Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-22T23:31:12.433Z Has data issue: false hasContentIssue false
  • English
  • Français

The evolution of tissue migration by parasitic nematode larvae

Published online by Cambridge University Press:  06 April 2009

A. F. Read  and
A. Sharping
A. F. Read
Affiliation:
Department of Ecology/Zoology, Institute of Biology and Geology, University of Tromso, Tromso N-9037, Norway Institute of Cell, Animal and Population Biology, University of Edinburgh, Edinburgh EH9 3JT, UK
A. Sharping
Affiliation:
Department of Ecology/Zoology, Institute of Biology and Geology, University of Tromso, Tromso N-9037, Norway
Get access Rights & Permissions [Opens in a new window]

Summary

Migration by nematode larvae through the tissues of their mammalian hosts can cause considerable pathology, and yet the evolutionary factors responsible for this migratory behaviour are poorly understood. The behaviour is particularly paradoxical in genera such as Ascaris and Strongylus in which larvae undergo extensive migrations which begin and end in the same location. The orthodox explanation for this apparently pointless behaviour is that a tissue phase is a developmental requirement following the evolutionary loss of skin penetration or intermediate hosts. Yet tissue migration is not always necessary for development, and navigation and survival in an array of different habitats must require costly biochemical and morphological adaptations. Migrating larvae also risk becoming lost or killed by the host. Natural selection should therefore remove such behaviour unless there are compensating benefits. Here we propose that migration is a selectively advantageous life-history strategy. We show that taxa exploiting tissue habitats during development are, on average, bigger than their closest relatives that develop wholly in the gastrointestinal tract. Time to reproduction is the same, indicating that worms with a tissue phase during development grow faster. This previously unsuspected association between juvenile habitat and size is independent of any effects of adult habitat, life-cycle, or host size, generation time or diet. Because fecundity is intimately linked with size in nematodes, this provides an explanation for the maintenance of tissue migration by natural selection, analogous to the pre-spawning migrations of salmon.

Keywords

larval migranslife-historynatural selectionnematode larvaetissue phase
Type
Research Article
Information
Parasitology , Volume 111 , Issue 3 , September 1995 , pp. 359 - 371
Copyright
Copyright © Cambridge University Press 1995

