Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T16:54:34.018Z Has data issue: false hasContentIssue false

Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala

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

In Guatemalan villages people commonly rear pigs, and both hosts may be infected with Ascaris. This study was designed to ask whether both humans and pigs are potential hosts in a single parasite transmission cycle in such villages, or alternatively, if there are two separate transmission cycles, one involving pigs and one involving human hosts. Parasites were collected from both host species from locations in the north and south of Guatemala. Allelic variation in the nuclear genome of Ascaris was measured using enzyme electrophoresis, while mitochondrial DNA (mtDNA) sequence variation was quantified using restriction mapping. Low levels of enzyme polymorphism were found in Ascaris, but allele frequencies at two loci, mannose phosphate isomerase and esterase, suggest that there is little gene exchange between parasite populations from humans and pigs. MtDNA haplotypes fall into two distinct clusters which differ in sequence by 3–4%; the two clusters broadly correspond to worms collected from humans and those collected from pigs. However, some parasites collected from humans have mtDNA characteristic of the ‘pig Ascaris’ haplotype cluster, while some parasites collected from pigs have mtDNA characteristic of the ’ haplotype cluster. These shared haplotypes are unlikely to represent contemporary cross-infection events. Patterns of phylogenetic similarity and geographical distribution of these haplotypes suggest, instead, that they are the result of two historical introgressions of mtDNA between the two host-associated Ascaris populations. The results clearly demonstrate that Ascaris from humans and pigs are involved in separate transmission cycles in Guatemala.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Aguilar, F. J. (1991). Parasitologia Medica, 2nd Edn.Guatemala City: Litografia Delgado, S.A.Google Scholar
Anderson, R. M. (1989). Transmission dynamics of Ascaris lumbricoides and the impact of chemotherapy. In Ascariasis and its Prevention and Control, (ed. Crompton, D. W. T., Nesheim, M. C. & Pawlowski, Z. S.) pp. 253273. London, New York and Philadelphia: Taylor and Francis.Google Scholar
Anderson, R. M. & May, R. M. (1985). Helminth infections of humans: mathematical models, population dynamics, and control. Advances in Parasitology 24, 199.Google Scholar
Anderson, R. M. & Medley, G. F. (1985). Community control of helminth infections of man by mass and selective chemotherapy. Parasitology 90, 629–60.CrossRefGoogle Scholar
Anderson, T. J. C., Zizza, C. A., Leche, G. M., Scott, M. E. & Solomons, N. W. (1993). The distribution of intestinal helminths in a rural village in Guatemala. Memorias do Instituto Oswaldo Cruz (in the Press).CrossRefGoogle Scholar
Ansel, M. & Thibaut, M. (1973). Value of specific distinction between Ascaris lumbricoides Linne, 1758 and Ascaris suum Goeze, 1782. International Journal for Parasitology 3, 317–19.CrossRefGoogle ScholarPubMed
Arnold, M. L. (1992). Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics 23, 237–61.CrossRefGoogle Scholar
Arnold, M. L., Robinson, J. J., Buckner, C. M. & Bennet, B. D. (1992). Pollen dispersal and interspecific gene flow in Louisiana irises. Heredity 68, 399404.CrossRefGoogle Scholar
Baverstock, P. R., Adams, M. & Beveridge, I. (1985). Biochemical differentiation in bile duct cestodes and their marsupial hosts. Molecular Biology and Evolution 2, 321–37.Google ScholarPubMed
Birky, C. W. Jr, Maruyama, T. & Fuerst, P. (1983). An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513–27.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
Brooks, D. R. & McLennan, D. A. (1991). Phylogeny, Ecology and Behaviour: a Research Program in Comparative Biology. Chicago: University of Chicago Press.Google Scholar
Brown, W. M. (1985). The mitochondrial genome of animals. In Molecular Evolutionary Genetics, (ed. McIntyre, R. J.) pp. 95130. New York: Plenum Press.Google Scholar
