Testing parasite 'intimacy': the whipworm Trichuris muris in the European house mouse hybrid zone
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
27064973
PubMed Central
PMC4798833
DOI
10.1002/ece3.2022
PII: ECE32022
Knihovny.cz E-zdroje
- Klíčová slova
- Hybrid zones, Mus musculus, parasite life history traits, phylogeography, population structure,
- Publikační typ
- časopisecké články MeSH
Host-parasite interaction studies across hybrid zones often focus on host genetic variation, treating parasites as homogeneous. 'Intimately' associated hosts and parasites might be expected to show similar patterns of genetic structure. In the literature, factors such as no intermediate host and no free-living stage have been proposed as 'intimacy' factors likely constraining parasites to closely follow the evolutionary history of their hosts. To test whether the whipworm, Trichuris muris, is intimately associated with its house mouse host, we studied its population genetics across the European house mouse hybrid zone (HMHZ) which has a strong central barrier to gene flow between mouse taxa. T. muris has a direct life cycle and nonmobile free stage: if these traits constrain the parasite to an intimate association with its host we expect a geographic break in the parasite genetic structure across the HMHZ. We genotyped 205 worms from 56 localities across the HMHZ and additionally T. muris collected from sympatric woodmice (Apodemus spp.) and allopatric murine species, using mt-COX1, ITS1-5.8S-ITS2 rDNA and 10 microsatellites. We show four haplogroups of mt-COX1 and three clear ITS1-5.8S-ITS2 clades in the HMHZ suggesting a complex demographic/phylogeographic history. Microsatellites show strong structure between groups of localities. However, no marker type shows a break across the HMHZ. Whipworms from Apodemus in the HMHZ cluster, and share mitochondrial haplotypes, with those from house mice. We conclude Trichuris should not be regarded as an 'intimate' parasite of the house mouse: while its life history might suggest intimacy, passage through alternate hosts is sufficiently common to erase signal of genetic structure associated with any particular host taxon.
Biodiversity Research Group Faculty of Science Udon Thani Rajabhat University Udon Thani Thailand
Institute of Vertebrate Biology of the Czech Academy of Sciences Brno Czech Republic
Zobrazit více v PubMed
Baird, S. J. E. , Ribas A., Macholán M., Albrecht T., Piálek J., and Goüy de Bellocq J.. 2012. Where are the wormy mice? A reexamination of hybrid parasitism in the European house mouse hybrid zone. Evolution 66:2757–2772. PubMed
Bandelt, H. J. , Forster P., and Röhl A.. 1999. Median‐joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16:37–48. PubMed
Barton, N. H. , and Hewitt G. M.. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113–148.
Behnke, J. M. , and Wakelin D.. 1973. The survival of PubMed
Behnke, J. M. , Lewis J. W., Zain S. N., and Gilbert F. S.. 1999. Helminth infections in PubMed
Behnke, J. M. , Eira C., Rogan M., Gilbert F. S., Torres J., Miquel J., et al. 2009. Helminth species richness in wild wood mice, PubMed
Boursot, P. , Auffray J. C., Britton‐Davidian J., and Bonhomme F.. 1993. The evolution of house mice. Annu. Rev. Ecol. Syst. 24:119–152.
Brant, S. V. , and Ortí G.. 2003. Evidence for gene flow in parasitic nematodes between two host species of shrews. Mol. Ecol. 12:2853–2859. PubMed
Callejón, R. , De Rojas M., Nieberding C., Foronda P., Feliú C., Guevara D., et al. 2010. Molecular evolution of PubMed
Cliffe, L. J. , and Grencis R. K.. 2004. The PubMed
Colangelo, P. , Abiadh A., Aloise G., Amori G., Capizzi D., Vasa E., et al. 2015. Mitochondrial phylogeography of the black rat supports a single invasion of the western Mediterranean basin. Biol. Invasions 17:1859–1868.
Darriba, D. , Taboada G. L., Doallo R., and Posada D.. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9:772. PubMed PMC
Deter, J. , Galan M., Charbonnel N., and Cosson J. F.. 2009. Characterization and PCR multiplexing of polymorphic microsatellite loci in the whipworm PubMed
Detwiler, J. T. , and Criscione C. D.. 2010. An infectious topic in reticulate evolution: introgression and hybridization in animal parasites. Genes 1:102–123. PubMed PMC
R Development Core Team . 2011. R: a language and environment for statistical computing. R Development Core Team, Vienna, Austria.
Ďureje, L. , Macholán M., Baird S. J. E., and Piálek J.. 2012. The mouse hybrid zone in central Europe: from morphology to molecules. Folia Zool. 61:308–318.
Duvaux, L. , Belkhir K., Boulesteix M., and Boursot P.. 2011. Isolation and gene flow: inferring the speciation history of European house mice. Mol. Ecol. 20:5248–5264. PubMed
Earl, D. A. , and vonHoldt B. M.. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv. Genet. Resour. 4:359–361.
Evanno, G. , Regnaut S., and Goudet J.. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14:2611–2620. PubMed
Feliu, C. , Spakulová M., Casanova J. C., Renaud F., Morand S., Hugot J. P., et al. 2000. Genetic and morphological heterogeneity in small rodent whipworms in southwestern Europe: characterization of PubMed
Gasser, R. B. , and Hoste H.. 1995. Genetic markers for closely‐related parasitic nematodes. Mol. Cell. Probes 9:315–320. PubMed
Geraldes, A. , Basset P., Gibson B., Smith K. L., Harr B., Yu H. T., et al. 2008. Inferring the history of speciation in house mice from autosomal, X‐linked, Y‐linked and mitochondrial genes. Mol. Ecol. 17:5349–5363. PubMed PMC
Goudet, J. 1995. FSTAT (vers. 1.2): a computer program to calculate F‐statistics. J. Hered. 86:485–486.