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

Adamson, M. L. (1986). Modes of transmission and evolution of life histories in zooparasitic nematodes. Canadian Journal of Zoology 64, 1375–84.CrossRefGoogle Scholar
Akahane, H. & Mako, T. (1986). Studies on the life cycle of Gnathostoma hispidium Fedtschenko, 1872. (2) The experimental infection of a pig with early third-stage larvae from loaches. Japanese Journal of Parasitology 35, 161–4.Google Scholar
Altaif, K. I. & Dargie, J. D. (1978). Genetic resistance to helminths. The influence of breed and haemoglobin type on the response of sheep to primary infections with Haemonchus contortus. Parasitology 77, 161–75.CrossRefGoogle ScholarPubMed
Andersen, S., Jorgensen, R. J., Nansen, P. & Nielsen, K. (1973). Experimental Ascaris suum infection in piglets. Acta Pathohgica et Microbiologica Scandinavica 81, 650–6.Google ScholarPubMed
Anderson, R. C. (1984). The origins of zooparasitic nematodes. Canadian Journal of Zoology 62, 317–28.CrossRefGoogle Scholar
Anderson, R. C. (1988). Nematode transmission patterns. Journal of Parasitology 74, 30–45.CrossRefGoogle ScholarPubMed
Anderson, R. C. (1992). Nematode Parasites of Vertebrates. Their Development and Transmission. Wallingford, UK: CAB International.Google Scholar
Anderson, R. C., Chabaud, A. G. & Willmott, S. (1974–1983). CIH Keys to the Nematode Parasites of Vertebrates. Wallingford, UK: CAB International.Google Scholar
Anderson, R. M. (1993). Epidemiology. In Modern Parasitology. A Textbook of Parasitology (ed. Cox, F. E. G.), pp. 75–116. London: Blackwell Scientific.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1991). Infectious Diseases of Humans. Dynamics and Control. Oxford: Oxford University Press.Google Scholar
Anderson, R. M. & Michel, J. F. (1977). Density-dependent survival in populations of Ostertagia ostertagi. International Journal for Parasitology 7, 321–9.CrossRefGoogle ScholarPubMed
Andrássy, I. (1956). Die Rauminhalts und Gewichtsbestimmung der Fadenwürmer (Nematoden). Acta Zoologica Academiae Scientianim Hungaricae 2, 1–15.Google Scholar
Barger, I. A. & Lejamdre, L. F. (1988). Regulation of Haemonchus contartus populations in sheep: mortality of established worms. International Journal for Parasitology 18, 269–73.CrossRefGoogle Scholar
Barus, V. & Libosvarsky, J. (1984). Phenetic and cladistic relations among genera of family Capillariidae. Folia Parasitologica 31, 227–40.Google Scholar
Beaver, P. C. (1969). The nature of visceral larval migrans. Journal of Parasitology 55, 3–12.CrossRefGoogle Scholar
Begon, M., Harper, J. L. & Townsend, C. R. (1990). Ecology. Individuals, Populations and Communities. Oxford: Blackwell Scientific.Google Scholar
Behnke, J. M. (1990). Laboratory animal models. In Hookworm Disease: Current Status and Nero Directions (ed. Schad, G. A. & Warren, K. S.), pp. 105–128. London: Taylor & Francis.Google Scholar
Behnke, J. M., Barnard, C. J. & Wakelin, D. (1992). Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.CrossRefGoogle ScholarPubMed
Blueweiss, L., Fox, H., Kudzma, V., Nakashima, D., Peters, R. H. & Sams, S. (1978). Relationships between body size and some life history parameters. Oecologia 37, 257–72.CrossRefGoogle ScholarPubMed
Burt, A. (1989). Comparative methods using phylogenetically independent contrasts. Oxford Surveys in Evolutionary Biology 6, 33–53.Google Scholar
Butterworth, E. W. & Beverley-Burton, M. (1980). The taxonomy of Capillaria spp. (Nematoda: Trichuroidea) in carnivorous mammals from Ontario, Canada. Systematic Parasitology 1, 211–36.CrossRefGoogle Scholar
Castro, G. A. (1990). Intestinal pathology. In Parasites: Immunity and Pathology. The Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), pp. 283–316. London: Taylor & Francis.Google Scholar
Chappell, L. H. (1993). Physiology and nutrition. In Modern Parasitology (ed. Cox, F. E. G.), pp. 157–192. London: Blackwell Scientific.CrossRefGoogle Scholar
Charlesworth, B. (1980). Evolution in Age-Structured Populations. Cambridge: Cambridge University Press.Google Scholar