Bundy, D. A. P. (1988). Population ecology of intestinal helminth infections in human communities. Philosophical Transactions of the Royal Society, London, Series B 321, 405–20.Google Scholar
Bullini, L., Nascetti, G., Paggi, L., Orecchia, P., Mattiucci, S. & Berland, B. (1986). Genetic variation of Ascaridoid worms with different lifecycles. Evolution 40, 437–40.CrossRefGoogle Scholar
Cann, R. L., Stoneking, M. & Wilson, A. C. (1987). Mitochondrial DNA and human evolution. Nature, London 325, 31–6.CrossRefGoogle ScholarPubMed
De Boer, E. (1935). Experimenteel onderzoek betreffende Ascaris lumbricoides van mensch en varken. Tijdscrift voor Diergeneeskunde 62, 673–95.Google Scholar
De Buron, I., Renaud, F. & Euzet, L. (1986). Speciation and specificity of acanthocephalans. Genetic and morphological studies of Acanthocephalloides geneticus sp. nov. parasitizing Arnoglossus laterna (Bothidae) from the Mediterranean littoral (Sete-France). Parasitology 92, 165–71.CrossRefGoogle Scholar
Dorado, O., Reiseberg, L. H. & Arias, D. M. (1992). Chloroplast DNA introgression in Southern California sunflowers. Evolution 46, 566–72.Google Scholar
Efron, B. (1982). The Jackknife, the Bootstrap, and other Resampling Plans. Philadelphia, Pennsylvania: Society for Industrial and Applied Mathematics.CrossRefGoogle Scholar
Farris, J. S., Kluge, A. G. & Eckardt, M. J. (1970). A numerical approach to phylogenetic systematics. Systematic Zoology 19, 172–91.Google Scholar
Feder, J. L., Chilcote, C. A. & Bush, G. L. (1990). The geographical pattern of genetic differentiation between host-associated populations of Rhagoletis pomonella (Diptera: Tephritidae) in the eastern United States and Canada. Evolution 44, 595608.Google Scholar
Ferris, S. D., Sage, B. D., Huang, C-M., Nielsen, J. T., Ritte, U. & Wilson, A. C. (1983). Flow of mitochondrial DNA across a species boundary. Proceedings of the National Academy of Sciences, USA 80, 2290–4.Google Scholar
Flockhart, H. A., Cibulskis, R., Karam, M. & Albiez, E. J. (1986). Onchocerca volvulus: enzyme polymorphism in relation to differentiation of forest and savannah strains of the parasite. Transactions of the Royal Society of Tropical Medicine and Hygiene 80, 285–92.Google Scholar
Galvin, T. J. (1968). Development of human and pig Ascaris in the pig and the rabbit. Journal of Parasitology 54, 1085–91.CrossRefGoogle ScholarPubMed
Guyatt, H. L., Bundy, D. A. P., Medley, G. F. & Grenfell, B. T. (1990). The relationship between the frequency distribution of Ascaris lumbricoides and the prevalence and intensity of infection in human communities. Parasitology 101, 139–45.CrossRefGoogle ScholarPubMed
Gyllensten, U. & Wilson, A. C. (1987). Interspecific mitochondrial DNA transfer and the colonization of Scandanavia by mice. Genetical Research 49, 25–9.Google Scholar
Hartl, D. L. & Clark, A. G. (1989). Principles of Population Genetics. Sunderland, Massachusetts: Sinauer Associates, Inc.Google Scholar
Hawley, J. H. & Peanaskey, R. J. (1992). Ascaris suum: are trypsin inhibitors involved in species specificity of ascarid nematodes? Experimental Parasitology 75, 112–18.CrossRefGoogle ScholarPubMed
He, L., Min, X. T., Liu, G. Z., Xu, P. & Li, W. (1986). Preliminary karyotype studies on Ascaris lumbricoides and Ascaris suum from Guangzhon. Journal of Parasitology and Parasitic Diseases 4, 206–8.Google Scholar
Hyman, B. C. (1988). Nematode mitochondrial DNA: anomalies and application. Journal of Nematology 20, 523–31.Google Scholar
Jaenike, J. (1993). Rapid evolution of host specificity in a parasitic nematode. Evolutionary Ecology 7, 103–8.Google Scholar
Kennedy, M. W., Qureshi, F., Haswell-Elkins, M. & Elkins, D. B. (1987). Homology and heterology between the secreted antigens of the parasitic larval stages of Ascaris lumbricoides and Ascaris suum. Clinical and Experimental Immunology 67, 2030.Google Scholar
Kofie, B. A. K. & Dipeolu, O. O. (1983). A study of human and porcine Ascariasis in a rural area of South-West Nigeria. International Journal of Zoonoses 10, 6670.Google Scholar
