Eurasian house mouse (Mus musculus L.) differentiation at microsatellite loci identifies the Iranian plateau as a phylogeographic hotspot

BMC Evolutionary Biology

François Bonhomme⁴  Diethard Tautz¹  Jamshid Darvish³  Meike Teschke¹  Annie Orth⁴  Emilie A Hardouin² 

[1] Max Planck Institute of Evolutionary Biology, Department of Evolutionary Genetics, August-Thienemann-Str. 2, Plön, 24306, Germany;Department of Life and Environmental Sciences, Faculty of Science and Technology, Bournemouth University, Christchurch House, Talbot Campus, Poole BH12 5BB, Dorset, UK;Rodentology Research group, Ferdowsi University of Mashhad, Mashhad, Iran;Institut des Sciences de l’Evolution, CNRS, IRD, EPHE, Université de Montpellier, Pl. E. Bataillon, Montpellier, 34095, France

关键词: Iranian plateau;    Phylogeographic hotspot;    Microsatellites;    House mouse;   

Others  :  1158315
DOI  :  10.1186/s12862-015-0306-4

 received in 2014-09-29, accepted in 2015-02-12,  发布年份 2015

【 摘 要 】

Background

The phylogeography of the house mouse (Mus musculus L.), an emblematic species for genetic and biomedical studies, is only partly understood, essentially because of a sampling bias towards its most peripheral populations in Europe, Asia and the Americas. Moreover, the present-day phylogeographic hypotheses stem mostly from the study of mitochondrial lineages. In this article, we complement the mtDNA studies with a comprehensive survey of nuclear markers (19 microsatellite loci) typed in 963 individuals from 47 population samples, with an emphasis on the putative Middle-Eastern centre of dispersal of the species.

Results

Based on correspondence analysis, distance and allele-sharing trees, we find a good coherence between geographical origin and genetic make-up of the populations. We thus confirm the clear distinction of the three best described peripheral subspecies, M. m. musculus, M. m. domesticus and M. m. castaneus. A large diversity was found in the Iranian populations, which have had an unclear taxonomic status to date. In addition to samples with clear affiliation to M. m. musculus and M. m. domesticus, we find two genetic groups in Central and South East Iran, which are as distinct from each other as they are from the south-east Asian M. m. castaneus. These groups were previously also found to harbor distinct mitochondrial haplotypes.

Conclusion

We propose that the Iranian plateau is home to two more taxonomic units displaying complex primary and secondary relationships with their long recognized neighbours. This central region emerges as the area with the highest known diversity of mouse lineages within a restricted geographical area, designating it as the focal place to study the mechanisms of speciation and diversification of this species.

