Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-23T10:49:56.873Z Has data issue: false hasContentIssue false

Mitochondrial DNA and Ascaris microepidemiology: the composition of parasite populations from individual hosts, families and villages

Published online by Cambridge University Press:  06 April 2009

T. J. C. Anderson
Affiliation:
Department of Biology, University of Rochester, Rochester, NY 14627, USA Center for Studies of Sensory Impairment, Aging and Metabolism (CeSSIAM), Hospital de Ojos y Oidos, ‘Dr Rodolfo Robles V’, Diagonal 21 y 19 Calle, Guatemala City, Guatemala
M. E. Romero-Abal
Affiliation:
Center for Studies of Sensory Impairment, Aging and Metabolism (CeSSIAM), Hospital de Ojos y Oidos, ‘Dr Rodolfo Robles V’, Diagonal 21 y 19 Calle, Guatemala City, Guatemala
J. Jaenike
Affiliation:
Department of Biology, University of Rochester, Rochester, NY 14627, USA

Summary

Patterns of genetic subdivision in parasite populations can provide important insights into transmission processes and complement information obtained using traditional epidemiological techniques. We describe mitochondrial sequence variation in 265 Ascaris collected from 62 individual hosts (humans and pigs) from 35 households in 3 Guatemalan locations. Restriction mapping of individual worms revealed 42 distinct mitochondrial genotypes. We ask whether the mitochondrial genotypes found in worms from individual hosts, from families of hosts and from villages represent random samples from the total Ascaris population. Patterns of genetic subdivision were quantified using F-statistics, while deviations from the null hypothesis of randomness were evaluated by a simple resampling procedure. The analysis revealed significant deviations from panmixia. Parasite populations were strongly structured at the level of the individual host in both humans and pigs: parasites bearing the same mitochondrial genotype were found more frequently than would be expected by chance within hosts. Significant heterogeneity was also observed among populations from different villages, but not from different families within a village. The clustering of related parasites within hosts suggests a similar clustering of related infective stages in the environment and may explain why sex ratios in Ascaris are female-biased. We discuss aspects of Ascaris biology which may lead to the observed patterns.

