Hostname: page-component-76fb5796d-qxdb6 Total loading time: 0 Render date: 2024-04-28T10:48:09.183Z Has data issue: false hasContentIssue false

Interactions between population growth and sexual reproduction in the viviparous monogenean Gyrodactylus turnbulli Harris, 1986 from the guppy, Poecilia reticulata Peters

Published online by Cambridge University Press:  06 April 2009

P.D. Harris
Affiliation:
Department of Zoology and Comparative Physiology, University of Birmingham, P.O. Box 363, Birmingham B15 2TT

Summary

Mating was observed in populations of Gyrodactylus turnbulli from guppies. Copulation took place between older (post-1st birth) flukes and resulted in the insemination of spermatozoa into the seminal receptacle. New-born flukes, and flukes which had only recently given birth for the first time (in which the penis was absent or developing), were never inseminated. Flukes were promiscuous, copulating with several partners in succession. The occurrence of mating was related to the size, age and crowding of the G. turnbulli population, taking place most frequently when the parasites were most densely crowded upon the peduncle of the fish on days 5 and 6 of the infection. Maximum population size was positively correlated with the number of flukes initiating an infection. As a result, mating began earlier, and continued for longer in populations founded by several parasites rather than those begun by single flukes. These observations are discussed with respect to the population biology of G. turnbulli: it is likely that sexual and asexual reproduction alternate, with sex being important only during phases of epidemic population growth. The significance of sex in gyrodactylids is discussed, and the potential importance of continuous sexual reproduction in G. turnbulli infections on cultivated guppies is noted.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1989

