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Acta Parasitologica

, Volume 60, Issue 1, pp 85–98 | Cite as

Phylogeography analysis and molecular evolution patterns of the nematode parasite Heligmosomum mixtum based on mitochondrial DNA sequences

  • Hela Sakka
  • Heikki Henttonen
  • Ghada Baraket
  • Salhi-Hannachi AmelEmail author
  • Johan Michaux
Article

Abstract

Mitochondrial DNA was explored to study phylogeography of the nematode parasite Heligmosomum mixtum and elucidate molecular evolution pattern of cytochrome b gene. The size of cyt b gene ranged from 511 bp to 591 bp and the average of GC contents was 28.9%. The overall transition/transversion ratio R was 5.773 indicating that the transitions are more frequent than transversion. The aligned sequences allowed identifying 54 mtDNA haplotypes among the 119 examined individuals. The genetic divergence registered among the populations of H. mixtum was low (0.3% to 1.5%). Neighbor-joining and maximum Likelihood trees evidenced a huge polytomy and unstructured phylogeographic pattern among the studied populations. The demographic analyses tend to evidence a recent and rapid expansion of H. mixtum. Our results imply a positive selection and the genetic hitchhiking effect is unlikely. Parameters performed supported scenario of sweep selection and recent expansion of H.mixtum populations. Both positive selection and demographic histories have jointly contributed to the observed patterns of nucleotide diversity and haplotypes structure. The comparison of the phylogeographical pattern of H. mixtum with the one of its most common rodent host M. glareolus, confirmed a strong incongruence between the two species. These results strongly suggest that the parasite would not be specific to M. glareolus and that it would switch easily from one rodent species to another. The mitochondrial diversity seems to be unstructured with any biogeographic repartition of the variability and that the genetic structure of H. mixtum is probably associated with weak host specificity.

Keywords

Mitochondrial DNA Cytochrome b gene Phylogeography Myodes glareolus Nematode parasite Heligmosomum mixtum 