Type
Research Article
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

Anders, R. F. & Smyth, J. A. (1989). Polymorphic antigens in Plasmodium falciparum. Blood 74, 1865–75CrossRefGoogle ScholarPubMed
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 199.CrossRefGoogle ScholarPubMed
Anderson, T. J. C. (1994). The population genetics, epidemiology and evolution of the parasitic nematode Ascaris. Ph.D. thesis, University of Rochester.Google Scholar
Anderson, T. J. C., Romero-Abal, E. & Jaenike, J. (1993 a). Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107, 319–34.CrossRefGoogle ScholarPubMed
Anderson, T. J. C., Zizza, C. A., Leche, G. M., Scott, M. E. & Solomons, N. W. (1993 b). The distribution of intestinal helminths in a rural village in Guatemala. Memorias do Institute Oswaldo Cruz 88, 5365.CrossRefGoogle Scholar
Avise, J. C. & Felley, J. (1979). Population structure of freshwater fishes. I. Genetic variation of Bluegill (Lepomis macrochirus) populations in man-made reservoirs. Evolution 33, 1526.Google ScholarPubMed
Berry, A. J. & Kreitman, M. (1993). Molecular analysis of an allozyme cline: alcohol dehydrogenase in Drosophila melanogaster on the East Coast of North America. Genetics 134, 869–93.CrossRefGoogle ScholarPubMed
Blouin, M. S., Dame, J. B., Tarrant, C. A. & Courtney, C. H. (1992). Unusual population genetics of a parasitic nematode: mtDNA variation within and between populations. Evolution 46, 470–6.CrossRefGoogle Scholar
Caugant, D. A., Froholm, L. O., Bovre, K., Holten, E., Frasch, C. E., Mocca, L. F., Zollinger, W. D. & Selander, R. K. (1986). Intercontinental spread of a genetically distinctive complex of clones of Neisseria meningitidis causing epidemic disease. Proceedings of the National Academy of Sciences, USA 83, 4927–31.CrossRefGoogle ScholarPubMed
Chakraborty, R. (1980). Gene-diversity analysis in nested subdivided populations. Genetics 96, 721–6.Google Scholar
Crofton, H. D. (1971). A quantitative approach to parasitism. Parasitology 62, 179–94.CrossRefGoogle Scholar
Dobson, A. P. (1985). Inequalities in the individual reproductive success of parasites. Parasitology 92, 675–82.CrossRefGoogle Scholar
Forrester, J. E., Scott, M. E., Bundy, D. A. P. & Golden, M. N. H. (1988). Clustering of Ascaris lumbricoides and Trichuris trichiura infections within households. Transactions of the Royal Society of Hygiene and Tropical Medicine 82, 282–8.CrossRefGoogle ScholarPubMed
Frank, S. A. (1992). Models of plant-pathogen coevolution. Trends in Genetics 8, 213–19.CrossRefGoogle ScholarPubMed
Guyatt, H. L. & Bundy, D. A. P. (1993). Estimation of intestinal nematode prevalence: influence of parasite mating patterns. Parasitology 107, 99106.CrossRefGoogle ScholarPubMed
Hamilton, W. (1967). Extraordinary sex ratios. Science 156, 477–88.CrossRefGoogle ScholarPubMed
Hillis, D. A. & Moritz, C. (1990). Molecular Systematics. Sunderland: Sinauer Associates Inc.Google Scholar
Hoffmann, A. A. & Neilsen, K. M. (1985). The effect of resource subdivision on genetic variation in Drosophila. American Naturalist 125, 421–30.CrossRefGoogle Scholar
Hugall, A., Moritz, C., Stanton, J. & Wolstenholme, D. R. (1994). Low, but structured mitochondrial DNA diversity in root knot nematodes (Meloidogyne). Genetics 106, 903–12.CrossRefGoogle Scholar
Hughes, A. L. (1991). Circumsporozooite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions. Genetics 127, 345–53.CrossRefGoogle ScholarPubMed
Hughes, A. L. (1992). Positive selection and interallelic recombination at the Merozooite Surface Antigen-1 (MSA-1) locus of Plasmodium falciparum. Molecular Biology and Evolution 9, 381–93.Google ScholarPubMed
Jaenike, J. & Selander, R. K. (1979). Ecological generalism in Drosphila falleni: genetic evidence. Evolution 33, 741–8.CrossRefGoogle Scholar
Keith, T. P., Brooks, L. D., Lewontin, R. C., Martinez-cruzado, J. C. & Rigby, D. L. (1985). Nearly identical distributions of xanthine dehydrogenase in two populations of Drosophila pseudoobscura. Molecular Biology and Evolution 2, 206–16.Google ScholarPubMed
Kennedy, M. K. (1989). Genetic control of the immune repertoire in nematode infections. Parasitology Today 5, 316–24.CrossRefGoogle ScholarPubMed
Lymberry, A. J., Thompson, R. C. A. & Hobbs, R. P. (1990). Genetic diversity and genetic differentiation in Echinococcus granulosus (Batsch, 1786) from domestic and sylvatic hosts on the mainland of Australia. Parasitology 101, 283–9.CrossRefGoogle Scholar
Macdonald, W. W. & Ramachandran, C. P. (1965). The influence of the gene fm (filarial susceptibility, Brugia malayi) on the susceptibility of Aedes aegypti to seven strains of Brugia, Wuchereria and Dirofilaria. Annals of Tropical Medicine and Parasitology 59, 6473.CrossRefGoogle ScholarPubMed
Manly, B. F. J. (1985). The Statistics of Natural Selection. New York: Chapman and Hall.Google Scholar
May, R. M. & Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasite and host. Proceedings of the Royal Society of London, B 219, 281313.Google Scholar
Mulvey, M., Aho, J. M., Lydeard, C., Leberg, P. L. & Smith, M. H. (1991). Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution 45, 1628–40.Google ScholarPubMed
Nadler, S. A. (1986). Biochemical polymorphism in Parascaris equorum, Toxocara canis and Toxocara cati. Molecular and Biochemical Parasitology 18, 4554.CrossRefGoogle ScholarPubMed
Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, USA 70, 3321–3.CrossRefGoogle ScholarPubMed
Nei, M. & Chesser, R. K. (1983). Estimation of fixation indices and gene diversities. Annals of Human Genetics 47, 253–9.CrossRefGoogle ScholarPubMed
Ochman, H., Jones, J. S. & Selander, R. K. (1987). Large-scale genetic differentiation at enzyme loci in the land snails Cepaea nemoralis and Cepaea hortensis. Heredity 58, 127–38.CrossRefGoogle ScholarPubMed
Ou, C-Y., Ciesielski, C. A., Myers, G., Bandea, C. I., Luo, C-C., Korber, B. T. M. et al. (1992). Molecular epidemiology of HIV transmission in a dental practice. Science 256, 1165–71.CrossRefGoogle Scholar
Plapp, F. W. (1986). Genetics and biochemistry of insecticide resistance in arthropods: prospects for the future. In Pesticide Resistance: Strategies and Tactics for Management, pp. 7486. Washington, D.C.: National Academy Press.Google Scholar
Price, P. W. (1980). The Evolutionary Biology of Parasites. Princeton: Princeton University Press.Google ScholarPubMed
Read, A. F., Narara, A., Nee, S., Keymer, A. E. & Day, K. P. (1992). Gametocyte sex ratios as indirect measures of outcrossing rates in malaria. Parasitology 104, 387–95.CrossRefGoogle ScholarPubMed
Rhodes, O. L., Smith, L. M. & Chesser, R. K. (1993). Temporal components of genetic variation in migrating and wintering wigeon. Canadian Journal of Zoology 71, 2229–35.CrossRefGoogle Scholar
Shostak, A. W. & Dick, T. A. (1987). Individual variability in reproductive success of Triaenophorus crassus Forel (Cestoda: Pseudophyllidea), with comments on use of the Lorez curve and Gini coefficient. Canadian Journal of Zoology 63, 2343–51.CrossRefGoogle Scholar
Taylor, H. R., Siler, J. A., Harran, A., Mkocha, B. M. & West, S. (1992). The natural history of endemic trachoma: a longitudinal study. American Journal of Tropical Medicine and Hygiene 46, 552–9.CrossRefGoogle ScholarPubMed
Thompson, J. N. & Burdon, J. J. (1992). Gene-for-gcne coevolution between plants and parasites. Nature, London 360, 121–5.CrossRefGoogle Scholar
Wakelin, D. & Blackwell, J. M. (1988). Genetics of Resistance to Bacterial and Parasitic Infections. London, Philadelphia, New York: Taylor and Francis.Google Scholar
Watterson, G. A. (1978). The homozygosity test of neutrality. Genetics 88, 405–17.CrossRefGoogle ScholarPubMed
Werren, J. H. (1983). Sex ratio competition under local mate competition in a parasitic wasp. Evolution 37, 116–24.CrossRefGoogle Scholar
Williams, D., Burke, G. & Hendley, J. O. (1974). Ascariasis: a family disease. Journal of Pedriatrics 84, 853–4.CrossRefGoogle ScholarPubMed
Wright, S. (1943). Isolation by distance. Genetics 28, 114–38.CrossRefGoogle ScholarPubMed