[en] The bank vole experienced a complex history during the Quaternary. Repeated isolation in glacial refugia led to the differentiation of several lineages in less than 300 000 years. We investigated if such a recent differentiation led to a significant divergence of phenotypic characters between European lineages, which might provide insight into processes of intraspecific differentiation. The size and shape of the first and third upper molars, and first lower molar, of bank voles genetically attributed to different lineages were quantified using an outline analysis of their occlusal surface. The three teeth present similar trends of decreasing size towards high latitudes. This trend, the inverse of Bergmann's rule, is interpreted as the result of a balance between metabolic efficiency and food availability, favouring small body size in cold regions. Molar shape appeared to differ between lineages despite genetic evidence of suture zones. A mosaic pattern of evolution between the different teeth was evidenced. The analysis of such phenotypic features appears as a valuable complement to genetic analyses, providing a complementary insight into evolutionary processes, such as selective pressures, that have driven the differentiation of the lineages. It may further allow the integration of the paleontological dimension of the bank vole phylogeographic history. (C) 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 681-694.
Disciplines :
Zoology
Author, co-author :
Ledevin, Ronan
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Deffontaine, Valerie
Henttonen, Heikki
Renaud, Sabrina
Language :
English
Title :
Evolutionary history of the bank vole Myodes glareolus: a morphometric perspective
Albertson RC, Kocher TD. Genetic architecture sets limits on transgressive segregation in hybrid cichlid fishes. Evolution 2005, 59:686-690.
Arnold ML, Hodges SA. Are natural hybrids fit or unfit relative to their parents? Trends in Ecology and Evolution 1995, 10:67-71.
Austin JD, Lougheed SC, Neidrauer L, Chek AA, Boaga PT. Cryptic lineages in a small frog: the post-glacial history of the spring peeper, Pseudacris crucifer (Anura: Hylidae). Molecular Phylogenetics and Evolution 2002, 25:316-329.
Avise JC. Phylogeography: the history and formation of species 2000, 1-464. Cambridge, Harvard University Press
Barnes I, Matheus P, Shapiro B, Jensen D, Cooper A. Dynamics of Pleistocene Population Extinctions in Beringian Brown Bears. Science 2002, 295:2267-2270.
Barnosky AD. Mosaic evolution at the population level in Microtus pennsylvaticus. Morphological change in Quaternary mammals of North America 1993, 24-58. Martin RABarnosky AD. In, eds., Cambridge University Press
Bauchau V, Chaline J. Variabilité de la troisième molaire supérieure de Clethrionomys glareolus (Arvicolidae, Rodentia) et sa signification évolutive. Mammalia 1987, 51:587-598.
Bergmann C. Über die Verhältnisse der Wärmeökonomie der Thiere zu ihrer Grösse. Gottinger Studien 1847, 3:595-708.
Bilton DT, Mirol PM, Mascheretti S, Fredga K, Zima J, Searle JB. Mediterranean Europe as an area of endemism for small mammals rather than a source for northwards postglacial colonization. Proceedings of the Royal Society of London 1998, 265:12919-12926.
Bookstein FL. Morphometric tools for landmark data: geometry and biology 1991, 1-414. Cambridge, Cambridge University Press
Boratynski Z, Koskela E, Mappes T. The effect of mtDNA introgression on phenotype - body mass and basal metabolic rate. 2009, 12th Congress European Society for Evolutionary Biology. Abstract with program, 24-36 poster
Carstens BC, Knowles LL. Shifting distributions and speciation: species divergence during rapid climate change. Molecular Ecology 2007, 16:619-627.
Caumul R, Polly PD. Phylogenetic and environmental components of morphological variation: skull, mandible and molar shape in marmots (Marmota, Rodentia). Evolution 2005, 59:2460-2472.
Chaline J, Brunet-Lecomte P, Montuire S, Viriot L, Courant F. Anatomy of the arvicoline radiation (Rodentia): palaeogeographical, palaeoecological history and evolutionary data. Annales Zoologici Fennici 1999, 36:239-267.
Conroy CJ, Cook JA. MtDNA Evidence for Repeated Pulses of Speciation Within Arvicoline and Murid Rodents. Journal of Mammalian Evolution 1999, 6:221-245.
Crampton JS. Elliptic Fourier shape analysis of fossil bivalves: some practical considerations. Lethaia 1995, 28:179-186.
Deffontaine V, Ledevin R, Fontaine MC, Quéré JP, Renaud S, Libois R, Michaux JR. A relict bank vole lineage highlights the biogeographic history of the Pyrenean region in Europe. Molecular Ecology 2009, 18:2489-2502.
