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.
Similar content being viewed by others
References
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, 131–140
Avise J.C. 2000. Phylogeography. The History and Formation of Species. Harvard University Press, Cambridge, MA
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.x
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.2008.06.017
Bauchau V., Chaline J. 1987. Variabilite de la troisieme molaire inferieure de Clethrionomys glareolus (Arvicolidae, Rodentia) et sa signification evolutive. Mammalia, 51, 587–598
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.1121360
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.x
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.x
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, London
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.x
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.x
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.x
Dybdahl M.F., Lively C.M. 1996. The geography of co-evolution: comparative population structures for a snail and its nematode parasite. Evolution, 50, 2264–2275
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, 2199–2205
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.2005.02.006
Ewens W.J. 1972. The sampling theory of selective neutral alleles. Theoretical Population Biology, 3, 87–112. DOI: 10.1016/0040-5809(72)90035-4
Excoffier L., Laval G., Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary bioinformatics, 1, 47–50
Fu Y.X., Li W.H. 1993. Statistical tests of neutrality of mutations. Genetics, 133, 693–709
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.2011.0482
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.2001.0925
Goüy de Bellocq J., Morand S., Feliu C. 2002. Patterns of parasite species richness of western Paleartic micro-mammals: island effects. Ecography, 25, 173–183
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/s00436-002-0806-1
Grikieniennë J. 2005. Investigations into endoparasites of small mammals in the environs of Lake Drukdiai. Acta Zoologica Lituanica, 15, 109–114
Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. DOI: 10.1080/10635150390235520
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, 95–98
Harpending H.C. 1994. Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biology 66, 591–600
Haukisalmi V., Henttonen H., Tenora F. 1988. Population dynamics of common and rare helminths in cyclic vole populations. Journal of Animal Ecology, 57, 807–825
Haukisalmi V., Henttonen H. 1993. Populations dynamics of taenia polyacantha metacestodes in the bank vole Clethrionomys glareolus. Annales Zoologici Fennici, 30, 81–84
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)00058-6
Hudson R.R., Salatkin M., Maddison W.P. 1992. Estimation of levels of gene flow from DNA sequence data. Genetics, 132, 583–590
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.x
Jukes T.H., Cantor C.R. 1969. Evolution of protein molecules. In: Munroled, H.N. (Ed.), Mammalian Protein Metabolism. Academy Press, New York, pp. 31–132
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, 15–20
Koressaar T., Remm M. 2007. Enhancements and modifications of primer design program Primer3. Bioinformatics, 23, 1289–1291. DOI: 10.1093/bioinformatics/btm091
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.1730921100
Librado P., Rozas J. 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452. DOI: 10.1093/bioinformatics/btp187
Lynch M., Crease T. 1990. The analysis of population survey data on DNA sequence variation. Molecular Biology and Evolution, 7, 377–394
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.6800127
Mazeika V., Paulauskas A., Balciauskas L. 2003. New data on the helminth fauna of rodents of Lithuania. Acta Zoologica Lituanica, 13, 41–47. DOI: 10.1080/13921657.2003.10512542
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.x
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.x
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: 10.2307/2409784
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, 942–951
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.2004.2930
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.x
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.2006.11.012
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.2008.01.028
Nei M. 1973. Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences of the United States of America, 70, 3321–3323
Nei M., Tajima F. 1983. Maximum likelihood estimation of the number of nucleotide substitutions from restriction sites data. Genetics 105, 207–217
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. 183
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.x
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.x
Posada D., Crandall K.A. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818. DOI: 10.1093/bioinformatics/14.9.817
Price P.W. 1980. Evolutionary Biology of Parasites. Princeton University Press, Princeton, New Jersey, USA
Ramos-Onsins S.E., Rozas J. 2002. Statistical properties of new neutrality tests against population growth. Molecular Biology and Evolution, 19, 2092–2100
Rogers A.R., Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution, 9, 552–569
Saitou N., Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425
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.x
Slatkin M., Hudson R.R. 1991. Pairwise comparaisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics, 12, 555–562
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. 212–213
Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585–595
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, 11030–11035
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/msr121
Trewick S.A., Wallis G.P. 2001. Bridging the ‘beech-gap’: New Zealand invertebrate phylogeography implictes Pleistocen glaciation and Pliocene isolation. Evolution, 55, 2170–2180
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.x
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.x
Wright S. 1951. The genetical structure of populations. Ann. Eugen., 15, 323–354
Zhigileva O.N. 2011. Correlation between Biodiversity Indices of Small Mammals and Their Helminths in West Siberian Ecosystems. Contemporary Problems of Ecology, 4, 416–422
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sakka, H., Henttonen, H., Baraket, G. et al. Phylogeography analysis and molecular evolution patterns of the nematode parasite Heligmosomum mixtum based on mitochondrial DNA sequences. Acta Parasit. 60, 85–98 (2015). https://doi.org/10.1515/ap-2015-0011
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1515/ap-2015-0011