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Heredity of specific host-finding behaviour in Schistosoma mansoni miracidia

Published online by Cambridge University Press:  13 May 2004

M. KALBE ,
B. HABERL ,
J. HERTEL  and
W. HAAS
M. KALBE
Affiliation:
Department of Evolutionary Ecology, Max Planck Institute for Limnology, August-Thienemann-Strasse 2, D-24306 Plön, Germany Institute for Zoology I, University of Erlangen, Staudtstrasse 5, 91058 Erlangen, Germany
B. HABERL
Affiliation:
Institute for Zoology I, University of Erlangen, Staudtstrasse 5, 91058 Erlangen, Germany
J. HERTEL
Affiliation:
Institute for Zoology I, University of Erlangen, Staudtstrasse 5, 91058 Erlangen, Germany
W. HAAS
Affiliation:
Institute for Zoology I, University of Erlangen, Staudtstrasse 5, 91058 Erlangen, Germany
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Abstract

Two strains of Schistosoma mansoni were used to investigate the hereditary basis of species-specific host recognition by analysing behavioural responses of miracidia to snail-conditioned water. An Egyptian strain of S. mansoni, capable of distinguishing its host snail Biomphalaria alexandrina from other snails was cycled repeatedly through Biomphalaria glabrata, the intermediate host of a Brazilian strain known to respond even to non-susceptible snails with high intensity. After 5 cycles in the non-natural host, miracidia of the Egyptian strain still retained their preference for the original host snail. In a second experiment, host-finding behaviour of hybrids between these two parasite strains was studied. In the F1 generation, hybrids of both parental combinations showed the same low degree of specificity as the pure-bred Brazilian strain. Approximately one quarter of F2 hybrids proved to be as discriminatory as the Egyptian strain, confirming dominant Mendelian inheritance of non-specificity in schistosome miracidial host-finding behaviour. Moreover, hybrids seem to have lost the ability to develop in B. alexandrina, possibly suggesting a link between host recognition and host compatibility. The heredity of this behavioural trait is of evolutionary and epidemiological significance, since a shift to low host-finding specificity might have been a prerequisite for S. mansoni to acquire new host snails after being introduced to South America by the slave trade.

Keywords

Schistosoma mansonimiracidiahost-finding behaviourhybridsspecies-specificityadaptation
Type
Research Article
Information
Parasitology , Volume 128 , Issue 6 , June 2004 , pp. 635 - 643
Copyright
2004 Cambridge University Press