Deffontaine V, Libois R, Kotlík P, Sommer R, Nieberding C, Paradis E, Searle JB, Michaux JR. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology 2005, 14:1727-1739.
Ellison GTH, Taylor PJ, Nix HA, Bronner GN, McMahon JP. Climatic adaptation of body size among pouched mice (Saccostomus campestris: Cricetidae) in the southern African subregion. Global Ecology and Biogeography Letters 1993, 3:41-47.
Erlinge S. Why do European stoats Mustela erminea not follow Bergmann's rule? Holarctic Ecology 1987, 10:33-39.
Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 1981, 17:368-376.
Ferson S, Rohlf FJ, Koehn R. Measuring shape variation of two-dimensional outlines. Systematic Zoology 1985, 34:59-68.
Garnier S, Magniez-Jannin F, Rasplus J-Y, Alibert P. When morphometry meets genetics: inferring the phylogeography of Carabus solieri using Fourier analyses of pronotum and male genitalia. Journal of Evolutionary Biology 2005, 18:269-280.
Good JM, Demboski JR, Nagorsen DW, Jack S. Phylogeography and Introgressive Hybridization: Chipmunks (Genus: Tamias) in the Northern Rocky Mountains. Evolution 2003, 57:1900-1916.
Guérécheau A, Ledevin R, Henttonen H, Deffontaine V, Michaux JR, Chevret P, Renaud S. Seasonal variation in molar outline of bank voles: An effect of wear? Mammalian Biology. 2010, 75:311-319.
Guindon S, Gascuel O. A simple fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 2003, 52:696-704.
Hadly EA, Kohn MH, Leonard JA, Wayne RK. A genetic record of population isolation in pocket gophers during Holocene climatic change. Proceedings of the National Academy of Sciences, USA 1998, 95:6893-6896.
Hewitt GM. The genetic legacy of the Quaternary ice ages. Nature 2000, 405:907-913.
Jaarola M, Searle JB. A highly divergent mitochondrial DNA lineage of Microtus agrestis in southern Europe. Heredity 2004, 92:228-234.
Jockusch E, Wake DB. Falling apart and merging: diversification of slender salamanders (Plethodontidae: Batrachoseps) in the American West. Biological Journal of the Linnean Society 2002, 76:361-391.
Kaneko Y. Identification and Morphological Characteristics of Clethrionomys rufocanus, Eothenomys shanseius, E. inez and E. eva from the USSR, Mongolia, and Northern and Central China. Journal of Mammalian Society of Japan 1992, 16:71-95.
Kavanagh KD, Evans AR, Jernvall J. Predicting evolutionary patterns of mammalian teeth from development. Nature 2007, 449:427-432.
Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. Proceedings of the National Academy of Sciences, USA 1981, 78:454-458.
Kitahara E. Taxonomic status of Anderson's red-backed vole on the Kii peninsula, Japan, based on skull and dental characters. Journal of Mammalian Society of Japan 1995, 20:9-28.
Kotlík P, Deffontaine V, Mascheretti S, Zima J, Michaux JR, Searle JB. A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences, USA 2006, 103:14860-14864.
Kuhl FP, Giardina CR. Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 1982, 18:259-278.
Lugon-Moulin N, Hausser J. Phylogeographical structure, postglacial recolonization and barriers to gene flow in the distinctive Valais chromosome race of the common shrew (Sorex araneus). Molecular Ecology 2002, 11:785-794.
Luo J, Yang D, Suzuki H, Wang Y, Chene W-J, Campbell KL, Zhang Y-P. Molecular phylogeny and biogeography of oriental voles: genus Eothenomys (Muridae, Mammalia). Molecular Phylogenetics and Evolution 2004, 3:349-362.
Marcolini F. Fourier analysis applied to Mimomys (Arvicolidae, Rodentia, Mammalia) first Lower molar - biochronological implications. Mathematical Geology 2006, 38:667-678.
Martin RA, Crockett CP, Marcolini F. Variation of the schmelzmuster and other enamel characters in molars of the primitive Pliocene vole Ogmodontomys from Kansas. Journal of Mammalian Evolution 2006, 13:223-241.
Meiri S, Dayan T. On the validity of Bergmann's rule. Journal of Biogeography 2003, 30:331-351.
Meiri S, Dayan T, Simberloff D. Carnivores, biases and Bergmann's rule. Biological Journal of the Linnean Society 2004, 81:579-588.
Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC. Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Molecular Ecology 2005, 14:2459-2464.