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References

  1. Asakawa M. 1987. Genus Heligmosomoides Hall, 1916 (Heligmosomoidae: Nematoda) from the Japanese wood mice, Apodemus spp. III. The life-cycle of Heligmosomoides kurilensis kobayashii (Nadtochii, 1966) in ICR mice and preliminary experimental infection to jirds. Journal of the College of Dairying, 12, 131–140Google Scholar
  2. Avise J.C. 2000. Phylogeography. The History and Formation of Species. Harvard University Press, Cambridge, MAGoogle Scholar
  3. Ballard J.W.O., Whitlock M.C. 2004. The incomplete natural history of mitochondria. Molecular Ecology, 13, 729–744. DOI: 10.1046/j.1365-294X.2003.02063.xCrossRefGoogle Scholar
  4. Barrett L.G., Thrall P.H., Burdon J.J., Linde C.C. 2008. Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology and Evolution, 23, 678–685. DOI: 10.1016/j.tree.2008.06.017CrossRefGoogle Scholar
  5. Bauchau V., Chaline J. 1987. Variabilite de la troisieme molaire inferieure de Clethrionomys glareolus (Arvicolidae, Rodentia) et sa signification evolutive. Mammalia, 51, 587–598CrossRefGoogle Scholar
  6. Biek R., Drummond A.J., Poss M. 2006. A virus reveals population structure and recent demographic history of its carnivore host. Science, 311, 538–541. DOI: 10.1126/science.1121360CrossRefGoogle Scholar
  7. Buckley T.R., Simon C., Chambers G.K. 2001. Phylogeography of the New Zealand cicada Maoricicada campbelli based on mitochondrial DNA sequences: ancient clades associated with Cenozoic environmental change. Evolution, 55, 1395–1407. DOI: 10.1111/j.0014-3820.2001.tb00661.xCrossRefGoogle Scholar
  8. Burban C., Petit R.J., 2003. Phylogeography of maritime pine inferred with organelle markers having contrasted inheritance. Molecular Ecology, 12, 1487–1495. DOI: 10.1046/j.1365-294X.2003.01817.xCrossRefGoogle Scholar
  9. Cordy J.M. 1991. Paleoecology of the late glacial and early postglacial of Belgium and neighbouring areas. In: The late glacial in Northwest Europe: human Adaptation and environmental Change at the End of the Pleistocene (eds Barton N, Robers AJ, Roe DA), pp.40–47. Council for British Archaeology, LondonGoogle Scholar
  10. Criscione C.D., Poulin R., Blouin M.S. 2005. Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Molecular Ecology, 14, 2247–2257. DOI: 10.1111/j.1365-294X.2005.02587.xCrossRefGoogle Scholar
  11. Deffontaine V., Libois R., Kotlik P., Sommer R., Nieberding C., Paradis E., Searle J.B., Michaux J.R. 2005. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology, 14, 1727–1739. DOI: 10.1111/j.1365-294X.2005.02506.xCrossRefGoogle Scholar
  12. Deffonatine V., Ledevin R., Fontaine M.C., Quéré J-P., Renaud S., Libois R., Michaux J.R. 2009. A relict bank vole lineage highlights the biogeographic history of the Pyrenean region in Europe. Molecular Ecology, 18, 2489–2502. DOI: 10.1111/j.1365-294X.2009.04162.xCrossRefGoogle Scholar
  13. Dybdahl M.F., Lively C.M. 1996. The geography of co-evolution: comparative population structures for a snail and its nematode parasite. Evolution, 50, 2264–2275CrossRefGoogle Scholar
  14. Emerson B.C., Oromi P., Hewitt G.M. 2000. Tracking colonization and diversification of insect lineages on islands: mitochondrial DNA phylogeography of Tarphius canariensis Coleoptera: Colydidae) on the Canary Islands. Proceedings of the Royal Society of London. Series B, Biological Sciences, 267, 2199–2205CrossRefGoogle Scholar
  15. Eswaran V., Harpending H., Roger A.R. 2005. Genomics refutes and exclusively African origin of humans. Journal of Human Evolution, 49, 1–18. DOI: 10.1016/j.jhevol.2005.02.006CrossRefGoogle Scholar
  16. Ewens W.J. 1972. The sampling theory of selective neutral alleles. Theoretical Population Biology, 3, 87–112. DOI: 10.1016/0040-5809(72)90035-4CrossRefGoogle Scholar
  17. Excoffier L., Laval G., Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary bioinformatics, 1, 47–50CrossRefGoogle Scholar
  18. Fu Y.X., Li W.H. 1993. Statistical tests of neutrality of mutations. Genetics, 133, 693–709PubMedPubMedCentralGoogle Scholar
  19. Galbreath K.E., Eric P., Hoberg E.P. 2012. Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas. Proceedings of the Royal Society B, 279, 371–378. DOI: 10.1098/rspb.2011.0482CrossRefGoogle Scholar
  20. Goüy de Bellocq J., Ferté H., Depaquit J., Justine J.L., Tillier A., Durette-Desset M.C. 2001. Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Molecular Phylogenetics and Evolution, 19, 430–442. DOI: 10.1006/mpev.2001.0925CrossRefGoogle Scholar
  21. Goüy de Bellocq J., Morand S., Feliu C. 2002. Patterns of parasite species richness of western Paleartic micro-mammals: island effects. Ecography, 25, 173–183CrossRefGoogle Scholar
  22. Goüy de Bellocq J., Sara M., Casanova J.C., Feliu C., Morand S. 2003. A comparaison of the strcuture of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the Western mediterranean and continental Europe. Parasitology Research, 90, 64–70. DOI: 10.1007/s00436-002-0806-1Google Scholar