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References

REFERENCES

ADEMA, C. M. & LOKER, E. S. (1997). Specificity and immunobiology of larval digenean–snail associations. In Advances in Trematode Biology (ed. Fried, B. & Graczyk, T. K.), pp. 229–263. CRC Press, Boca Raton, FL, USA.
BASCH, P. F. (1976). Parasitological review: intermediate host specificity in Schistosoma mansoni. Experimental Parasitology 39, 150–169.CrossRefGoogle Scholar
BAYNE, C. J., HAHN, U. K. & BENDER, R. C. (2001). Mechanisms of molluscan host resistance and of parasite strategies for survival. Parasitology 123 (Suppl.), S159–S167.CrossRefGoogle Scholar
BAYNE, C. J. & YOSHINO, T. P. (1989). Determinants of compatibility in mollusc-trematode parasitism. American Zoologist 29, 399–407.CrossRefGoogle Scholar
BARBOSA, F. S. & CARNEIRO, E. (1965). Penetration of Schistosoma mansoni miracidia in abnormal hosts. Revista do Instituto de Medicina Tropical de São Paulo 7, 99–102.Google Scholar
BLAIR, D., DAVIS, G. M. & WU, B. (2001). Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123 (Suppl.), S229–S243.CrossRefGoogle Scholar
BROWN, D. S. (1994). Freshwater Snails of Africa and their Medical Importance, 2nd Edn. Taylor and Francis, London.
CAMPBELL, G., JONES, C. S., LOCKYER, A. E., HUGHES, S., BROWN, D., NOBLE, L. R. & ROLLINSON, D. (2000). Molecular evidence supports an African affinity of the neotropical freshwater gastropod, Biomphalaria glabrata, Say 1818, an intermediate host for Schistosoma mansoni. Proceedings of the Royal Society London, Series B 267, 2351–2358.CrossRefGoogle Scholar
CHASSÉ, J. L. & THÉRON, A. (1988). An example of circular statistics in chronobiological studies: analysis of polymorphism in the emergence rhythm of Schistosoma mansoni cercariae. Chronobiology International 5, 433–439.CrossRefGoogle Scholar
CHERNIN, E. & PERLSTEIN, J. M. (1971). Protection of snails against miracidia of Schistosoma mansoni by various aquatic invertebrates. Journal of Parasitology 57, 217–219.CrossRefGoogle Scholar
CHIPEV, N. H. (1993). Decoy effect and host infection by miracidia within snail communities. Parasitology 106, 265–276.CrossRefGoogle Scholar
CHRISTENSEN, N. Ø., NANSEN, P. & FRANDSEN, F. (1976). Molluscs interfering with the capacity of Fasciola hepatica miracidia to infect Lymnaea truncatula. Parasitology 73, 161–167.CrossRefGoogle Scholar
COMBES, C. (1991). Evolution of parasite life cycles. In Parasite–Host Associations – Coexistence or Conflict? (ed. Toft, A. C., Aeschlimann, A. & Bolis, L.), pp. 62–82. Oxford University Press, Oxford.
COMBES, C. & MONÉ, H. (1987). Possible mechanisms of the decoy effect in Schistosoma mansoni transmission. International Journal for Parasitology 17, 971–975.CrossRefGoogle Scholar
DeJONG, R. J., MORGAN, J. A. T., PARAENSE, W. L., POINTIER, J.-P., AMARISTA, M., AYEH-KUMI, P. F. K., BABIKER, A., BARBOSA, C. S., BREMOND, P., CANESE, A. P., DE SOUZA, C. P., DOMINGUEZ, C., FILE, S., GUTIERREZ, A., INCANI, R. N., KAWANO, T., KAZIBWE, F., KPIKPI, J., LWAMBO, N. J. S., MIMPFOUNDI, R., NJIOKOU, F., PODA, J. N., SENE, M., VELASQUEZ, L. E., YONG, M., ADEMA, C. M., HOFKIN, B. V., MKOJI, G. M. & LOKER, E. S. (2001). Evolutionary relationships and biogeography of Biomphalaria (Gastropoda: Planorbidae) with implications regarding its role as host of the human bloodfluke, Schistosoma mansoni. Molecular Biology and Evolution 18, 2225–2239.CrossRefGoogle Scholar
DESPRÉS, L., IMBERT-ESTABLET, D. & MONNEROT, M. (1993). Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Molecular and Biochemical Parasitology 60, 221–230.CrossRefGoogle Scholar