Kurimoto, H. (1974). Morphological, biochemical and immunological studies on the differences between Ascaris lumbricoides Linnaeus, 1758 and Ascaris suum Goeze, 1782. Japanese Journal of Parasitology 23, 251–67.Google Scholar
La Rosa, G., Pozio, E., Rossi, P. & Murrell, K. D. (1992). Allozyme analysis of Trichinella isolates from various host species and geographical regions. Journal of Parasitology 78, 641–6.Google Scholar
Lehman, N., Eisenhawer, A., Hansen, K., Mech, L. D., Peterson, R. O., Gogan, P. J. P. & Wayne, R. K. (1991). Introgression of Coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45, 104–19.CrossRefGoogle ScholarPubMed
Leslie, J. F., Cain, G. D., Meffe, G. K. & Vrijenhoek, R. C. (1980). Enzyme polymorphism in Ascaris suum (Nematoda). Journal of Parasitology 68, 576–87.CrossRefGoogle Scholar
Lewontin, R. C. & Hubby, J. (1966). A molecular approach to the study of genetic heterozygosity in natural populations. II. Amounts of variation and degree of heterozygosity in natural populations of Drosophila pseudobscura. Genetics 54, 595609.CrossRefGoogle Scholar
Lively, C. M. (1989). Adaptation by a parasite trematode to local populations of its snail host. Evolution 43, 1663–71.Google Scholar
Lord, W. D. & Bullock, W. L. (1982) Swine Ascaris in humans. New England Journal of Medicine 306, 1113.Google ScholarPubMed
Lydeard, C., Mulvey, M., Aho, J. M. & Kennedy, P. K. (1989). Genetic variability among natural populations of the liver fluke Fascioloides magna in the white-tailed deer, Odocoileus virginianus. Canadian Journal of Zoology 67, 2021–5.CrossRefGoogle Scholar
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.Google Scholar
Lynch, M. & Crease, T. J. (1990). The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution 7, 377–94.Google Scholar
Lysek, H. (1963). Contribution to the morphological problem of differences between Ascaris lumbricoides Linne, 1758 and Ascaris suum Goeze, 1782. Acta Societatis Zoologicae Bohemoslovenicae 27, 97101.Google Scholar
Malynicz, G. L. (1977). A demographic analysis of highlands village pig production. In Tenth Waigani Seminar on Agriculture in the Tropics, (ed. Enyi, B. A. C. & Varghese, T.) pp. 201209. Papua New Guinea University of Technology: Lae, Papua New Guinea.Google Scholar
Maung, M. (1973). Ascaris lumbricoides Linne, 1758 and Ascaris suum Goeze, 1782: morphological differences between specimens obtained from man and pig. South-East Asia Journal of Tropical Medicine and Public Health 4, 41–5.Google Scholar
Mayr, E. (1969). Animal Species and Evolution. Cambridge, Massachusetts: Belknap Press of Harvard University Press.Google Scholar
Miller, J. C. (1991). RESTSITE: a phylogenetic program that sorts raw restriction site data. Journal of Heredity 82, 262–3.Google Scholar
Mutafova, T. (1983). Comparative caryological studies of Ascaris lumbricoides and Ascaris suum. Helminthologia 15, 4856.Google Scholar
Nadler, S. A. (1987). Biochemical and immunological systematics of some ascaridoid nematodes: genetic divergence between congeners. Journal of Parasitology 73, 811–16.CrossRefGoogle ScholarPubMed
Nascetti, G., Grapelli, C. & Bullini, L. (1979). Ricerche sul differenziamento di Ascaris lumbricoides e Ascaris suum. Rendiconti delle Sedute della Accademia Nazionale dei Lincei, Classe di Scienze Fisiche, Matematiche e Naturali LXVII, 457465.Google Scholar
Nevo, E. (1978). Genetic variation in natural populations: patterns and theory. Theoretical Population Biology 13, 121–77.Google Scholar
Nickrent, D. L. & Stell, A. L. (1990). Electrophoretic evidence for differentiation in two host races of Hemlock Dwarf Mistletoe (Arceuthobium tsugense) Biochemical Systematics 18, 267–80.CrossRefGoogle Scholar
Okimoto, R., Macfarlane, J. L., Clary, D. O. & Wolstenholme, D. R. (1992). The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471–98.Google Scholar
Pasteur, N., Pasteur, G., Bonhomme, F., Catalan, J. & Britton-Davidian, J. (1988). Practical Isozyme Genetics. Chichister: Ellis Horwood Ltd.Google Scholar