  23. Grikieniennë J. 2005. Investigations into endoparasites of small mammals in the environs of Lake Drukdiai. Acta Zoologica Lituanica, 15, 109–114CrossRefGoogle Scholar
  24. Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. DOI: 10.1080/10635150390235520CrossRefGoogle Scholar
  25. Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series, 41, 95–98Google Scholar
  26. Harpending H.C. 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591–600PubMedGoogle Scholar
  27. Haukisalmi V., Henttonen H., Tenora F. 1988. Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology, 57, 807–825CrossRefGoogle Scholar
  28. Haukisalmi V., Henttonen H. 1993. Populations dynamics of taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus. Annales Zoologici Fennici, 30, 81–84Google Scholar
  29. Haukisalmi V., Henttonen H., Vikman P. 1996. Variability of sex ratio, mating probability and egge production in an intestinal nematode in its fluctuating host population International Journal for Parasitology, 26, 755–764. DOI: 10.1016/0020-7519(96)00058-6CrossRefGoogle Scholar
  30. Hudson R.R., Salatkin M., Maddison W.P. 1992. Estimation of levels of gene flow from DNA sequence data. Genetics, 132, 583–590PubMedPubMedCentralGoogle Scholar
  31. Jones P.H., Britten H.B. 2010. The absence of concordant population genetic structure in the black-tailed prairie dog and the flea, Oropsylla hirsuta, with implications for the spread of Yersinia pestis. Molecular Ecology, 19, 2038–2049. DOI: 10.1111/j.1365-294X.2010.04634.xCrossRefGoogle Scholar
  32. Jukes T.H., Cantor C.R. 1969. Evolution of protein molecules. In: Munroled, H.N. (Ed.), Mammalian Protein Metabolism. Academy Press, New York, pp. 31–132Google Scholar
  33. Kia E.B., Shahryary-Rad E., Mohebali M., Mahmoudi M., Mobedi I., Zahabiun F., Zarei Z., Miahipoor A., Mowlavi Gh., Akhavan A.A., Vatandoost’ H. 2010. Endoparasites of Rodents and Their Zoonotic Importance in Germi, Dashte-Mogan, Ardabil Province, Iran. Iranian Journal of Parasitology, 5, 15–20PubMedPubMedCentralGoogle Scholar
  34. Koressaar T., Remm M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics, 23, 1289–1291. DOI: 10.1093/bioinformatics/btm091CrossRefGoogle Scholar
  35. Lessa E.P., Cook J.A., Patton J.L. 2003. Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proceedings of the National Academy of Sciences of the United States of America, 100, 10331–10334. DOI: 10.1073/pnas.1730921100CrossRefGoogle Scholar
  36. Librado P., Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. DOI: 10.1093/bioinformatics/btp187CrossRefGoogle Scholar
  37. Lynch M., Crease T. 1990. The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution, 7, 377–394PubMedGoogle Scholar
  38. Mavarez J., Pointier J-P., David P., Delay B., Jarne P. 2002. Genetic differentiation, dispersal and mating system in the schistosome-transmitting freshwater snail Biomphalaria glabrata. Heredity, 89, 258–265. DOI: 10.1038/sj.hdy.6800127CrossRefGoogle Scholar
  39. Mazeika V., Paulauskas A., Balciauskas L. 2003. New data on the helminth fauna of rodents of Lithuania. Acta Zoologica Lituanica, 13, 41–47. DOI: 10.1080/13921657.2003.10512542CrossRefGoogle Scholar
  40. McCoy K., Boulinier T., Tirard C., Michalakis Y. 2003. Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution, 57, 288–296. DOI: 10.1111/j.0014-3820.2003.tb00263.xCrossRefGoogle Scholar
  41. McCoy K., Boulinier T., Tirard C. 2005. Comparative host-parasite population structures: disantangling prospecting and dispersal in the black-legged kittiwake Rissae tridactyla. Molecular Ecology, 14, 2825–2838. DOI: 10.1111/j.1365-294X.2005.02631.xCrossRefGoogle Scholar
  42. Mulvey M., Aho J.M., Lydeard C. 1991. Comparative population genetic structure of a parasite (Fascioloides magna) and its definitive host. Evolution, 45, 1628–1640. DOI: 10.2307/2409784PubMedGoogle Scholar
  43. Nadler S.A., Hafner M.S. 1990. Genetic differentiation among chewing louse populations (Mallaphaga: Trichodectidae) in a pocket gopher contact zone (Rodentia: Geomyidae). Evolution, 44, 942–951CrossRefGoogle Scholar
  44. Nieberding C., Morand S., Libois R., Michaux J.R. 2004. A parasite reveals cryptic phylogeographic history of its host. Proceedings of the Royal Society of London. Series B, 271, 2559–2568. DOI: 10.1098/rspb.2004.2930CrossRefGoogle Scholar
  45. Nieberding C., Libois R., Douady S., Morand S., Michaux J.R. 2005. Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages? Molecular Ecology, 14, 765–779. DOI: 10.1111/j.1365-294X.2005.02440.xCrossRefGoogle Scholar
  46. Nieberding C.M., Olivieri I. 2007. Parasites: proxies for host genealogy and ecology? Trends in Ecology and Evolution, 22, 156–165. DOI: 10.1016/j.tree.2006.11.012CrossRefGoogle Scholar
