Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-14T11:15:16.676Z Has data issue: false hasContentIssue false
  • English
  • Français

Population genetics of the bovine/cattle lungworm (Dictyocaulus viviparus) based on mtDNA and AFLP marker techniques

Published online by Cambridge University Press:  06 March 2006

J. HÖGLUND ,
D. A. MORRISON ,
J. G. MATTSSON  and
A. ENGSTRÖM
J. HÖGLUND
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, 751 89 Uppsala, Sweden
D. A. MORRISON
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, 751 89 Uppsala, Sweden
J. G. MATTSSON
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, 751 89 Uppsala, Sweden
A. ENGSTRÖM
Affiliation:
Department of Parasitology (SWEPAR), National Veterinary Institute and Swedish University of Agricultural Sciences, 751 89 Uppsala, Sweden
Get access Rights & Permissions [Opens in a new window]

Abstract

Mitochondrial DNA (mtDNA) sequence data and amplified fragment length polymorphism (AFLP) patterns were compared for the lungworm Dictyocaulus viviparus, a nematode parasite of cattle. Eight individual D. viviparus samples from each of 8 herds in Sweden and 1 laboratory isolate were analysed, with the aim of describing the diversity and genetic structure in populations using different genetic markers on exactly the same DNA samplesNucleotide sequence data reported in this paper have been submitted to GenBank under the Accession numbers DQ299539-DQ299826.. There was qualitative agreement between the whole-genome AFLP data and the mtDNA sequence data, both indicating relatively strong genetic differentiation among the Swedish farms. However, the AFLP data detected much more genetic variation than did the mtDNA data, even after allowing for the different inheritance patterns of the markers, and indicated that there was much less differentiation among the populations. The mtDNA data therefore seemed to be more informative about the most recent history of the parasite populations, as the general patterns were less obscured by detailed inter-relationships among individual worms. The 4 mtDNA genes sequenced (1542 bp) showed consistent patterns, although there was more genetic variation in the protein-coding genes than in the structural RNA genes. Furthermore, there appeared to be at least 3 distinct genetic groups of D. viviparus infecting Swedish cattle, 1 of which was predominant and showed considerable differentiation between farms, but not necessarily within farms. Second, the 2 smaller genetic groups occurred on farms where the predominant group also occurred, suggesting that these farms have had multiple introductions of D. viviparus.

Keywords

Strongylidagenotypespopulation genetic analysisgene flowgenetic structureruminants
Type
Research Article
Information
Parasitology , Volume 133 , Issue 1 , July 2006 , pp. 89 - 99
Copyright
2006 Cambridge University Press