DUBOIS, M., GILES, K. A., HAMILTON, J. K., REBERS, P. A. & SMITH, F. ( 1956). Colorimetric methods for determination of sugars and related substance. Analytical Chemistry 28, 350–356.CrossRefGoogle Scholar
GASSER, R. B., MOHARAN, G. & MITCHEL, G. F. (1991). Sexing single larval stages of Schistosoma mansoni by polymerase chain reaction. Molecular and Biochemical Parasitology 47, 255–258.CrossRefGoogle Scholar
GREVELDING, C. G., KAMPKÖTTER, A. & KUNZ, W. (1997). Schistosoma mansoni: sexing cercariae by PCR without DNA extraction. Experimental Parasitology 85, 99–100.CrossRefGoogle Scholar
FILES, V. S. & CRAM, E. B. (1949). A study on the comparative susceptibility of snail vector to strains of Schistosoma mansoni. Journal of Parasitology 35, 555–560.CrossRefGoogle Scholar
HAAS, W., HABERL, B., KALBE, M. & KÖRNER, M. (1995). Snail-host finding by miracidia and cercariae: chemical host cues. Parasitology Today 11, 468–472.CrossRefGoogle Scholar
HABERL, B. & HAAS, W. (1992). Miracidium of Schistosoma mansoni: a macromolecular glycoconjugate as signal for the behaviour after contact with the snail host. Comparative Biochemistry and Physiology 101A, 329–333.CrossRefGoogle Scholar
HABERL, B., KALBE, M., FUCHS, H., STRÖBEL, M., SCHMALFUSS, G. & HAAS, W. (1995). Schistosoma mansoni and S. haematobium: miracidial host-finding behaviour is stimulated by macromolecules. International Journal for Parasitology 25, 551–560.Google Scholar
HABERL, B., KÖRNER, M., SPENGLER, Y., HERTEL, J., KALBE, M. & HAAS, W. (2000). Host-finding in Echinostoma caproni: miracidia and cercariae use different signals to identify the same snail species. Parasitology 120, 479–486.CrossRefGoogle Scholar
HASSAN, A. H. M., HABERL, B., HERTEL, J. & HAAS, W. (2003). Miracidia of an Egyptian strain of Schistosoma mansoni differentiate between sympatric snail species. Journal of Parasitology 89, 1248–1250.CrossRefGoogle Scholar
IMBERT-ESTABLET, D. & COMBES, C. ( 1986). Schistosoma mansoni: comparison of a Caribbean and African strain and experimental crossing based on compatibility with intermediate hosts and Rattus rattus. Experimental Parasitology 61, 210–218.CrossRefGoogle Scholar
KALBE, M., HABERL, B. & HAAS, W. (1996). Schistosoma mansoni miracidial host-finding: species-specificity of an Egyptian strain. Parasitology Research 82, 8–13.CrossRefGoogle Scholar
KALBE, M., HABERL, B. & HAAS, W. (1997). Miracidial host-finding in Fasciola hepatica and Trichobilharzia ocellata is stimulated by species-specific glycoconjugates from the host snails. Parasitology Research 83, 806–812.CrossRefGoogle Scholar
KALBE, M., HABERL, B. & HAAS, W. (2000). Snail host finding by Fasciola hepatica and Trichobilharzia ocellata: compound analysis of ‘Miracidia-Attracting Glycoproteins’. Experimental Parasitology 96, 231–242.CrossRefGoogle Scholar
KOCK, S. (2001). Investigations of the intermediate host specificity help to elucidate the taxonomic status of Trichobilharzia ocellata (Digenea: Schistosomatidae). Parasitology 123, 67–70.CrossRefGoogle Scholar
LIVELY, C. M. (1999). Migration, virulence and the geographic mosaic of adaptation by parasites. American Naturalist 153, S34–S47.CrossRefGoogle Scholar
LIVELY, C. M. & DYBDAHL, M. F. (2000). Parasite adaptation to locally common host genotypes. Nature, London 405, 679–681.CrossRefGoogle Scholar
MONÉ, H. & COMBES, C. (1986). Analyse expérimentale de l'effet ‘decoy’ (ou effet leurre) exercé par les mollusques non cibles sur le système hôte–parasite Biomphalaria glabrata (Say, 1818) – Schistosoma mansoni Sambon, 1907. Acta Oecologica. Oecologica Applicata 7, 281–286.Google Scholar
