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Environmental sex determination and density-dependent population regulation in the entomogenous nematode Romanomermis culicivorax

Published online by Cambridge University Press:  06 April 2009

G. A. Tingley  and
R. M. Anderson
G. A. Tingley
Affiliation:
Department of Pure and Applied Biology, Imperial College, Prince Consort Road, London SW7 2BB
R. M. Anderson
Affiliation:
Department of Pure and Applied Biology, Imperial College, Prince Consort Road, London SW7 2BB
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Summary

Environmental sex determination in the mermithid nematode Romanomermis culicivorax is examined in the context of parasite reproductive success and population regulation. Experimental results show that the sex ratio of the nematode within its mosquito host (Culex quinquefasciatus) is dependent on parasite density. Sex ratios are biased to females at low parasite burdens and to males at high parasite burdens. Low temperature further enhances female-biased ratios. The net effect of density-dependent sex determination on parasite and host population growth is shown to be critically dependent on the frequency distribution of parasite numbers/host. Mermithid parasite distributions within natural host populations show low degrees of aggregation relative to other helminth species. The population regulation of the parasite is examined with respect to environmental sex determination and parasite-induced host mortalities by means of simple mathematical models of the dynamics of parasite transmission via its life-cycle. The significance of regulatory constraints on population growth are discussed in relation to the use of mermithids as biological control agents of insect pests or disease vectors.

Type
Research Article
Information
Parasitology , Volume 92 , Issue 2 , April 1986 , pp. 431 - 449
Copyright
Copyright © Cambridge University Press 1986