Clayton, H. M. & Duncan, J. L. (1977). Experimental Parascaris equorum infection in foals. Research in Veterinary Science 23, 109–14.CrossRefGoogle ScholarPubMed
Coles, G. C. (1985). Allergy and immunopathology of ascariasis. In Ascariasis and its Public Health Significance (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.), pp. 167–84. London: Taylor & Francis.Google Scholar
Cox, F. E. G. (1993). Immunology. In Modern Parasitology (ed. Cox, F. E. G.), pp. 193–218. London: Blackwell Scientific.CrossRefGoogle Scholar
Crompton, D. W. T. & Pawlowski, Z. S. (1985). Life history and development of Ascaris Itimbricoides and the persistence of human ascariasis. In Ascariasis and its Public Health Significance (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.), pp. 9–23. London: Taylor & Francis.Google Scholar
Crompton, D. W. T. & Stephenson, L. S. (1990). Hookworm infection, nutritional status and productivity. In Hookworm Disease: Current Status and New Directions (ed. Schad, G. A. & Warren, K. S.), pp. 231–264. London: Taylor & Francis.Google Scholar
Dash, K. M. (1981). Interaction Between Oesophagostomum columbianum and Oesophagostomum venulosum in sheep. International Journal for Parasitology 11, 201–7.CrossRefGoogle ScholarPubMed
Dineen, J. K. & Windon, R. G. (1980). The effect of sire selection on the response of lambs to vaccination with irradiated Trichostrongylus colubriformis larvae. International Journal for Parasitology 10, 189–96.CrossRefGoogle ScholarPubMed
Douson, C. (1974). Studies on the immunity of sheep to Oesophagostomum columbianum: effects of different and successive doses of larvae on worm burdens, worm growth and fecundity. Parasitology 68, 313–22.Google Scholar
Dobson, C., Sitepu, P. & Brindley, P. J. (1985). Influence of primary infection on the population dynamics of Nematospiroides dubius after challenge infections in mice. International Journal for Parasitology 15, 353–9.CrossRefGoogle ScholarPubMed
Durette-Desset, M. -C. (1985). Trichostrongylid nematodes and their vertebrate hosts: reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24, 239–306.CrossRefGoogle Scholar
Felsenstein, J. (1988). Phylogenies and quantitative methods. Annual Review of Ecology and Systematics 19, 445–71.CrossRefGoogle Scholar
Fülleborn, F. (1920). Ueber die Anpassung der Nematoden an den Parasitismus und den Infektionsweg bei Askaris und anderen Fadenwürmern des Menschen. Archiv für Schiffs- und Tropen-Hygiene, Pathologie und Therapie exotischer Krankheiten 24, 340–7.Google Scholar
Fülleborn, F. (1927). Ueber das Verhalten der Larven von Strongyloides stercoralis, Hakenwürmern und Ascaris lumbricoides im Körper des Wirtes und ein Versuch, es biologisch zu denken. Beihefte (2) Archiv für Schiffs- und Tropen-Hygiene, Pathologie und Therapie exotischer Krankheiten 31, 151–202.Google Scholar
Fülleborn, F. (1929). On the larval migration of some parasitic nematodes in the body of the host and its biological significance. Journal of Helminthology 7, 15–26.CrossRefGoogle Scholar
Galvin, T. J. (1968). Development of human and pig Ascaris in the pig and rabbit. Journal of Parasitology 54, 1085–91.CrossRefGoogle Scholar
Goater, C. P. (1992). Experimental population dynamics of Rhabdias bufonis (Nematoda) in toads (Bufo bufo): density dependence in primary infection. Parasitology 104, 179–87.CrossRefGoogle ScholarPubMed
Goldberg, A. (1973). Interaction of Trichostrongylus axei and Haemonchus contortus administered simultaneously to cows. Proceedings of the Helminthological Society of Washington 40, 169–70.Google Scholar
Gregg, P. & Dineen, J. K. (1978). The response of sheep vaccinated with irradiated Trichostrongylus colubriformis larvae to impulse and sequential challenge with normal larvae. Veterinary Parasitology 4, 49–78.CrossRefGoogle Scholar
Harvey, P. H. & Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology. Oxford: Oxford University Press.CrossRefGoogle Scholar
Harvey, P. H., Read, A. F. & Promislow, D. E. L. (1989). Life History Variation in Placental Mammals: Unifying the Data with the Theory. Oxford Surveys in Evolutionary Biology 6, 13–32.Google Scholar
