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Mitochondrial DNA Gene Diversity and Morphological Variability of the Common Vole (Microtus arvalis) in
France
Amélie Petitjean, Sophie Montuire, Elodie Renvoisé, Jean-Pierre Quéré, Christelle Tougard
To cite this version:
Amélie Petitjean, Sophie Montuire, Elodie Renvoisé, Jean-Pierre Quéré, Christelle Tougard. Mito-chondrial DNA Gene Diversity and Morphological Variability of the Common Vole (Microtus arvalis) in France. 10th Rodens and Spatium, the international congress on rodent biology, Jul 2006, Parme, Italy. 2006, pp.104, Hystrix supp. �hal-01925484�
IIntroduction
ntroduction
The common vole (
The common vole (Microtus arvalisMicrotus arvalis, Pallas 1778) is widespread throughout western Europe, from , Pallas 1778) is widespread throughout western Europe, from Atlantic coast of France to central Russia with isolated Iberian popolations (Mitchell-Jones
Atlantic coast of France to central Russia with isolated Iberian popolations (Mitchell-Jones et aet al., 2002; l., 2002; Le Louarn & Quéré, 2003). Genetic structure of this species and colonization processes in Europe were Le Louarn & Quéré, 2003). Genetic structure of this species and colonization processes in Europe were examined by analysing mitochondrial DNA sequences from cytochrome b gene, control region and examined by analysing mitochondrial DNA sequences from cytochrome b gene, control region and nuclear microsatellite loci (Haynes
nuclear microsatellite loci (Haynes et alet al., 2003; Fink ., 2003; Fink et alet al., 2004; Heckel ., 2004; Heckel et alet al., 2005). Five main ., 2005). Five main evolutionary lineages in Europe were defined: Western (W), Central (C), Eastern (E), Italian (I) and evolutionary lineages in Europe were defined: Western (W), Central (C), Eastern (E), Italian (I) and Freiburg (F). Haynes
Freiburg (F). Haynes et alet al. (2003) suggest that there were several glacial refugia, in . (2003) suggest that there were several glacial refugia, in Iberia (W), Italy (I) and the Balkans (C and E). On the other hand, according to Fink Iberia (W), Italy (I) and the Balkans (C and E). On the other hand, according to Fink
et al
et al. (2004) and Heckel . (2004) and Heckel et alet al. (2005), the genetic diversity in populations suggests . (2005), the genetic diversity in populations suggests a glacial survival of the common vole outside the classical refugial areas and a a glacial survival of the common vole outside the classical refugial areas and a potentially more ancient colonization from the northeast to the southwest of Europe. potentially more ancient colonization from the northeast to the southwest of Europe. We investigated the genetic and morphological structure of common vole We investigated the genetic and morphological structure of common vole populations in France from molecular (mitochondrial sequences from the 5' populations in France from molecular (mitochondrial sequences from the 5'
peripheral domain of the control region) and morphometrical (global morphological analyses from teeth) peripheral domain of the control region) and morphometrical (global morphological analyses from teeth) dataset in order to clarify the evolutionary history of the western lineage and its hypothetic implication dataset in order to clarify the evolutionary history of the western lineage and its hypothetic implication in postglacial recolonization of western Europe.
in postglacial recolonization of western Europe.
Fig. 3: Morphometry of the first lower molar of Microtus arvalis. A: with the 27 measurements (occlusal view) and the morphometric index description, n ame and formula (in box; Brunet-Lecomte, 1988; Laplana et al., 2000)); B: centroid projection of 10 populations onto the first two canonical discriminant axes. Circles, surrounding some populations, have no statistical value but are here for your information on population clusters.
Statistical tests performed on our morphometrical dataset are congruent with the Statistical tests performed on our morphometrical dataset are congruent with the clusters presented on Fig. 3:
clusters presented on Fig. 3:
- Mahalanobis distances between populations are all significant (p<0.05). - Mahalanobis distances between populations are all significant (p<0.05). Weakest values are for the Ha/Sa (5.51829, p=0) and Hg/Vi/Do (from 4.94289 to Weakest values are for the Ha/Sa (5.51829, p=0) and Hg/Vi/Do (from 4.94289 to 5.80034, 0.000001<p<0.001641) clusters. Highest values oppose 1) the population 5.80034, 0.000001<p<0.001641) clusters. Highest values oppose 1) the population Ve to those of Ha (14.902216, p=0) and Sa (10.92477, p=0) and 2) the population Ve to those of Ha (14.902216, p=0) and Sa (10.92477, p=0) and 2) the population Au to those of Vo (15.9544, p=0) and Yv (16.27632, p=0);
Au to those of Vo (15.9544, p=0) and Yv (16.27632, p=0);
- the classification matrix enables the reclassifying of populations at more than - the classification matrix enables the reclassifying of populations at more than 60%.
