PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of procbThe Royal Society PublishingProceedings BAboutBrowse by SubjectAlertsFree Trial
 
Proc Biol Sci. 2004 December 22; 271(1557): 2559–2568.
PMCID: PMC1691906

A parasite reveals cryptic phylogeographic history of its host.

Abstract

This study compares the continental phylogeographic patterns of two wild European species linked by a host-parasite relationship: the field mouse Apodemus sylvaticus and one of its specific parasites, the nematode Heligmosomoides polygyrus. A total of 740 base pairs (bp) of the mitochondrial cytochrome b (cyt b) gene were sequenced in 122 specimens of H. polygyrus and compared with 94 cyt b gene sequences (974 bp) previously acquired for A. sylvaticus. The results reveal partial spatial and temporal congruences in the differentiation of both species' lineages: the parasite and its host present three similar genetic and geographical lineages, i.e. Western European, Italian and Sicilian, and both species recolonized northwestern Europe from the Iberian refuge at the end of the Pleistocene. However, H. polygyrus presents three particular differentiation events. The relative rate of molecular evolution of the cyt b gene was estimated to be 1.5-fold higher in the parasite than in its host. Therefore, the use of H. polygyrus as a biological magnifying glass is discussed as this parasite may highlight previously undetected historical events of its host. The results show how incorporating phylogeographic information of an obligate associate can help to better understand the phylogeographic pattern of its host.