【 授权许可】

   
2015 Hardouin et al.; licensee BioMed Central.

【 图 表 】

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【 参考文献 】

• [1]Mouse Genome Sequencing Consortium: Initial sequencing and comparative analysis of the mouse genome Nature 2002, 420:520-62.
• [2]Church DM, Goodstadt L, Hillier LW, Zody MC, Goldstein S, She X, et al.: Lineage-specific biology revealed by a finished genome assembly of the mouse. PLoS Biol 2009, 7(5):e1000112. doi:10.1371/journal.pbio.1000112
• [3]Teschke M, Buentge A, Tautz D: Tracing recent adaptations in natural populations of the house mouse. In Evolution of the House mouse (Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology). Edited by Macholán M, Baird SJE, Munclinger P, Piálek J. Cambridge University Press, UK; 2012:315-33.
• [4]Guénet J-L, Bonhomme F: Wild mice: an ever-increasing contribution to a popular mammalian model. Trends Genet 2003, 19:24-31.
• [5]Bonhomme F, Searle JB: House mouse phylogeography. In Evolution of the House mouse (Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology). Edited by Macholán M, Baird SJE, Munclinger P, Piálek J. Cambridge University Press, UK; 2012:278-96.
• [6]Searle JB, Jamieson PM, Gündüz I, Stevens MI, Jones EP, Gemmill CEC, et al.: The diverse origins of New Zealand house mice. Proc R Soc B 2009, 276:209-17. doi:10.1098/rspb.2008.0959
• [7]Hardouin EA, Chapuis J-L, Stevens MI, Van Vuuren JB, Quillfeldt P, Scavetta RJ, et al.: House mouse colonization patterns on the sub-Antarctic Kerguelen Archipelago suggest singular primary invasions and resilience against re-invasion. BMC Evol Biol 2010, 10:325. BioMed Central Full Text
• [8]Gabriel SI, Stevens MI, Da Luz MM, Searle JB: Of mice and ‘convicts’: origin of the Australian house mouse. Mus musculus. PLoS One 2011, 6(12):e28622. doi:10.1371/journal.pone.0028622
• [9]Jones EP, Jóhannesdóttir F, Gündüz I, Richards MB, Searle JB: The expansion of the house mouse into northern-western Europe. J Zool 2011, 283:257-68.
• [10]Suzuki H, Aplin KP: Phylogeny and biogeography of the genus Mus in Eurasia. In Evolution of the House mouse (Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology). Edited by Macholán M, Baird SJE, Munclinger P, Piálek J. Cambridge University Press, UK; 2012:35-64.
• [11]Prager EM, Orrego C, Sage RD: Genetic variation and phylogeography of central Asian and other house mice, including a major new mitochondrial lineage in Yemen. Genetics 1998, 150:835-61.
• [12]Rajabi-Maham H, Orth A, Siahsarvie R, Boursot P, Darvish J, Bonhomme F: The south-eastern house mouse Mus musculus castaneus (Rodentia: Muridae) is a polytypic subspecies. Biol J Linn Soc 2012, 107:295-306.
• [13]Suzuki H, Nunome M, Kinoshita G, Aplin KP, Vogel P, Kryukov AP, et al.: Evolutionary and dispersal history of Eurasian house mice Mus musculus clarified by more extensive geographic sampling of mitochondrial DNA. Heredity 2013, 111(5):375-90.
• [14]Cucchi T, Eszter Kovács Z, Berthon R, Orth A, Bonhomme F, Evin A, et al.: On the trail of Neolithic mice and men towards Transcaucasia: zooarchaeological clues from Nakhchivan (Azerbaijan). Biol J Linn Soc 2013, 108:917-28.
• [15]Duplantier J-M, Orth A, Catalan J, Bonhomme F: Evidence for a mitochondrial lineage originating from the Arabian peninsula in the Madagascar House Mouse (Mus musculus). Heredity 2002, 89:154-8.
• [16]Orth A, Belkhir K, Britton-Davidian J, Boursot P, Benazzou T, Bonhomme F: Hybridation naturelle entre deux espèces sympatriques de souris M. musculus domesticus L. et M. spretus Lataste. C R Biol 2002, 325:89-97.
• [17]Bonhomme F, Orth A, Cucchi T, Rajabi-Maham H, Catalan J, Boursot P, et al.: Genetic differentiation of the house mouse around the Mediterranean basin: matrilineal footprints of early and late colonization. Proc R Soc B 2011, 278:1034-43.
• [18]Orth A, Lyapunova E, Kandaurov A, Boissinot S, Boursot P, Vorontsov N, et al.: L’espèce polytypique Mus musculus en Transcaucasie. C R Biol 1996, 319:435-41.
• [19]Ihle S, Ravaoarimanana I, Thomas M, Tautz D: An analysis of signatures of selective sweeps in natural populations of the house mouse. Mol Biol Evol 2006, 23:790-7.
• [20]Din W, Anand R, Boursot P, Darviche D, Dod B, Jouvin-Marche E, et al.: Origin and radiation of the house mouse: Clues from nuclear genes. J Evol Biol 1996, 9:519-39.