Michaux J, Chevret P, Renaud S. Morphological diversity of Old World rats and mice (Rodentia, Muridae) mandible in relation with phylogeny and adaptation. Journal of Zoological Systematics and Evolutionary Research 2007, 45:263-279.
Mikulová P, Frynta D. Test of character displacement in urban populations of Apodemus sylvaticus. Canadian Journal of Zoology 2001, 79:794-801.
Navarro N, Zatarain X, Montuire S. Effects of morphometric descriptor change on statistical classification and morphospaces. Biological Journal of the Linnean Society 2004, 83:243-260.
Osipova OV, Soktin AA. Bank and red vole hybridization under experimental conditions. Doklady Biological Sciences 2006, 410:381-383.
Posada D, Crandall KA. Modeltest: testing the model of DNA substitution. Bioinformatics 1998, 14:817-818.
Potapov SG, Illiarionova NA, Andreeva TA, Baskevitch MI, Okulova NM, Lavrenchenko LA, Orlov VN. Transfer of Mitochondrial Genome of the Northern Redbacked Vole (Clethrionomys rutilus) to the Bank Vole (Clethrionomys glareolus) in Northwestern Europe. Doklady Biological Sciences 2007, 417:435-438.
Renaud S, Chevret P, Michaux J. Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents. Zoologica Scripta 2007, 36:525-535.
Renaud S, Michaux JR. Mandibles and molars of the wood mouse, Apodemus sylvaticus (L.): integrated latitudinal signal and mosaic insular evolution. Journal of Biogeography 2007, 34:339-355.
Renaud S, Michaux J, Jaeger J-J, Auffray J-C. Fourier analysis applied to Stephanomys (Rodentia, Muridae) molars: nonprogressive evolutionary pattern in a gradual lineage. Paleobiology 1996, 22:255-265.
Renaud S, Millien V. Intra- and interspecific morphological variation in the field mouse species Apodemus argenteus and A. speciosus in the Japanese archipelago: the role of insular isolation and biogeographic gradients. Biological Journal of the Linnean Society 2001, 74:557-569.
Renvoisé E, Evans AR, Jebrane A, Labruère C, Laffont R, Montuire S. Evolution of mammal tooth patterns: new insights from a developmental prediction model. Evolution 2009, 63:1327-1340.
Rohlf FJ. Fitting curves to outlines. proceedings of the michigan morphometrics workshop 1990, 169-176. Rohlf FJBookstein FL. In, eds., Spec. Publ. 2, University of Michigan Museum of Zoology, Ann Arbor
Rohlf FJ. NTSYS-pc, numerical taxonomy and multivariate analysis system 2000, New York, Exeter Software
Rohlf FJ, Archie JW. A comparison of Fourier methods for the description of wing shape in mosquitoes (Diptera: Culicidae). Systematic Zoology 1984, 33:302-317.
Rychlik L, Ramalhinho G, Polly PD. Response to environmental factors and competition: skull, mandible and tooth shapes in Polish water shrews (Neomys, Soricidae, Mammalia). Journal of Zoological Systematics and Evolutionary Research 2006, 44:339-351.
Sommer RS, Benecke N. The recolonization of Europe by brown bears Ursus arctos Linnaeus, 1758 after the Last Glacial Maximum. Mammal Review 2005, 35:156-164.
Sundell J, Norrdahl K. Body size-dependent refuges in voles: an alternative explanation of the Chitty effect. Annales Zoologici Fennici 2002, 39:325-333.
Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007, 24:1596-1599.
Tegelström H. Transfer of mitochondrial DNA from the northern red-backed vole (Clethrionomys rutilus) to the bank vole (C. glareolus). Journal of Molecular Ecology 1987, 24:218-227.
Tougard C, Brunet-Lecomte P, Fabre M, Montuire S. Evolutionary history of two allopatric Terricola species (Arvicolinae, Rodentia) from molecular, morphological, and palaeontological data. Biological Journal of the Linnean Society 2008, 93:309-323.
Wilson DE, Reeder DM. Mammal species of the world, a taxonomic and geographic reference. 2005, Vol. 1-2, Baltimore, Maryland, The Johns Hopkins University Press, 1-2142
Yom-Tov Y, Geffen E. Geographic variation in body size: the effects of ambient temperature and precipitation. Oecologia 2006, 148:213-218.
Zalewski A. Geographical and seasonal variation in food habits and prey size of European pine martens. Martens and fishers (martes) in human-altered environments 2005, 77-98. Harrison DJFuller AKProulx G. In, eds., Springer Science & Business Media, Springer-Verlag