Full Text

The Full Text of this article is available as a PDF (299K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Anderson TJ, Blouin MS, Beech RN. Population biology of parasitic nematodes: applications of genetic markers. Adv Parasitol. 1998;41:219–283. [PubMed]
  • Avise JC, Nelson WS, Bowen BW, Walker D. Phylogeography of colonially nesting seabirds, with special reference to global matrilineal patterns in the sooty tern (Sterna fuscata). Mol Ecol. 2000 Nov;9(11):1783–1792. [PubMed]
  • Bermingham E, Martin AP. Comparative mtDNA phylogeography of neotropical freshwater fishes: testing shared history to infer the evolutionary landscape of lower Central America. Mol Ecol. 1998 Apr;7(4):499–517. [PubMed]
  • Blouin MS. Mitochondrial DNA diversity in nematodes. J Helminthol. 1998 Dec;72(4):285–289. [PubMed]
  • Blouin MS, Yowell CA, Courtney CH, Dame JB. Host movement and the genetic structure of populations of parasitic nematodes. Genetics. 1995 Nov;141(3):1007–1014. [PubMed]
  • Blouin MS, Yowell CA, Courtney CH, Dame JB. Substitution bias, rapid saturation, and the use of mtDNA for nematode systematics. Mol Biol Evol. 1998 Dec;15(12):1719–1727. [PubMed]
  • da Silva MN, Patton JL. Amazonian phylogeography: mtDNA sequence variation in arboreal echimyid rodents (Caviomorpha). Mol Phylogenet Evol. 1993 Sep;2(3):243–255. [PubMed]
  • da Silva MN, Patton JL. Molecular phylogeography and the evolution and conservation of Amazonian mammals. Mol Ecol. 1998 Apr;7(4):475–486. [PubMed]
  • Dawson MN, Louie KD, Barlow M, Jacobs DK, Swift CC. Comparative phylogeography of sympatric sister species, Clevelandia ios and Eucyclogobius newberryi (Teleostei, Gobiidae), across the California Transition Zone. Mol Ecol. 2002 Jun;11(6):1065–1075. [PubMed]
  • Denver DR, Morris K, Lynch M, Vassilieva LL, Thomas WK. High direct estimate of the mutation rate in the mitochondrial genome of Caenorhabditis elegans. Science. 2000 Sep 29;289(5488):2342–2344. [PubMed]
  • Ditchfield AD. The comparative phylogeography of neotropical mammals: patterns of intraspecific mitochondrial DNA variation among bats contrasted to nonvolant small mammals. Mol Ecol. 2000 Sep;9(9):1307–1318. [PubMed]
  • Douady Christophe J, Delsuc Frédéric, Boucher Yan, Doolittle W Ford, Douzery Emmanuel J P. Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol Biol Evol. 2003 Feb;20(2):248–254. [PubMed]
  • Edwards SV, Beerli P. Perspective: gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution. 2000 Dec;54(6):1839–1854. [PubMed]
  • Evans BJ, Morales JC, Picker MD, Kelley DB, Melnick DJ. Comparative molecular phylogeography of two Xenopus species, X. gilli and X. laevis, in the south-western Cape Province, South Africa. Mol Ecol. 1997 Apr;6(4):333–343. [PubMed]
  • Gouÿ de Bellocq J, Ferté H, Depaquit J, Justine JL, Tillier A, Durette-Desset MC. Phylogeny of the Trichostrongylina (Nematoda) inferred from 28S rDNA sequences. Mol Phylogenet Evol. 2001 Jun;19(3):430–442. [PubMed]
  • de Bellocq Joëlle Goüy, Sarà Maurizio, Casanova Juan Carlos, Feliu Carlos, Morand Serge. A comparison of the structure of helminth communities in the woodmouse, Apodemus sylvaticus, on islands of the western Mediterranean and continental Europe. Parasitol Res. 2003 May;90(1):64–70. [PubMed]
  • Guindon Stéphane, Gascuel Olivier. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003 Oct;52(5):696–704. [PubMed]
  • Hafner MS, Sudman PD, Villablanca FX, Spradling TA, Demastes JW, Nadler SA. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science. 1994 Aug 19;265(5175):1087–1090. [PubMed]
  • Hewitt GM. Speciation, hybrid zones and phylogeography - or seeing genes in space and time. Mol Ecol. 2001 Mar;10(3):537–549. [PubMed]
  • Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001 Aug;17(8):754–755. [PubMed]
  • Hugall Andrew, Moritz Craig, Moussalli Adnan, Stanisic John. Reconciling paleodistribution models and comparative phylogeography in the Wet Tropics rainforest land snail Gnarosophia bellendenkerensis (Brazier 1875). Proc Natl Acad Sci U S A. 2002 Apr 30;99(9):6112–6117. [PubMed]
  • Jaarola M, Searle JB. A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe. Heredity (Edinb) 2004 Mar;92(3):228–234. [PubMed]
  • Michaux JR, Chevret P, Filippucci M-G, Macholan M. Phylogeny of the genus Apodemus with a special emphasis on the subgenus Sylvaemus using the nuclear IRBP gene and two mitochondrial markers: cytochrome b and 12S rRNA. Mol Phylogenet Evol. 2002 May;23(2):123–136. [PubMed]
  • Michaux JR, Magnanou E, Paradis E, Nieberding C, Libois R. Mitochondrial phylogeography of the Woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Mol Ecol. 2003 Mar;12(3):685–697. [PubMed]
  • Montgomery SS, Montgomery WI. Cyclic and non-cyclic dynamics in populations of the helminth parasites of wood mice, Apodemus sylvaticus. J Helminthol. 1988 Mar;62(1):78–90. [PubMed]
  • Page RD, Lee PL, Becher SA, Griffiths R, Clayton DH. A different tempo of mitochondrial DNA evolution in birds and their parasitic lice. Mol Phylogenet Evol. 1998 Apr;9(2):276–293. [PubMed]
  • Pastorini Jennifer, Thalmann Urs, Martin Robert D. A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Natl Acad Sci U S A. 2003 May 13;100(10):5879–5884. [PubMed]
  • Paterson AM, Banks J. Analytical approaches to measuring cospeciation of host and parasites: through a glass, darkly. Int J Parasitol. 2001 Jul;31(9):1012–1022. [PubMed]
  • Philippe H. MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res. 1993 Nov 11;21(22):5264–5272. [PMC free article] [PubMed]
  • Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14(9):817–818. [PubMed]
  • Queney G, Ferrand N, Weiss S, Mougel F, Monnerot M. Stationary distributions of microsatellite loci between divergent population groups of the European rabbit (Oryctolagus cuniculus). Mol Biol Evol. 2001 Dec;18(12):2169–2178. [PubMed]
  • Rocha Luiz A, Bass Anna L, Robertson D Ross, Bowen Brian W. Adult habitat preferences, larval dispersal, and the comparative phylogeography of three Atlantic surgeonfishes (Teleostei: Acanthuridae). Mol Ecol. 2002 Feb;11(2):243–252. [PubMed]
  • Rozas J, Rozas R. DnaSP version 2.0: a novel software package for extensive molecular population genetics analysis. Comput Appl Biosci. 1997 Jun;13(3):307–311. [PubMed]
  • Sullivan J, Arellano E, Rogers DS. Comparative Phylogeography of Mesoamerican Highland Rodents: Concerted versus Independent Response to Past Climatic Fluctuations. Am Nat. 2000 Jun;155(6):755–768. [PubMed]
  • Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF. Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol. 1998 Apr;7(4):453–464. [PubMed]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society