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References

REFERENCES

Anderson, R. M. (1978 a). The regulation of host population growth by parasitic species. Parasitology 76, 119–57.CrossRefGoogle ScholarPubMed
Anderson, R. M. (1978 b). Population dynamics of snail infection by miracidia. Parasitology 77, 201–24.CrossRefGoogle ScholarPubMed
Anderson, R. M. & Crombie, J. A. (1984). Experimental studies of age prevalence curves for Schistosoma mansoni infections in populations of Biomphalaria glabrata. Parasitology 89, 78–105.CrossRefGoogle ScholarPubMed
Anderson, R. M. & Gordon, D. M. (1982). Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortalities. Parasitology 85, 373–98.CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host-parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–47.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1979). Population biology of infectious diseases. Part I. Nature, London 280, 361–7.CrossRefGoogle ScholarPubMed
Anderson, R. M., Whltfield, P. J. & Dobson, A. P. (1978 a). Experimental studies of infection dynamics: infection of the definitive host by the cercariae of Transuersotrema patialense. Parasitology 77, 189–200.CrossRefGoogle ScholarPubMed
Anderson, R. M., Whitfield, P. J., Donson, A. P. & Keymer, A. E. (1978 b). Concomitant predation and infection processes: an experimental study. Journal of Animal Ecology 47, 891–911.CrossRefGoogle Scholar
Brown, B. J. & Platzer, E. G. (1977). The effects of temperature on the infectivity of Romanomermis culicivorax. Journal of Nematology 9, 166–72.Google ScholarPubMed
Bull, B. J. (1980). Sex determination in reptiles. The Quarterly Review of Biology 55, 3–21.CrossRefGoogle Scholar
Bull, J. J. (1983). Evolution of Sex-determining Mechanisms. Benjamin Cummings.Google Scholar
Buxton, P. A. (1937). The numbers of males and females in natural populations of head-lice (Pediculus: Anoplura). Proceedings of the Royal Entomological Society of London 12, 12–14.CrossRefGoogle Scholar
Chapman, H. C. & Finney, J. R. (1982). Mass production of mermithid and steinernematid nematodes with vector control potential. In Invertebrate Pathology and Microbial Control, Proceedings of the 3rd International Colloquium on Invertebrae Pathology, 1982, Brighton, UK, pp. 358–362.Google Scholar
Charnov, E. L. & Bull, J. J. (1977). When is sex environmentally determined? Nature 266, 828–30.CrossRefGoogle ScholarPubMed
Charnov, E. L., Los-Den Hartogh, R. L., Jones, W. T. & Van Den Assem, J. (1981). Sex ratio evolution in a variable environment. Nature, London 289, 27–33.CrossRefGoogle Scholar
Christie, J. R. (1929). Some observation on sex in the Mermithidae. Journal of Experimental Zoology 53, 59–76.CrossRefGoogle Scholar
Clausen, C. P. (1939). The effect of host size upon the sex ratio of hymenopterous parasites and its relation to methods of rearing and colonization. Journal of the New York Entomological Society 47, 1–9.Google Scholar
Crombie, J. A. & Anderson, R. M. (1985). Repeated infection of mice with Schistosoma mansoni: population dynamics and acquired immunity. Nature, London (in the Press).CrossRefGoogle Scholar
Ellenby, C. (1954). Environmental determination of the sex ratio of a plant parasitic nematode. Nature, London 174, 1016–17.CrossRefGoogle Scholar
Ezenwa, A. O. & Carter, N. E. (1975). Influence of multiple infections on sex ratios of mermithid parasites of blackflies. Environmental Entomology 4, 142–4.CrossRefGoogle Scholar
Ferguson, M. W. J. & Joanen, T. (1982). Temperature of egg incubation determines sex in Alligator misissippiensis. Nature, London 296, 850–3.CrossRefGoogle Scholar
Fisher, R. A. (1930). The Genetical Theory of Natural Selection. Oxford: Oxford University Press.CrossRefGoogle Scholar
Flanders, S. E. (1956). The mechanism of sex regulation in the (parasitic) Hymenoptera. Insectes Sociaux 3, 325–34.CrossRefGoogle Scholar
Galloway, T. D. & Brust, R. A. (1976). Observations on mermithid parasites of mosquitoes in Manitoba. Proceedings of the First International Colloquium on Invertebrate Pathology pp. 227–31. Kingston, Ontario, Canada.Google Scholar
Galloway, T. D. & Brust, R. A. (1977). Effects of temperature and photoperiod on the infection of two mosquito species by the mermithid Ronianomermis culicivorax. Journal of Nematology 9, 218–21.Google ScholarPubMed
Geodakin, V. A., Kosobutski, V. I. & Bileva, D. S. (1967). The negative feedback regulation of sex ratio. Genetika 9, 153–63.Google Scholar
Gordon, R., Squires, J. M., Babie, S. J. & Burford, I. R. (1981). Effects of host diet on Romanomermis culicivorax, a mermithid parasite of mosquitoes. Journal of Nematology 13, 285–90.Google ScholarPubMed
Hannah, A. (1955). The effect of aging the maternal parent upon the sex ratio in Drosophila melanogaster. Zeitschrifl für inductive Abstammungs und Verenbungslehre 86, 574–99.Google ScholarPubMed
Hassell, M. P. & Waage, J. K. (1984). Host-parasite population interactions. Annual Review of Entomology 29, 89–114.CrossRefGoogle Scholar