MORGAN, J. A. T., DEJONG, R. J., SNYDER, S. D., MKOOJI, G. M. & LOKER, E. S. (2001). Schistosoma mansoni and Biomphalaria: past history and future trends. Parasitology 123 (Suppl.), S211–S228.CrossRefGoogle Scholar
MUTANI, A., CHRISTENSEN, N. Ø. & FRANDSEN, F. (1985). A study of the biological characteristics of a hybrid line between male Schistosoma haematobium (Dar es Salaam, Tanzania) and S. intercalatum (Edea, Cameroun). Acta Tropica 42, 319–331.Google Scholar
PARAENSE, W. L. & CORRÊA, L. R. (1981). Observations on two biological races of Schistosoma mansoni. Memórias do Instituto Oswaldo Cruz 76, 287–291.CrossRefGoogle Scholar
SALADIN, K. S. (1979). Behavioral parasitology and perspectives on miracidial host-finding. Zeitschrift für Parasitenkunde 60, 197–210.CrossRefGoogle Scholar
TCHUEM TCHUENTÉ, L. A., SOUTHGATE, V. R., JOURDANE, J., KAUKAS, A. & VERCRUYSSE, J. (1997). Hybridisation between digenean Schistosoma haematobium and S. mattheei: viability of hybrids and their development in sheep. Systematic Parasitology 36, 123–131.Google Scholar
THÉRON, A. & COMBES, C. (1988). Genetic analysis of cercarial emergence rhythms. Genetics 18, 201–209.Google Scholar
THÉRON, A. & COMBES, C. (1995). Asynchrony of infection timing, habitat preference, and sympatric speciation of schistosome parasites. Evolution 49, 372–375.CrossRefGoogle Scholar
TOLEDO, R., MUÑOZ-ANTOLI, C., PEREZ, M. & ESTEBAN, J. G. (1999). Miracidial infectivity of Hypoderaeum conoideum (Trematoda: Echinostomatidae): differential susceptibility of two lymnaeid snails. Parasitology Research 85, 212–215.CrossRefGoogle Scholar
UPATHAM, E. S. (1972). Interference by unsusceptible aquatic animals with the capacity of the miracidia of Schistosoma mansoni Sambon to infect Biomphalaria glabrata (Say) under field-simulated conditions in St. Lucia, West Indies. Journal of Helminthology 46, 277–283.CrossRefGoogle Scholar
WEBBE, G. & JAMES, C. (1971). The importation and maintenance of schistosomes of medical and veterinary importance. In Isolation and Maintenance of Parasites in vivo (ed. Taylor, A. E. R. & Muller, R.). Symposia of the British Society for Parasitology, vol. 9, pp. 77–107. Blackwell, Oxford.
WEBSTER, J. P. & WOOLHOUSE, M. E. J. (1998). Selection and strain specificity of compatibility between snail intermediate host and their parasitic schistosomes. Evolution 5, 1627–1634.CrossRefGoogle Scholar
WEBSTER, J. P. (2001). Compatibility and sex in a snail-schistosome system. Parasitology 122, 423–432.CrossRefGoogle Scholar
WEBSTER, P., MANSOUR, T. E. & BIEBER, D. (1989). Isolation of a female specific, highly repeated Schistosoma mansoni DNA probe and its use in an assay of cercarial sex. Molecular and Biochemical Parasitology 36, 217–222.CrossRefGoogle Scholar
WEBSTER, B. L. & SOUTHGATE, V. R. (2003). Compatibility of Schistosoma haematobium, S. intercalatum and their hybrids with Bulinus truncatus and B. forskalii. Parasitology 127, 231–242.Google Scholar
WILSON, R. A. & DENISON, J. (1970). Short chain fatty acids as stimulants of turning activity by the miracidium of Fasciola hepatica. Comparative Biochemistry and Physiology 32, 511–517.CrossRefGoogle Scholar
WOODRUFF, D. S. & MULVEY, M. (1997). Neotropical schistosomiasis: African affinities of the host snail Biomphalaria glabrata (Gastropoda: Planorbidae). Biological Journal of the Linnean Society 60, 505–516.CrossRefGoogle Scholar
WRIGHT, C. A. (1971). Flukes and Snails. George Allen and Unwin Ltd, London.
WRIGHT, C. A. & SOUTHGATE, V. R. (1976). Hybridisation of schistosomes and some of its implications. In Genetic Aspects of Host–Parasite Relationships (ed. Taylor, A. E. R. & Muller, R. ), pp. 55–86. Blackwell, Oxford.