  47. Nieberding C., Durette-Desset M.C., Vanderpoorten A., Casanova J.C., Ribas A., Deffontaine V., Feliu C., Morand S., Libois R., Michaux J.R. 2008. Geography and host biogeography matter for understanding the phylogeography of a parasite. Molecular Phylogenetics and Evolution, 47, 538–554. DOI:10.1016/j.ympev.2008.01.028CrossRefGoogle Scholar
  48. Nei M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America, 70, 3321–3323CrossRefGoogle Scholar
  49. Nei M., Tajima F. 1983. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105, 207–217PubMedPubMedCentralGoogle Scholar
  50. N’Zobadila G. 1994. Biologie d’Heligmosomoides polygyrus polygyrus (Dujardin, 1845) (Nematoda-Trichostrongylina). Comparaison avec les espèces proches et sa sous spéciation americaine. Thèse de Doctorat. Muséum National d’Histoire Naturelle, pp. 183Google Scholar
  51. Petit R.J., Duminil J., Fineshi S., Hampe A., Salvini D., Vendramin G.V. 2005. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molecular Ecology, 14, 689–701. DOI: 10.1111/j.1365-294X.2004.02410.xCrossRefGoogle Scholar
  52. Parker M.A., Spoerke J.M. 1998. Geographic structure of lineage associations in a plant-bacterial mutualism. Journal of Evolutionary Biology, 11, 549–562. DOI: 10.1046/j.1420-9101.1998.11050549.xCrossRefGoogle Scholar
  53. Posada D., Crandall K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818. DOI: 10.1093/bioinformatics/14.9.817CrossRefGoogle Scholar
  54. Price P.W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey, USAGoogle Scholar
  55. Ramos-Onsins S.E., Rozas J. 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092–2100CrossRefGoogle Scholar
  56. Rogers A.R., Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569PubMedGoogle Scholar
  57. Saitou N., Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425PubMedGoogle Scholar
  58. Schulthesis A.S., Weigt L.A., Hendricks A.C. 2002. Gene flow, dispersal, and nested clade analysis among populations of the stonefly Peltoperla tarteri in the southern Appalachians. Molecular Ecology, 11, 317–327. DOI: 10.1046/j.1365-294X.2002.01445.xCrossRefGoogle Scholar
  59. Slatkin M., Hudson R.R. 1991. Pairwise comparaisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 12, 555–562Google Scholar
  60. Spitzenberger F. 1999. Clethrionomys glareolus. In: The Atlas of European Mammals (eds Mitchell-Jones AJ, Amori G, Bogdanowicz. W et al.), Academic Press, London. pp. 212–213Google Scholar
  61. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595PubMedPubMedCentralGoogle Scholar
  62. Tamura K., Nei M., Kumar S. 2004. Prospects for inferring very large phylogenies by using the neighbor-joining method. Proceedings of the National Academy of Sciences of the United States of America, 101, 11030–11035CrossRefGoogle Scholar
  63. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Molecular Biology and Evolution, 28, 2731–2739. DOI: 10.1093/molbev/msr121CrossRefGoogle Scholar
  64. Trewick S.A., Wallis G.P. 2001. Bridging the ‘beech-gap’: New Zealand invertebrate phylogeography implictes Pleistocen glaciation and Pliocene isolation. Evolution, 55, 2170–2180PubMedGoogle Scholar
  65. Wickström L.M., Haukisalmi V., Varis S., Hantula J., Fedorov V.B., Henttonen H. 2003. Phylogeography of the circumpolar Paranoplocephala arctica species complex (Cestoda: Anoplocephalidae) parasitizing collared lemmings (Dicrostonyx spp.). Molecular Ecology, 12, 3259–3371. DOI: 10.1046/j.1365-294X.2003.01985.xCrossRefGoogle Scholar
  66. Whiteman N.K., Kimball R.T., Parker P.G. 2007. Co-phylogeography and comparative population genetics of the threatened Galapagos hawk and three ectoparasite species: ecology shapes population histories within parasite communities. Molecular Ecology, 16, 4759–4773. DOI: 10.1111/j.1365-294X.2007.03512.xCrossRefGoogle Scholar
  67. Wright S. 1951. The genetical structure of populations. Ann. Eugen., 15, 323–354CrossRefGoogle Scholar
  68. Zhigileva O.N. 2011. Correlation between Biodiversity Indices of Small Mammals and Their Helminths in West Siberian Ecosystems. Contemporary Problems of Ecology, 4, 416–422CrossRefGoogle Scholar

Copyright information

© W. Stefański Institute of Parasitology, PAS 2015

Authors and Affiliations

  • Hela Sakka
    • 1
    • 2
    • 3
  • Heikki Henttonen
    • 5
  • Ghada Baraket
    • 1
  • Salhi-Hannachi Amel
    • 1
    Email author
  • Johan Michaux
    • 3
    • 4
  1. 1.Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie. Département de Biologie, faculté des Sciences de TunisUnversité Tunis El Manar 2092 El ManarTunisTunisia
  2. 2.Faculté des Sciences de BizerteZarzounaTunisia
  3. 3.INRA, UMR CBGP 1062Campus international de Baillarguet, CS 30016Montferrier-sur-Lez cedexFrance
  4. 4.Conservation Genetics UnitUniversity of Liege, Institute of Botany (Bat. 22)LiègeBelgium
  5. 5.The Finnish Forest Research Institute Vantaa Research UnitVantaa UnitFinland

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