Powell, J. R. (1983). Interspecific cytoplasmic gene flow in the absence of nuclear gene flow; Evidence from Drosophila. Proceedings of the National Academy of Sciences, USA 80, 492–5.Google Scholar
Powers, T. O., Platzer, E. G. & Hyman, B. C. (1986). Species specific restriction site polymorphism in root-knot nematode mitochondrial DNA. Journal of Nematology 18, 288–93.Google ScholarPubMed
Rogers, M. R., Popper, S. J. & Wirth, D. F. (1990). Amplification of kinetoplast DNA as a tool in the detection and diagnosis of Leishmania. Experimental Parasitology 71, 267–75.Google Scholar
Rollinson, D., Imbert Establet, D. & Ross, G. C. (1986). Schistosoma mansoni from naturally infected Rattus rattus in Guadeloupe; identification, prevalence and enzyme polymorphism. Parasitology 93, 3953.Google Scholar
Saitou, N. & Nei, M. (1987). The neighbour-joining method; a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–25.Google Scholar
Sarti, E., Schantz, P. M., Placarte, A., Wilson, M., Gutierrez, I. O., Lopez, A. S., Roberts, J. & Flisser, A. (1992). Prevalence and risk factors for Taenia solium taeniasis and cysticercosis in humans and pigs in a village in Morelos, Mexico. American Journal of Tropical Medicine and Hygiene 46, 677–85.Google Scholar
Selander, R. L., Caugant, D. A., Ochman, H., Musser, J. M., Gilmour, M. N. & Whittam, T. S. (1986). Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Applied Environmental Microbiology 51, 873–84.Google Scholar
Shoemaker-Nawas, P., Frost, F., Kobayashi, J. & Jones, P. (1982). Ascaris infection in Washington. Western Journal of Medicine 136, 436–7.Google Scholar
Simpson, L. (1987). The mitochondrial genome of kinetoplastid protozoa; genomic organization, transcription, replication and evolution. Annual Review of Microbiology 41, 363–82.Google Scholar
Sokal, R. R. & Rohlf, F. J. (1981). Biometry. San Francisco; W. H. Freeman and Company.Google Scholar
Sprent, J. F. A. (1952). Anatomical distinction between human and pig strains of Ascaris. Nature, London 170, 627–8.Google Scholar
Swofford, D. L. (1991). PAUP: Phylogenetic Analysis Using Parsimony, Version 3.0 s. Computer program distributed by the Illinois Natural History Survey, Champaign. Illinois.Google Scholar
Takata, I. (1951). Experimental infection of man with Ascaris of man and the pig. Kitasato Archives of Experimental Medicine 23, 4959.Google ScholarPubMed
Viney, M. E. & Ashford, R. W. (1990). The use of isozyme electrophoresis in the taxonomy of Strongyloides. Annals of Tropical Medicine and Parasitology 84, 3547.CrossRefGoogle ScholarPubMed
Vrijenhoek, R. C. (1978). Genetic differentiation among larval nematodes infecting fishes. Journal of Parasitology 64, 790–8.CrossRefGoogle Scholar
Waring, G. L., Abrahamson, W. G. & Howard, D. J. (1990). Genetic differentiation among host associated populations of the gallmaker Eurosta solidaginis (Diptera: Tethritidae). Evolution 44, 1648–55.Google Scholar
Wolstenholme, D. R., Macfarlane, J. L., Okimoto, B., Clary, D. O. & Wahleithner, J. A. (1987). Bizarre tRNAs inferred from DNA sequences of mitochondrial genomes of nematode worms. Proceedings of the National Academy of Sciences, USA 84, 1324–8.Google Scholar
Woodruff, D. S., Merenlender, A. M., Upatham, E. S. & Viyanant, (1986). Genetic variation and differentiation of three schistosome species form the Philippines, Laos and Peninsular Malaysia. American Journal of Tropical Medicine and Hygiene 36, 345–54.CrossRefGoogle Scholar
Yadav, A. K. & Tandon, V. (1989). Nematode parasite infections of domestic pigs in a sub-tropical and high-rainfall area of India. Veterinary Parasitology 31, 133–9.Google Scholar
Zhong-Jin, L., Ling, W., Qing, L., Guang-Zhao, T., Ziao-Su, H., Guang-Qui, H., Fang, Q. & Rui-Tu, R. (1987). Comparative study of amino acid contents and LDH isozyme by electrophoresis and slab-page in adult worms of Ascaris lumbricoides, Ascaris suum and Toxocara canis. Chinese Medical Journal 100, 740–4.Google Scholar
Zouros, E., Freeman, K. R., Ball, A. O. & Pogson, G. H. (1992). Direct evidence for extensive paternal mitochondrial DNA inheritance in the marine muscle Mytilus. Nature, London 359, 412–14.Google Scholar