60%.
The morphometric analyses display a morphological structure for m1. It seems The morphometric analyses display a morphological structure for m1. It seems that this morphological structure for some populations is influenced by a climatic that this morphological structure for some populations is influenced by a climatic gradient (continental climate
gradient (continental climate vsvs "pyrenean" climate and altitude "pyrenean" climate and altitude vsvs plain). The plain). The discriminant factor for these populations seem to be the evolutionary stage of the T7 discriminant factor for these populations seem to be the evolutionary stage of the T7 triangle (more or less derived).
triangle (more or less derived).
T6 T7
axis 1 (32.7%)
Ma1 Ma1 Ma2 Ma2 Paris Lille Rennes Poitiers Dijon Toulouse Lyon Marseille Vi Vi Ve Ve Yv Yv VoVo Pb Pb HgHg Au Au Ha Ha Hs Hs Sa Sa He He Ma4 Ma4 Ma5 Ma5 Ma6 Ma6 Ma7 Ma7 Ma8 Ma8 Ma9 Ma9 Do Do Ma10 Ma10 Ma12 Ma12 Ma19 Ma19 Ma195 Ma195 Ma196 Ma196 Ma13 Ma13 Ma14 Ma14 Ma15 Ma15 Ma17 Ma17 Ma18 Ma18 Ma20 Ma20 Ma21 Ma21 Ma22 Ma22 Ma23 Ma23Fig. 2: Maximum-likelihood tree from a fragment (5' peripheral domain; 371 bp) of the control region (GTR+I+Γ8;
lnL=-1745.8923; I=0.2661; α=0.5220). Bayesian approach yielded the same tree topology. Numbers above branches or
at nodes refer to (from left to right) bootstraps (1000 replications) in maximum-likelihood (PhyML) and Bayesian posterior probabilities (MrBayes). The molecular clock hypothesis (Puzzle) was not rejected when tested by likelihood ratio test (2
∆lnL=27.49<χ²=37.65; df=25; p=0.05). Numbers below branches are divergence dates estimated for some population
split (black hexagons), calibrated on the split between Chionomys and Microtus lineages at 1±0.2 Myr (red hexagon;
Chaline, 1987; Nadachowski, 1991). In box, composite stack of many δ18O deep sea core (Imbrie et al., 1984).
High supports are observed for the
High supports are observed for the Microtus arvalisMicrotus arvalis clade. Three groups are clade. Three groups are highly or moderately supported: sub-groups (A1, A2 and A3);
highly or moderately supported: sub-groups (A1, A2 and A3);
- the group B is more geographically structured. It groups together the - the group B is more geographically structured. It groups together the populations Hg, Au, Pb and also one Vo sample. Two sub-groups (B1 and B2) populations Hg, Au, Pb and also one Vo sample. Two sub-groups (B1 and B2) could be identified: B1 (Hg+Au) is moderately supported, whereas B2 (Pb+Vo) is could be identified: B1 (Hg+Au) is moderately supported, whereas B2 (Pb+Vo) is highly supported;
highly supported;
- the group C encompasses AF267285 (Austria) and the third Vo sample. - the group C encompasses AF267285 (Austria) and the third Vo sample.
Populations from Austria belong to the central lineage, whereas populations Populations from Austria belong to the central lineage, whereas populations from France should be included in the western lineage. Samples from Vo are from France should be included in the western lineage. Samples from Vo are distributed in groups A, B and C as well.
distributed in groups A, B and C as well.
Discussion
Discussion
Central Lineage Pb Hg Au Ha Hs Sa Vo Austria Western Lineage 0.20 Myr 0.20 MyrC
C
0.13 Myr 0.13 MyrB
B
A
A
0.12 Myr 0.12 MyrThe influence of Quaternary cold periods on composition and distribution of European fauna and flora is The influence of Quaternary cold periods on composition and distribution of European fauna and flora is unquestioned. Some general trends of postglacial expansions have been identified for several species of plants and unquestioned. Some general trends of postglacial expansions have been identified for several species of plants and animals: 1) postglacial recolonization of northern regions generally from southern peninsulas (Iberia and the animals: 1) postglacial recolonization of northern regions generally from southern peninsulas (Iberia and the Balkans), acting as refugia; 2) isolation of the Italian lineage due to the Alpine barrier; 3) occurrence of 4 main Balkans), acting as refugia; 2) isolation of the Italian lineage due to the Alpine barrier; 3) occurrence of 4 main suture-zones where populations from different refugia meet (Taberlet
suture-zones where populations from different refugia meet (Taberlet et alet al., 1998; Hewitt, 2004). In the case of the ., 1998; Hewitt, 2004). In the case of the common vole, Haynes
common vole, Haynes et alet al. (2003) agree with these general trends of colonization, whereas Fink . (2003) agree with these general trends of colonization, whereas Fink et alet al. (2004) and . (2004) and Heckel
Heckel et alet al. (2005) bring an other vision of its evolutionary history in western Europe.. (2005) bring an other vision of its evolutionary history in western Europe.
