxonomy and phylogeography: Walbachia-associated divergence in mitochondrial DNA is not reflected in morphology and nuclear markers in a butterfly species. Ecology & Evolution 3, 51675176.
Kolárová, L. (2007). Schistosomes causing cercarial dermatitis: a mini – review of current trends in systematic and of host specificity and pathogenicity. Folia Parasitologica 54, 8187.
Lawton, S. P. and Majoros, G. (2013). A foreign invader or a reclusive native? DNA bar coding reveals a distinct European lineage of the zoonotic parasite Schistosoma turkestanicum (syn. Orientobilharzia turkestanicum (Dutt and Srivastava, 1955)). Infection, Genetics & Evolution 13, 186193.
Librado, P. and Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14512452.
Lichtenbergova, L., Kolbekova, P., Kourilova, P., Kansy, M., Mikes, L., Haas, H., Schramm, G., Horak, P., Kolrova, L. and Mountford, A. P. (2008). Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunology 30, 585595.
Lu, D., Wang, T., Rudge, J. W., Donnelly, C. A., Fang, G. and Webster, J. P. (2011). Genetic diversity of Schistosoma japonicum miracidia from individual rodent hosts. International Journal for Parasitology 41, 13711376.
Majoros, G., Dán, A. and Erdélyi, K. (2010). A natural focus of the blood fluke Orientobilharzia turkestanica (Skrjabin, 1913) (Trematoda: Schistosomatidae) in red deer (Cervus elaphus) in Hungary. Veterinary Parasitology 170, 218223.
McDonough, M. M., Šumbera, R., Mazoch, V., Ferguson, A. W., Phillips, C. D. and Bryja, J. (2015). Multilocus phylogeography of a widespread savanna-woodland-adapted rodents reveals the influence of Pleistocene geomorphology and climate change in Africa's Zambezi region. Molecular Ecology 24, 52485266.
Morales, H. E., Pavlova, A., Joseph, L. and Sunnucks, P. (2015). Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Molecular Ecology 24, 28202837.
Morgan, J. A. T., DeJong, R. J., Lwambo, N. J. S., Mungai, B. N., Mkoji, G. M. and Locker, E. S. (2003). First report of a natural hybrid between Schistosoma mansoni and S. rodaini . International Journal for Parasitology 89, 416418.
Nesi, N., Kadjo, B., Pourrut, X., Leroy, E., Shongo, C. P., Cruaud, C. and Hassanin, A. (2013). Molecular systematics and phylogeography of the tribe Myonycterini (Mammalia, Pteropodidae) inferred from mitochondrial and nuclear markers. Molecular Phylogenetics & Evolution 66, 126137.
Paczesniak, D., Jokela, J., Larkin, K. and Neiman, M. (2013). Discordance between nuclear and mitochondrial genomes in sexual and asexual lineages of the freshwater snail Potamopyrgus antipodarum . Molecular Ecology 22, 46954710.
Pavlova, A., Amos, J. N., Joseph, L., Loynes, K., Austin, J. J., Keogh, J. S., Stone, G. N., Nicholls, J. A. and Sunnucks, P. (2013). Perched at the mito-nuclear crossroads: divergent mitochondrial lineages correlate with environment in the face on ongoing nuclear gene flow in an Australian Bird. Evolution 67, 34123428.
Poole, J. E., Hellmann, I., Jensen, J. D. and Nielsen, R. (2010). Population genetic inference from genomic sequence variation. Genome Research 20, 291300.
Prugnolle, F., Theron, A., Pointer, J. P., Jabbour-Zahab, R., Jarne, P., Durand, P. and de Meeusm, T. (2005). Dispersal in a parasitic worm and it's two hosts: consequences for local adaptation. Evolution 59, 296303.
Rudge, J. W., Lu, D. B., Fang, G. R., Wang, T. P., Basanez, M. C. and Webster, J. P. (2009). Parasite genetic differentiation by habitat type and host species: molecular epidemiology of Schistosoma japonicum in hilly and marshland areas of Anuhui Province, China. Molecular Ecology 18, 21342146.
Sequeira, F., Sodré, D., Ferrand, N., Bernardi, J. A. R., Sampaio, I., Schneider, H. and Vallinoto, M. (2011). Hybridization and massive mtDNA unidirectional introgression between closely related Neotropical toads Rhinella marina and R. scheideri inferred from mtDNA and nuclear markers. BMC Evolutionary Biology 11, 264.
Silva, G., Lima, F. P., Martel, P. and Castilho, R. (2014). Thermal adaptation and clinal mitochondrial DNA variation of European anchovy. Proceedings of the Royal Society B 281, pii: 20141093.
Sire, C., Durand, P., Pointer, J. P. and Theron, A. (2001). Genetic diversity of Schistosoma mansoni within and among individual hosts (Rattus rattus): infrapopulation differentiation at microspatial scale. International Journal for Parasitology 31, 16091616.
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.
Sun, J., Wang, M., Zhang, Y., Chapuis, M., Jiang, X., Hu, G., Yang, X., Ge, C., Xue, X. and Hong, X. (2015). Evidence for high dispersal ability and mito-nuclear discordance in the small brown plant hopper, Laodelphax striatellus . Scientific Reports 5, 8045.
Tabaripour, R., Youssefi, M. R. and Tabaripour, R. (2015). Genetic Identification of Orientobilharzia turkestancicum from sheep isolates in Iran. Iranian Journal of Parasitology 10, 6268.
Toews, D. P. and Brelsford, A. (2012). The biogeography of mitochondrial and nuclear discordance in animals. Molecular Ecology 21, 39073930.
Tomasco, I. H. and Lessa, E. P. (2011). The evolution of mitochondrial genes in subterranean caviomorph rodents: adaptation against a background of purifying selection. Molecular Phylogenetics and Evolution 61, 6470.
Van den Broeck, F., Meurs, L., Raeymaekers, J. A. M., Boon, N., Dieye, T. N., Volchaert, F. A. M., Polman, K. and Huyse, T. (2014). Inbreeding within human Schistosoma mansoni: do host-specific factors shape the genetic composition of parasite populations? Heredity 113, 3241.
Wang, C. R., Chen, J., Zhao, J. P., Chen, A. H., Zhai, Y. Q., Li, L. and Zhu, X. Q. (2009). Orientobilharzia species: neglected parasitic zoonotic agents. Acta Tropica 109, 171175.
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). DNA ‘barcoding’ of Schistosoma mansoni across sub-Saharan Africa supports substantial within locality diversity and geographical separation of genotypes. Acta Tropica 128, 250260.
Wikström, M. and Verkhovsky, M. I. (2011). The D-channel of cytochrome oxidase: an alternative view. Biochemica et Biophysica Acta 1807, 12731278.
Woolley, S., Johnson, J., Smith, M. J., Crandall, K. A. and McClellan, D. A. (2003) TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 19, 671672.
Zhao, Q. P., Jiang, M. S., Dong, H. F. and Nie, P. (2012). Diversification of Schistosoma japonicum in Mainland China revealed by mitochondrial DNA. PLoS Neglected Tropical Diseases 6, e1503.

Keywords

Type Description Title
WORD
Supplementary materials

Lawton supplementary material
Table S1

 Word (16 KB)
16 KB
WORD
Supplementary materials

Lawton supplementary material
Figure S1

 Word (740 KB)
740 KB

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