Herlich, H. (1959). Experimental infections of cattle with the stomach worms, Ostertagia ostertagi and Trichostrongylus axei. Proceedings of the Helminthological Society of Washington 26, 97–102.Google Scholar
Imai, J., Akahane, H., Horiuchi, S., Maruyama, H. & Nawa, Y. (1989). Gnathostoma doloresi: development of larvae obtained from snakes, Agkistodon halys, to adult worms in a pig. Japanese Journal of Parasitology 38, 221–5.Google Scholar
Levine, N. D. (1980). Nematode Parasites of Domestic Animals and of Man. Minneapolis: Burgess Publishing Co.Google Scholar
Lichtenfels, J. R. (1979). A conventional approach to a new classification of the Strongyloidea, nematode parasites of mammals. American Zoologist 19, 1185–94.CrossRefGoogle Scholar
Lumley, A. M. & Lee, D. L. (1981). Nippostrongylus brasiliensis and Nematodirus battus: changes in numbers and weight during the course of infection. Experimental Parasitology 52, 183–90.CrossRefGoogle ScholarPubMed
Maddison, W. P. & Maddison, D. R. (1992). MocClade: Analysis of Phylogeny and Character Evolution. Version 3.0, Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Maema, M. M. (1986). Dynamics of repeated infection of high and low responder inbred mice with Heligmosomoides polygyrus. Ph.D. thesis, London University.Google Scholar
Maizels, R. M., Dundy, D. A. P., Selkirk, M. E., Smith, D. F. & Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature, London 365, 797–805.CrossRefGoogle ScholarPubMed
Mansour, T. F. (1979). Chemotherapy of parasitic worms: new biochemical strategies. Science 205, 462–9.CrossRefGoogle ScholarPubMed
Michael, E. & Bundy, D. A. P. (1989). Density-dependence in establishment, growth and worm fecundity in intestinal helminthiasis: the population biology of Trichuris muris (Nematoda) infection in CBA/Ca mice. Parasitology 98, 451–8.CrossRefGoogle ScholarPubMed
Mitter, C., Farrell, D. & Wiegmann, B. (1988). The phylogenetic study of adaptive zones: has phy tophagy promoted diversification? American Naturalist 132, 107–28.CrossRefGoogle Scholar
Moqbel, R. & MacDonald, A. J. (1990). Immunological and inflammatory responses in the small intestine associated with helminthic infections. In Parasites: Immunity and Pathology. Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), pp. 249–282. London: Taylor & Francis.Google Scholar
Moravec, F. (1981). Invalidity of the genus Thominx Dujardin, 1845 (Nematoda: Capillariidae). Folia Parasitologica 28, 104.Google Scholar
Moravec, F. (1982). Proposal of a new systematic arrangement of nematodes in the family Capillariidae. Folia Parasitologica 29, 119–32.Google ScholarPubMed
Moravec, F., Prokopic, J. & Shlikas, A. V. (1987). The biology of the family Capillariidae Neveu-Lemaire 1936. Folia Parasitologica 34, 39–56.Google ScholarPubMed
Muller, R. (1975). Worms and Disease. London: Heinemann.Google Scholar
Murrell, K. D. (1985). Trichinella spiralis: acquired immunity in swine. Experimental Parasitology 59, 347–54.CrossRefGoogle ScholarPubMed
Noble, E. R. & Noble, G. A. (1976). Parasitology. The Biology of Animal Parasites. Philadelphia: Lea & Febiger.Google Scholar
Ogbourne, C. P. & Duncan, J. L.Strongylus vulgaris in the Horse: Its Biology and Veterinary Importance, 2nd edn.Slough: Commonwealth Agricultural Bureaux.Google Scholar
Pagel, M. D. & Harvey, P. U. (1988). Recent developments in the analysis of comparative data. Quarterly Review of Biology 63, 413–40.CrossRefGoogle ScholarPubMed
Quinnell, R. J. & Keymer, A. E. (1990). Acquired immunity and epidemiology. In Parasites: Immunity and Pathology. The Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), pp. 317–337. London: Taylor & Francis.Google Scholar
Read, A. F. (1991). Passerine polygyny: a role for parasites? American Naturalist 138: 434–59.CrossRefGoogle Scholar
Read, A. F. & Harvey, P. H. (1989). Life history differences among the cutherian radiations. Journal of Zoology 219, 329–53.CrossRefGoogle Scholar
Read, C. P. (1970). Parasitism and Symbiology. An Introductory Text. New York: Ronald Press.Google Scholar
Robinson, M., Wahid, F., Behnke, J. M. & Gilbert, F. S. (1989). Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): dose-dependent expulsion of adult worms. Parasitology 98, 115–24.CrossRefGoogle ScholarPubMed