Hertwig, R. (1912). Über den derzeitigen Stand des sexual Probleme. Biologisches Zentralbiall 32, 1–146.Google Scholar
Hominick, W. M. & Tingley, G. A. (1984). Mermithid nematodes and the control of insect vectors of human disease. Commonwealth Agricultural Bureau. Biocontrol News and Information 5, 7–20.Google Scholar
Hominick, W. M. & Welch, H. E. (1971). Synchronization of life-cycles of three mermithids (Nematoda) with their chironomid (Diptera) hosts and some observations on the pathology of the infections. Canadian Journal of Zoology 49, 975–82.CrossRefGoogle Scholar
Hughes, D. S. & Platzer, E. G. (1977). Temperature effects on the parasitic phase of Ronzanoniermis culicivorax in Culex pipiens. Journal of Neinatology 9, 173–5.Google ScholarPubMed
James, H. C. (1937). The effect of delayed fertilization on the sex ratio of a species of insect in which the female is the heterogametic sex (Ephestia kuhniella Zell. Lepid. Phycitidae). Proceedings of the Royal Entomological Society of London 12, 92–8.CrossRefGoogle Scholar
Koliopanos, C. N. & Triantaphyllou, A. C. (1972). Effect of infection density on sex ratio of Ileterdoera glycines. Nematoloqica 18, 131–7.CrossRefGoogle Scholar
Kurihara, T. (1976). Population behaviour of Reesimermis nielseni, a nematode parasite of mosquitoes, with note on the attraction of infective stage nematodes by mosquito larvae Culex pipiens niolestus. Japanese Journal of Parasitology 25, 8–16.Google Scholar
Malaquin, A. (1901). Le parasitisme evolutifdes monstrillides. Archives de Zoologie Experimentale et Generale 9, 81–232.Google Scholar
May, R. M. (1973). Stability and Complexity in Model Ecosystems. Princeton: Princeton University Press.Google ScholarPubMed
May, R. M. & Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. II. Destabilizing processes. Journal of Animal Ecology 47, 249–67.CrossRefGoogle Scholar
Maynard Smite, J. (1978). Evolution of Sex. Cambridge: Cambridge University Press.Google Scholar
Mrsic, W. (1923). Die Spätbefruchtung und deren Einfiuss auf Entwicklung und Geschlechtsbildung. Archiv für mikroskopische Anatomie und Entwicklungsmechanilc 98, 129–209.CrossRefGoogle Scholar
Nickle, W. R. (1979). Probable establishment and overwintering of a mermithid parasite of mosquitoes in Maryland. Proceedings of the Ilelminthological Society of Washington 46, 21–7.Google Scholar
Parenti, U. (1962). Richerche sulla sessualita dei mermithidi. I. Rapporto sessi in una popolazione di Paramermis contorta. Archivivo Zoologico Italiano 47, 209–23.Google Scholar
Petersen, J. J. (1972). Factors affecting sex ratios of a mermithid parasite of mosquitoes. Journal of Nematology 4, 83–7.Google ScholarPubMed
Petersen, J. J. (1977). Effects of host size and parasite burden on sex ratio in the mosquito parasite Oct omyomermis muspratti. Journal of Nematology 9, 343–6.Google ScholarPubMed
Petersen, J. J., Chapman, H. C. & Woodard, D. B. (1968). Bionomics of a mermithid nematode of larval mosquitoes in southwestern Louisiana. Mosquito News 28, 345–52.Google Scholar
Petersen, J. J. & Willis, O. R. (1971). A two-year survey to determine the incidence of a mermithid nematode in mosquitoes in Louisiana. Mosquito News 31, 558–66.Google Scholar
Phelps, R. J. & Defoliart, G. R. (1964). Nematode Parasitism of Simuliidae. University of Wisconsin Research Bulletin No. 245, 78pp.Google Scholar
Platzer, E. C. & Brown, B. J. (1976). Physiological ecology of Reesimermis nielseni. Proceedings of the First International Colloquium on Invertebrate Pathology, Kingston, Canada, pp. 263–67.Google Scholar
Poinar, G. O. Jr. (1979). Nematodes for Biological Control of Insects. West Palm Beach: CRC Press.Google Scholar
Rubtzov, I. A. (1974). Aquatic mermithidae of the fauna of the USSR. US Department of Commerce, Clearing-house for Federal Scientific and Technical Information, Springfield, VA 22151, USA, 1981, 274 ppGoogle Scholar
Seiler, J. (1920). Geschlechtschrornosomenuntersuchungen an Psychiden. 1. Experimentelle Beein flussung der geschlechtsbestimmenden Reifeteilung bei Talaeporia tubulosa Retz. Archiv für Zellforschung 15, 249–68.Google Scholar
Shapiro, D. Y. (1980). Serial female sex changes after simultaneous removal of males from social groups of a coral reef fish. Scienve 209, 1136–7.CrossRefGoogle ScholarPubMed
Tingley, G. A. (1983). Population dynamics of the entomophilic nematode Romanomermis culicivorax. Ph.D. thesis, University of London.Google Scholar
Welch, H. E. (1960). Hydromermis churchillensis N. sp (Nematoda: Mermithidae) a parasite of Aedes communis (DeG.) from Churchill, Manitoba with observations on its incidence and bionomics. Canadian Journal of Zoology 38, 465–74.CrossRefGoogle Scholar
Welch, H. E. (1965). Entomophilic nematodes. Annual Review of Entomology 10, 275–302.CrossRefGoogle Scholar
Werren, J. H. (1980). Sex ratio adaptations to local mate competition in a parasitic wasp. Science 208, 1157–9.CrossRefGoogle Scholar