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

Abu-Madi, M. A., Mohd-Zain, S. N., Lewis, J. W. and Reid, A. P. ( 2000). Genomic variability within laboratory and wild isolates of the trichostrongyle mouse nematode Heligmosomoides polygyrus. Journal of Helminthology 74, 195–201.Google Scholar
Anderson, T. J. ( 2001). The dangers of using single locus markers in parasite epidemiology: Ascaris as a case study. Trends in Parasitology 17, 183–188.CrossRefGoogle Scholar
Anderson, T. J., Romero-Abal, M. E. and Jaenike, J. ( 2003). Genetic structure and epidemiology of Ascaris populations: patterns of host affiliation in Guatemala. Parasitology 107, 319–334.Google Scholar
Avise, J. C., Walker, D. and Johns, G. C. ( 1998). Speciation durations and Pleistocene effects on vertebrate phylogeography. Proceedings of the Royal Society of London, B 265, 1707–1712.CrossRefGoogle Scholar
Birky, C. W. Jr, Maruyama, T. and Fuerst, P. ( 1983). An approach to population and evolutionary genetic theory for genes in mitochondria and chloroplasts, and some results. Genetics 103, 513–527.Google Scholar
Blouin, M. S. ( 1998). Mitochondrial DNA diversity in nematodes. Journal of Helminthology 72, 285–289.CrossRefGoogle Scholar
Blouin, M. S. ( 2002). Molecular prospecting for cryptic species of nematodes: mitochondrial DNA versus internal transcribed spacer. International Journal for Parasitology 32, 527–531.CrossRefGoogle Scholar
Blouin, M. S., Liu, J. and Berry, R. E. ( 1999). Life cycle variation and the genetic structure of nematode populations. Heredity 83, 253–259.CrossRefGoogle Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. ( 1995). Host movement and the genetic structure of populations of parasitic nematodes. Genetics 141, 1007–1014.Google Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. ( 1997). Haemonchus placei and Haemonchus contortus are distinct species based on mtDNA evidence. International Journal for Parasitology 27, 1383–1387.CrossRefGoogle Scholar
Blouin, M. S., Yowell, C. A., Courtney, C. H. and Dame, J. B. ( 1998). Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Molecular Biology and Evolution 15, 1719–1727.CrossRefGoogle Scholar
Borgsteede, F. H. M., Hendriks, J. and Leeuw, W. A. ( 1994). Winter survival of Dictyocaulus viviparus in the Netherlands. Helminthologia 31, 9–15.Google Scholar
Braisher, T. L., Gemmell, N. J., Grenfell, B. T. and Amos, W. ( 2004). Host isolation and patterns of genetic variability in three populations of Teladorsagia from sheep. International Journal for Parasitology 34, 1197–1204.CrossRefGoogle Scholar
Brant, S. V. and Orti, G. ( 2003). Evidence for gene flow in parasitic nematodes between two host species of shrews. Molecular Ecology 12, 2853–2859.CrossRefGoogle Scholar
Buonaccorsi, V. P., McDowell, J. R. and Graves, J. E. ( 2001). Reconciling patterns of inter-ocean molecular variance from four classes of molecular markers in blue marlin (Makaira nigricans). Molecular Ecology 10, 1179–1196.CrossRefGoogle Scholar
Creer, S., Thorpe, R. S., Malhotra, A., Chou, W. H. and Stenson, A. G. ( 2004). The utility of AFLPs for supporting mitochondrial DNA phylogeographical analyses in the Taiwanese bamboo viper, Trimeresurus stejnegeri. Journal of Evolutionary Biology 17, 100–107.CrossRefGoogle Scholar
Criscione, C. D., Poulin, R. and Blouin, M. S. ( 2005). Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology 14, 2247–2257.CrossRefGoogle Scholar
Dame, J. B., Blouin, M. S. and Courtney, C. H. ( 1993). Genetic structure of populations of Ostertagia ostertagi. Veterinary Parasitology 46, 55–62.CrossRefGoogle Scholar
de Gruijter, J. M., Polderman, A. M., Zhu, X. Q. and Gasser, R. B. ( 2002). Screening for haplotypic variability within Oesophagostomum bifurcum (Nematoda) employing a single-strand conformation polymorphism approach. Molecular and Cellular Probes 16, 185–190.CrossRefGoogle Scholar
Denver, D. R., Morris, K., Lynch, M., Vassilieva, L. L. and Thomas, W. K. ( 2000). High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science 289, 2342–2344.CrossRefGoogle Scholar
Divina, B., Wilhelmnsson, E., Mattsson, J. G., Waller, P. and Höglund, J. ( 2000). Identification of Dictyocaulus spp. in ruminants by morphological and molecular analyses. Parasitology 121, 193–201.Google Scholar
Divina, B. P. and Höglund, J. ( 2002). Heterologous transmission of Dictyocaulus capreolus from roe deer (Capreolus capreolus) to cattle (Bos taurus). Journal of Helminthology 76, 125–130.CrossRefGoogle Scholar
Eysker, M. ( 1994). Dictyocaulosis in cattle. Compendium Continuing Education Centre Practicing Veterinarian 16, 669–675.Google Scholar
Fu, Y. X. and Li, W. H. ( 1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709.Google Scholar
Grant, W. N. and Whitington, G. E. ( 1994). Extensive DNA polymorphism within and between two strains of Trichostrongylus colubriformis. International Journal for Parasitology 24, 719–725.CrossRefGoogle Scholar
Graustein, A., Gaspar, J. M., Walters, J. R. and Palopoli, M. F. ( 2002). Levels of DNA polymorphism vary with mating system in the nematode genus Caenorhabditis. Genetics 161, 99–107.Google Scholar
Hawdon, J. M., Li, T., Zhan, B. and Blouin, M. S. ( 2001). Genetic structure of populations of the human hookworm, Necator americanus, in China. Molecular Ecology 10, 1433–1437.CrossRefGoogle Scholar
Higgins, D. G. and Sharp, P. M. ( 1988). CLUSTAL: a package for performing multiple sequence alignments on a microcomputer. Gene 73, 237–244.CrossRefGoogle Scholar
Hoberg, E. P., Monsen, K. J., Kutz, S. and Blouin, M. S. ( 1999). Structure, biodiversity, and historical biogeography of nematode faunas in holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus n. sp. (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen (Ovibos moschatus). Journal of Parasitology 85, 910–934.Google Scholar