Rothschild, M. & Clay, T. (1952). Fleas, Flukes and Cuckoos. A Study of Bird Parasites. London: Collins.Google Scholar
Rothwell, R. L. W. (1989). Immune expulsion of parasitic nematodes from the alimentary tract. International Journal for Parasitology 19, 139–68.CrossRefGoogle ScholarPubMed
Schmidt, G. D. & Roberts, L. S. (1989). Foundations of Parasitology, 4th edn.Baltimore: Williams & Wilkins.Google Scholar
Sibly, R. M. & Calow, P. (1986). Physiological Ecology of Animals: an Evolutionary Approach. Oxford: Blackwell Scientific.Google Scholar
Sinniah, B. & Subramaniam, K. (1991). Factors influencing the egg production of Ascaris lumbricoides: relationship to weight, length and diameter of worms. Journal of Helminthology 65, 141–7.CrossRefGoogle ScholarPubMed
Skorping, A., Read, A. F. & Keymer, A. E. (1991). Life history covariation in intestinal nematodes of mammals. Oikos 60, 365–72.CrossRefGoogle Scholar
Skrjabin, K. I. (1949–1954). Key to parasitic nematodes. Moscow: Akademiya Nauk SSSR Publishers. (Israel Program for Scientific Translations 1969 and Amerind Publishing, New Delhi 1991).Google Scholar
Skrjabin, K. I. (1953–1971). Essentials of Nematodology Vols. 1–13. Moscow: Akademii Nauk SSSR. (Israel Program for Scientific Translations 1960–71).Google Scholar
Smyth, J. D. (1994). Introduction to Animal Parasitology, 3rd edn.Cambridge: Cambridge University Press.Google Scholar
Soulsby, E. J. L. (1968). Helminths, Arthropods and Protozoa of Domesticated Animals. London: Baillière, Tindall & Cassell Ltd.Google Scholar
Southwood, T. R. E. (1977). Habitat, the templet for ecological strategies? Journal of Animal Ecology 46, 337–65.CrossRefGoogle Scholar
Sprent, J. F. A. (1954). The life cycles of nematodes in the family Ascarididae Blanchard 1896. Journal of Parasitology 40, 608–17.CrossRefGoogle ScholarPubMed
Sprent, J. F. A. (1962). The evolution of the Ascaridoidea. Journal of Parasitology 48, 818–24.CrossRefGoogle ScholarPubMed
Stearns, S. C. (1992). Evolution of Life Histories. Oxford: Oxford University Press.Google Scholar
Szalai, A. J. & Dick, T. A. (1989). Differences in numbers and inequalities in mass and fecundity during the egg-producing period for Raphidascaris acus (Nematoda: Anisakidae). Parasitology 98, 489–95.CrossRefGoogle Scholar
Tilens, A. G. M. (1994). Energy generation in parasitic helminths. Parasitology Today 10, 346–52.CrossRefGoogle Scholar
Tromba, F. G. (1978). Immunization of pigs against experimental Ascaris suum infection by feeding ultraviolet-attenuated eggs. Journal of Parasitology 64, 651–6.CrossRefGoogle ScholarPubMed
Urquhart, G. M., Armour, J., Duncan, J. L., Dunn, A. M. & Jennings, F. W. (1987). Veterinary Parasitology. Harlow: Longman Scientific & Technical.Google Scholar
Vercruysse, J., Taraschewski, H. & Voight, W. P. (1988). Main clinical and pathological signs of parasitic infection in domestic animals. In Parasitology in Focus, Facts and Trends (ed. Mehlhorn, H.), pp. 477–539. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Wakelin, D. (1973). The stimulation of immunity to Trichuris muris in mice exposed to low level infections. Parasitology 66, 181–9.CrossRefGoogle ScholarPubMed
Wakelin, D. (1975 a). Genetic control of immune responses to parasites: immunity to Trichuris muris in inbred and random-bred mice. Parasitology 71, 51–60.CrossRefGoogle Scholar
Wakelin, D. (1975 b). Genetic control of immune responses to parasites: selection for responsiveness and non-responsiveness to Trichuris muris in randombred mice. Parasitology 71, 377–84.CrossRefGoogle Scholar
Wenceslao-Ollague, L., Eduardo-Gomez, L., Manuel-Briones, I., Ollague, L. W., Gomez, L. E. & Briones, I. M. (1988). Experimental infection of an adult domestic cat with third-stage larvae of Gnathostoma spinigerum from a freshwater fish. Medicina Cutanea Ibero Latino Americana 16, 295–7.Google Scholar
Wilson, R. A. (1990). Pulmonary immune responses to parasites. In Parasites: Immunity and Pathology. The Consequences of Parasitic Infection in Mammals (ed. Behnke, J. M.), pp. 208–248. London: Taylor & Francis.Google Scholar