Goüy de Bellocq, J. , Sarà M., Casanova J. C., Feliu C., and Morand S.. 2003. A comparison of the structure of Helminth communities in the woodmouse, PubMed
Goüy de Bellocq, J. , Ribas A., and Baird S. J. E.. 2012. New insights into parasitism in the house mouse hybrid zone Pp. 455–481
Goüy de Bellocq, J. , Baird S. J. E., Albrechtová J., Sobeková K., and Piálek J.. 2015. Murine Cytomegalovirus is not restricted to the house mouse PubMed PMC
Guénet, J. L. , and Bonhomme F.. 2003. Wild mice: an ever‐increasing contribution to a popular mammalian model. Trends Genet. 19:24–31. PubMed
Guindon, S. , and Gascuel O.. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696–704. PubMed
Guindon, S. , Dufayard J. F., Lefort V., Anisimova M., Hordijk W., and Gascuel O.. 2010. New algorithms and methods to estimate maximum‐likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59:307–321. PubMed
Hasegawa, H. , Modrý D., Kitagawa M., Shutt K. A., Todd A., Kalousová B., et al. 2014. Humans and great apes cohabiting the forest ecosystem in central African Republic harbour the same hookworms. PLoS Negl. Trop Dis. 8:1–10. PubMed PMC
Hewitt, G. M. 1988. Hybrid zones‐natural laboratories for evolutionary studies. Trends Ecol. Evol. 3:158–167. PubMed
Jakobsson, M. , and Rosenberg N. A.. 2007. CLUMPP: A cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. PubMed
Jombart, T. 2008. Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. PubMed
Jombart, T. , Devillard S., and Balloux F.. 2010. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet. 11:94. PubMed PMC
Jones, E. P. , Van Der Kooij J., Solheim R., and Searle J. B.. 2010. Norwegian house mice ( PubMed
Kváč, M. , McEvoy J., Loudová M., Stenger B., Sak B., Květoňová D., et al. 2013. Coevolution of PubMed PMC
Librado, P. , and Rozas J.. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. PubMed
Macholán, M. , Munclinger P., Šugerková M., Dufková P., Bímová B., Božíková E., et al. 2007. Genetic analysis of autosomal and X‐linked markers across a mouse hybrid zone. Evolution 61:746–771. PubMed
Mallet, J. 2005. Hybridization as an invasion of the genome. Trends Ecol. Evol. 20:229–237. PubMed
Mccoy, K. D. , Boulinier T., Tirard C., and Michalakis Y.. 2001. Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick
Michaux, J. R. , Libois R., and Filippucci M. G.. 2005. So close and so different: comparative phylogeography of two small mammal species, the yellow‐necked fieldmouse ( PubMed
Milazzo, C. , de Bellocq J. Goüy, Cagnin M., Casanova J. C., di Bella C., Feliu C., et al. 2003. Helminths and ectoparasites of
Moulia, C. , Le Brun N., Dallas J., Orth A., and Renaud F.. 1993. Experimental evidence of genetic determinism in high susceptibility to intestinal pinworm infection in mice: a hybrid zone model. Parasitology 106:387–393. PubMed
Nieberding, C. M. , and Olivieri I.. 2007. Parasites: proxies for host genealogy and ecology?. Trends Ecol. Evol. 22:156–165. PubMed
Peakall, R. , and Smouse P. E.. 2006. GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol. Ecol. Notes 6:288–295. PubMed PMC
Poulin, R. , Krasnov B. R., and Morand S.. 2006. Patterns of host specificity in parasites exploiting small mammals Pp. 233–256
Pritchard, J. K. , Stephens M., and Donnelly P.. 2000. Inference of population structure using PubMed PMC
Rašková, V. , Květoňová D., Sak B., McEvoy J., Edwinson A., Stenger B., et al. 2013. Human cryptosporidiosis caused by PubMed PMC
Raymond, M. , and Rousset F.. 1995. GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J. Hered. 86:248–249.
Ribas, A. , López S., Makundi R. H., Leirs H., and de Bellocq J. Goüy. 2013. PubMed
Ronquist, F. , and Huelsenbeck J. P.. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. PubMed
Rosenberg, N. A. 2004. DISTRUCT: A program for the graphical display of population structure. Mol. Ecol. Notes 4:137–138.
Rousset, F. 1997. Genetic differentiation and estimation of gene flow from F‐statistics under isolation by distance. Genetics 145:1219–1228. PubMed PMC
Sage, R. D. , Heyneman D., Lim K. C., and Wilson A. C.. 1986. Wormy mice in a hybrid zone. Nature 324:60–63. PubMed
Tamura, K. , Stecher G., Peterson D., Filipski A., and Kumar S.. 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30:2725–2729. PubMed PMC
Wagnerová, P. , Sak B., McEvoy J., Rost M., Perec Matysiak A., Ježková J., et al. 2015. Genetic diversity of PubMed
Wang, L. , Luzynski K., Pool J. E., Janoušek V., Dufkova P., Vyskočilova M. M., et al. 2011. Measures of linkage disequilibrium among neighbouring SNPs indicate asymmetries across the house mouse hybrid zone. Mol. Ecol. 20:2985–3000. PubMed
Whiteman, N. K. , and Parker P. G.. 2005. Using parasites to infer host population history: a new rationale for parasite conservation. Anim. Conserv. 8:175–181.