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

Bell, G. (1982). The Masterpiece of Nature: the Evolution and Genetics of Sexuality. London and Canberra: Croon Helm.Google Scholar
Braun, E. (1966). Beiträge zur mikroskopischen Anatomie und Fortpflanzungsbiologie von Gyrodactylus wageneri V. Nordmann, 1832. Zeitschrift für Parasitenkunde 28, 142–74.CrossRefGoogle ScholarPubMed
Bychowsky, B. E. (1957). Monogenetic Trematodes, their Systematics and Phylogeny. Moscow and Leningrad: Academy of Sciences U.S.S.R. [In Russian] English translation by W. J. Hargis & P. C. Oustinoff (1961). Washington: American Institute of Biological Sciences.Google Scholar
Case, T. J. & Taper, M. L. (1986). On the coexistence and coevolution of asexual and sexual competitors. Evolution 40, 366–87.CrossRefGoogle ScholarPubMed
Esch, G. W., Gibbons, J. W. & Bourque, J. E. (1975). An analysis of the relationship between stress and parasitism. American Midland Naturalist 93, 339–53.CrossRefGoogle Scholar
Gille, K. (1914). Untersuchungen über die Eireifung, Befruchtung und Zellteilung von Gyrodactylus elegans v. Nordmann. Archiv für Zellforschung 12, 415–56.Google Scholar
Goven, B. A. & Amend, D. F. (1982). Mebendazole/trichlorfon combination: a new anthelminthic for removing monogenetic trematodes from fish. Journal of Fish Biology 20, 373–8.CrossRefGoogle Scholar
Harris, P. D. (1983). The morphology and life-cycle of the oviparous Oogyrodactylus farlowellae gen. et sp.nov. (Monogenea, Gyrodactylidea). Parasitology 87, 405–20.CrossRefGoogle Scholar
Harris, P. D. (1985). Observations on the development of the male reproductive system in Gyrodactylus gasterostei Glaser, 1974 (Monogenea, Gyrodactylidea). Parasitology 91, 519–29.CrossRefGoogle Scholar
Harris, P. D. (1986). Species of Gyrodactylus von Nordmann, 1832 (Monogenea, Gyrodactylidea) from poeciliid fishes with a description of G. turnbulli sp. nov. from the guppy, Poecilia reticulata Peters. Journal of Natural History 20, 183–91.CrossRefGoogle Scholar
Harris, P. D. (1988). Changes in the site specificity of Gyrodactylus turnbulli Harris, 1986 (Monogenea) during infections of individual guppies (Poecilia reticulata Peters). Canadian Journal of Zoology (in the Press).CrossRefGoogle Scholar
Harris, P. D. & Tinsley, R. C. (1987). The biology of Gyrdicotylus gallieni, an unusual viviparous monogenean from the African clawed toad, Xenopus laevis. Journal of Zoology 212, 325–46.CrossRefGoogle Scholar
Hebert, P. D. N., Ward, R. D. & Weider, L. J. (1988). Clonal diversity patterns and breeding system variation in Daphnia pulex, an asexual-sexual complex. Evolution 42, 147–59.Google ScholarPubMed
Jackson, H. (1982). Protopolystoma xenopodis: success of reproduction in single and multiple worm infections. Parasitology 85, v.Google Scholar
Katheriner, L. (1904). Ueber die Entwicklung von Gyrodactylus v. Nrd. Zoologischer Jahrbucher 7, Supplyes. 519–51.Google Scholar
Kearn, G. C. (1970). The physiology and behaviour of the monogenean skin parasite Entobdella soleae in relation to its host (Solea solea). In Ecology and Physiology of parasites (ed. Fallis, A. M.), pp. 161–87. Toronto: University of Toronto Press.Google Scholar
Kritscky, D. C. (1976). Observations on the ultrastructure of spermatozoa and spermiogenesis in the monogenean Gyrodactylus eucaliae Ikezaki and Hoffman, 1957. [In Russian.] Proceedings of the Institute of Biology and Pedology, Far-East Science Centre, Academy of Sciences of the USSR, N.S. 34, 70–4.Google Scholar
Lester, R. J. G. & Adams, J. R. (1974). Gyrodactylus alexanderi: reproduction, mortality and effect on the host. Canadian Journal of Zoology 52, 827–33.CrossRefGoogle Scholar
Llewellyn, J. (1983). Sperm transfer in the monogenean gill parasite Gastrocotyle trachuri. Proceedings of the Royal Society, B219, 439–46.Google Scholar
Lynch, M. (1984). Destabilising hybridisation, general-purpose genotypes and geographical parthenogenesis. Quarterly Reviews of Biology 59, 257–90.CrossRefGoogle Scholar
Lynch, M. & Gabriel, W. (1983). Phenotypic evolution and parthenogenesis. American Naturalist 122, 745–64.CrossRefGoogle Scholar
Macdonald, S. & Caley, J. (1975). Sexual reproduction in the monogenean Diclidophora merlangi: tissue penetration by sperms. Zeitschrift für Parasitenkunde 45, 323–34.CrossRefGoogle ScholarPubMed
Mackiewicz, J. S. (1981). Caryophyllidea (Cestoidea): evolution and classification. In Advances in Parasitology vol. 19, (ed. Lumsden, W. H. R., Baker, J. R. and Muller, R.) pp. 136206, New York and London: Academic Press.Google Scholar
Madhavi, R. & Anderson, R. M. (1985). Variability in the susceptibility of the fish host Poecilia reticulata to infection with Gyrodactylus bullatarudis. Parasitology 91, 531–44.CrossRefGoogle Scholar
Malmberg, G. (1956). On a new genus of viviparous monogenetic trematodes. Arkiv für Zoologie 10, 317–29.Google Scholar
Minouchi, O. (1936). Cytologische Studien über des Ei von Polystoma intergerrimum von der Eiablage bis zu den fruhen Furchungstadien. Zeitschrift für Zellforschung und mikroskopischen Anatomie 24, 85127.CrossRefGoogle Scholar
Nollen, P. M. (1983). Patterns of sexual reproduction among parasitic platyhelminths. In The Reproductive Biology of Parasites, Symposia of the British Society of Parasitology, vol. 20 (ed. Whitfield, P. J.) Parasitology 86, 99120.Google Scholar
Reznick, D. N. & Endler, J. A. (1982). The impact of predation on life history evolution in Trinidadian guppies. Evolution 36, 160–70.Google ScholarPubMed
Scott, M. E. (1982). Reproductive potential of Gyrodactylus bullatarudis on guppies (Poecilia reticulata). Parasitology 85, 217–36.CrossRefGoogle Scholar
Scott, M. E. (1985 a). Experimental epidemiology of Gyrodactylus (Monogenea) on guppies (Poecilia reticulata): short and long term studies. In Ecology and Genetics of Host Parasite Interactions (ed. Rollinson, D. and Anderson, R. M.), Linnaean Society Symposium No. 11, pp. 2138. London, New York: Academic Press.Google Scholar
Scott, M. E. (1985 b). Dynamics of challenge infections of Gyrodactylus bullatarudis Turnbull (Monogenea) on guppies, Poecilia reticulata Peters. Journal of Fish Diseases 8, 495504.CrossRefGoogle Scholar
Scott, M. E. & Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis within laboratory populations of the fish host Poecilia reticulata. Parasitology 89, 159–95.CrossRefGoogle ScholarPubMed
Scott, M. E. & Nokes, D. J. (1984). Temperature dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89, 221–9.CrossRefGoogle Scholar
Scott, M. E. & Robinson, M. A. (1984). Challenge infections of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata) following treatment. Journal of Fish Biology 24, 581–6.CrossRefGoogle Scholar
Thibault, R. E. & Schultz, R. J. (1978). Reproductive adaptations amongst viviparous fishes (Poecilidae). Evolution 32, 320–33.CrossRefGoogle Scholar
Wagener, G. R. (1860). Ueber Gyrodactylus elegans von Nordmann. Archiv fur Anatomisch und Physiologisch Wissenschaft 768–97.Google Scholar
Williams, G. C. (1975). Sex and Evolution. Princeton, New Jersey: Princeton University Press.Google ScholarPubMed