• [21]Rajabi-Maham H, Orth A, Bonhomme F: Phylogeography and postglacial expansion of Mus musculus domesticus inferred from mitochondrial DNA coalescent, from Iran to Europe. Mol Ecol 2008, 17:627-41.
• [22]Auffray J-C, Orth A, Catalan J, Gonzalez J, Desmarais E, Bonhomme F: Phylogenetic position and description of a new species of subgenus Mus (Rodentia, Mammalia) from Thailand. Zool Scr 2003, 32:119-27.
• [23]Cucchi T, Orth A, Auffray J-C, Renaud S, Fabre L, Catalan J, et al.: A new endemic species of the subgenus Mus (Rodentia, Mammalia) on the Island of Cyprus. Zootaxa 2006, 1241:1-36.
• [24]Teschke M, Mukabayire O, Wiehe T, Tautz D: Identification of selective sweeps in closely related populations of the house mouse based on microsatellite scans. Genetics 2008, 180:1537-45.
• [25]Ihle S. Detecting genes involved in selective sweeps within populations of the house mouse species complex-a multi-locus candidate gene approach. PhD thesis. University of Cologne;2004. http://kups.ub.uni-koeln.de/view/creators/Ihle=3ASonja=3A=3A.html.
• [26]Darvish J, Orth A, Bonhomme F: Genetic transition in the house mouse, Mus musculus of Eastern Iranian Plateau. Folia Zool 2006, 55:349-57.
• [27]Pritchard JK, Stephens M, Donnelly P: Inference of population structure using multilocus genotype data. Genetics 2000, 155:945-59.
• [28]Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 2005, 14:2611-20.
• [29]Gao H, Bryc B, Bustamente CD: On Identifying the optimal number of population clusters via the deviance information criterion. PLoS One 2011, 6:e21014. doi:10.1371/journal.pone.0021014
• [30]Nunome M, Ishimori C, Aplin KP, Tsuchiya K, Yonekawa H, Moriwaki K, et al.: Detection of recombinant haplotypes in wild mice (Mus musculus) provides new insights into the origin of Japanese mice. Mol Ecol 2010, 19:2474-89.
• [31]Karn RC, Orth A, Bonhomme F, Boursot P: The complex history of a gene proposed to participate in a sexual isolation mechanism in house mice. Mol Biol Evol 2002, 19:462-71.
• [32]Duvaux L, Belkhir K, Boulesteix M, Boursot P: Isolation and gene flow: inferring the speciation history of European house mouse. Mol Ecol 2011, 20:5248-64.
• [33]Siahsarvie R, Auffray J-C, Darvish J, Rajabi-Maham H, Yu HT, Agret S, et al.: Patterns of morphological evolution in the mandible of the house mouse Mus musculus (Rodentia: Muridae). Biol J Linn Soc 2012, 105:635-47.
• [34]Staubach F, Lorenc A, Messer PW, Tang K, Petrov DA, Tautz D: Genome patterns of selection and introgression of haplotypes in natural populations of the house mouse (Mus musculus). PLoS Genet 2012, 8:e1002891. doi:10.1371/journal.pgen.1002891
• [35]Phifer-Rixey M, Bomhoff M, Nachman M: Genome-wide patterns of differentiation among house mouse subspecies. Genetics 2014, 198:283-97.
• [36]Baird SJE, Macholan M: What can the Mus musculus musculus/M. m. domesticus hybrid zone tell us about speciation? In Evolution of the House mouse (Cambridge Studies in Morphology and Molecules: New Paradigms in Evolutionary Biology). Edited by Macholán M, Baird SJE, Munclinger P, Piálek J. Cambridge University Press, UK; 2012:334-72.
• [37]Thomas M, Moeller F, Wiehe T, Tautz D: A pooling approach to detect signatures of selective sweeps in genome scans using microsatellites. Mol Ecol Notes 2007, 7:400-3.
• [38]Bayer T. Duplicated genes and their relevance in the process of speciation. PhD thesis. University of Cologne;2009. http://kups.ub.uni-koeln.de/2751/.
• [39]Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F: GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5171. Université de Montpellier II, Montpellier (France); 1996.
• [40]Excoffier L, Lischer HEL: Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 2010, 10:564-7.
• [41]Felsenstein J: PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle; 2005.
• [42]Langella O. Populations, 1.2.30 Copyright (C). CNRS UPR9034; 1999. Available at http://bioinformatics.org/~tryphon/populations/.
• [43]Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6. Molecular Evolutionary Genetics Analysis Version 6.0; 2013 http://www.megasoftware.net/.
• [44]Earl DA, von Holdt BM: STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 2012, 4:359-61.
• [45]Jakobsson M, Rosenberg NA: CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 2004, 23:1801-6.
• [46]Rosenberg NA: Distruct: a program for the graphical display of population structure. Mol Ecol Notes 2004, 4:137-8.
• [47]Tamura K, Nei M: Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 1993, 10:512-26.