Hu, M., Chilton, N. B., Abs El-Osta, Y. G. and Gasser, R. B. ( 2003). Comparative analysis of mitochondrial genome data for Necator americanus from two endemic regions reveals substantial genetic variation. International Journal for Parasitology 33, 955–963.CrossRefGoogle Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. ( 2002 a). The mitochondrial genomes of the human hookworms, Ancylostoma duodenale and Necator americanus (Nematoda: Secernentea). International Journal for Parasitology 32, 145–158.Google Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. ( 2002 b). Long PCR-based amplification of the entire mitochondrial genome from single parasitic nematodes. Molecular and Cellular Probes 16, 261–267.Google Scholar
Hu, M., Chilton, N. B., Zhu, X. and Gasser, R. B. ( 2002 c). Single-strand conformation polymorphism-based analysis of mitochondrial cytochrome c oxidase subunit 1 reveals significant substructuring in hookworm populations. Electrophoresis 23, 27–34.Google Scholar
Hu, M., Chilton, N. B. and Gasser, R. B. ( 2004). Mitochondrial genomics of parasitic nematodes – progress and implications for population genetics and systematics studies. Advances in Parasitology 56, 133–212.Google Scholar
Hudson, R. R., Kreitman, M. and Aguade, M. ( 1987). A test of neutral molecular evolution based on nucleotide data. Genetics 116, 153–159.Google Scholar
Hudson, R. R., Slatkin, M. and Maddison, W. P. ( 1992). Estimation of levels of gene flow from DNA sequence data. Genetics 132, 583–589.Google Scholar
Höglund, J., Engström, A., Morrison, D. A. and Mattsson, J. G. ( 2004 a). Genetic diversity assessed by amplified fragment length polymorphism analysis of the parasitic nematode Dictyocaulus viviparus the lungworm of cattle. International Journal for Parasitology 34, 475–484.Google Scholar
Höglund, J., Morrison, D. A., Divina, B. P., Wilhelmsson, E. and Mattsson, J. G. ( 2003). Phylogeny of Dictyocaulus (lungworms) from eight species of ruminants based on analyses of ribosomal RNA data. Parasitology 127, 179–187.CrossRefGoogle Scholar
Höglund, J., Viring, S. and Törnqvist, M. ( 2004 b). Seroprevalence of Dictyocaulus viviparus in first grazing season calves in Sweden. Veterinary Parasitology 125, 343–352.Google Scholar
Leignel, V. and Humbert, J. F. ( 2001). Mitochondrial DNA variation in benzimidazole-resistant and -susceptible populations of the small ruminant parasite Teladorsagia circumcincta. Journal of Heredity 92, 503–506.CrossRefGoogle Scholar
Lynch, M. and Crease, T. J. ( 1990). The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution 7, 377–394.Google Scholar
Maddison, D. R. and Maddison, W. P. ( 2000). MacClade: Analysis of Phylogeny and Character Evolution. Sunderland: Sinauer Associates.
Morrison, D. A. ( 2005). Networks in phylogenetic analysis: new tools for population biology. International Journal for Parasitology 35, 567–582.CrossRefGoogle Scholar
Morrison, D. A. and Höglund, J. ( 2005). Testing the hypothesis of recent population expansions in nematode parasites of human-associated hosts. Heredity 94, 426–434.CrossRefGoogle Scholar
Nei, M. ( 1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences, USA 70, 3321–3323.CrossRefGoogle Scholar
Nei, M. and Tateno, Y. ( 1975). Interlocus variation of genetic distance and the neutral mutation theory. Proceedings of the National Academy of Sciences, USA 72, 2758–2760.CrossRefGoogle Scholar
Okimoto, R., MacFarlane, J. L., Clary, D. O. and Wolstenholme, D. R. ( 1992). The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130, 471–498.Google Scholar
Page, R. D. M. and Holmes, E. C. ( 1998). Molecular Evolution: a Phylogenetic Approach. Blackwell Science, Oxford.
Roos, M. H., Boersema, J. H., Borgsteede, F. H., Cornelissen, J., Taylor, M. and Ruitenberg, E. J. ( 1990). Molecular analysis of selection for benzimidazole resistance in the sheep parasite Haemonchus contortus. Molecular Biochemistry and Parasitology 43, 77–88.CrossRefGoogle Scholar
Rozas, J. and Rozas, R. ( 1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.CrossRefGoogle Scholar
Schneider, S., Roesslie, D. and Excoffier, L. ( 2000). Arlequin ver 2.000: a Software for Population Genetics Data Analysis. Genetics and Biometry Laboratory University of Geneva, Switzerland.
Schnieder, T., Kaup, F. J. and Drommer, W. ( 1991). Morphological investigations on the pathology of Dictyocaulus viviparus infections in cattle. Parasitology Research 77, 260–265.CrossRefGoogle Scholar
Thomas, W. K. and Wilson, A. C. ( 1991). Mode and tempo of molecular evolution in the nematode Caenorhabditis: cytochrome oxidase II and calmodulin sequences. Genetics 128, 269–279.Google Scholar
van der Veer, M., Kanobana, K., Ploeger, H. W. and de Vries, E. ( 2003). Cytochrome oxidase c subunit 1 polymorphisms show significant differences in distribution between a laboratory maintained population and a field isolate of Cooperia oncophora. Veterinary Parasitology 116, 231–238.CrossRefGoogle Scholar
Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M. and Zabeau, M. ( 1995). AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23, 4407–4414.CrossRefGoogle Scholar
Wakelin, D., Farias, S. E. and Bradley, J. E. ( 2002). Variation and immunity to intestinal worms. Parasitology 125 (Suppl.), S39–S50.CrossRefGoogle Scholar
Woolley, H. ( 1997). The economic impact of husk in dairy cattle. Cattle Practice 5, 315–317.Google Scholar
Yan, G., Romero-Severson, J., Walton, M., Chadee, D. D. and Severson, D. W. ( 1999). Population genetics of the yellow fever mosquito in Trinidad: comparisons of amplified fragment length polymorphism (AFLP) and restriction fragment length polymorphism (RFLP) markers. Molecular Ecology 8, 951–963.CrossRefGoogle Scholar