Our study brings to the fore a genetic and morphological structure of common vole populations in France. The Vo Our study brings to the fore a genetic and morphological structure of common vole populations in France. The Vo population looks particularly like a part of the second suture-zone as defined by Taberlet
population looks particularly like a part of the second suture-zone as defined by Taberlet et alet al. (1998), between the . (1998), between the central lineage (C) and the western lineage (A and B), but also as a spreading centre for the French populations after central lineage (C) and the western lineage (A and B), but also as a spreading centre for the French populations after the penultimate glaciation (around 0.13 Myr and 0.12 Myr; Fig. 2 and 4). Morphological variability reflects the the penultimate glaciation (around 0.13 Myr and 0.12 Myr; Fig. 2 and 4). Morphological variability reflects the evolutionary stage of the T7 triangle of the m1. In fact, this variability seems more related to an adaptation of the evolutionary stage of the T7 triangle of the m1. In fact, this variability seems more related to an adaptation of the common vole to some "colder" habitats (altitude, "pyrenean" climate) and, especially a diet with more abrasive plants common vole to some "colder" habitats (altitude, "pyrenean" climate) and, especially a diet with more abrasive plants as Graminae (Fig.3). This trend was already mentionned for others vole species (Brunet-Lecomte, 1988).
as Graminae (Fig.3). This trend was already mentionned for others vole species (Brunet-Lecomte, 1988).
In conclusion, our study corroborates the hypothesis of an ancient colonization from northeast to southwest of In conclusion, our study corroborates the hypothesis of an ancient colonization from northeast to southwest of Europe (before 0.20 Myr) and the occurrence of other glacial refugia such as the Vosges area (Vo) in France. The Europe (before 0.20 Myr) and the occurrence of other glacial refugia such as the Vosges area (Vo) in France. The glacial survival of the common vole outside the classical refugial areas is maybe due to its power of adaptation to glacial survival of the common vole outside the classical refugial areas is maybe due to its power of adaptation to colder environments.
colder environments.
Fig. 4: Proposed colonization scenarios for Microtus arvalis in France before and after the penultimate glaciation. Arrows indicate the possible ways of migration. Stars are for the populations mentionned in this study (Vo: Vosges; Hs: Haute Savoie; Sa: Savoie; Ha: Hautes Alpes; Pb: Pays Basque; Hg: Haute Garonne; Au: Aude).
Dataset
Dataset
Our sampling includes 22
Our sampling includes 22 M. arvalisM. arvalis from 8 populations for molecular analyses and 429 first lower from 8 populations for molecular analyses and 429 first lower molars (m1) covering 10 populations for morphometrical analyses (Fig. 1). In molecular analyses, other
molars (m1) covering 10 populations for morphometrical analyses (Fig. 1). In molecular analyses, other MicrotusMicrotus species ( species (M. rossiaemeridionalisM. rossiaemeridionalis, , M. M. ((T.T.)) subterraneus subterraneus
and
and M. M. ((T.T.) ) multiplexmultiplex) were added for phylogenetic reconstructions, as well as ) were added for phylogenetic reconstructions, as well as Chionomys nivalisChionomys nivalis and and Clethrionomys glareolus Clethrionomys glareolus used as outgroups.used as outgroups.
Fig. 1: Distribution of the common vole in France (dark green) and sampling locations (Yv: Yvelines; Vo: Vosges; Do: Doubs; Hs: Haute Savoie; Sa: Savoie; Ha: Hautes Alpes; He: Hérault; Au: Aude; Hg: Haute Garonne; Pb: Pays Basque; Vi: Vienne; Ve: Vendée). Open stars are for morphometric data, whereas filled stars (with sample labels) are for molecular data.
Mitochondrial DNA Gene Diversity and Morphological Variability
of the Common Vole (Microtus arvalis) in France
Amélie Petitjean¹, Sophie Montuire¹², Elodie Renvoisé¹, Jean-Pierre Quéré³ & Christelle Tougard¹*
¹UMR CNRS 5561 Biogéosciences-Dijon, Université de Bourgogne, 6 boulevard Gabriel, 21000 Dijon, France (*Corresponding author: Christelle.Tougard@u-bourgogne.fr)
²Laboratoire Paléobiodiversité et Préhistoire EPHE, Université de Bourgogne
³UMR INRA 1062, Centre de Biologie et Gestion des Populations, Campus International de Baillarguet, 34988 Montferrier-le-Lez cedex
00 -100 -100 -200 -200 -300 -300 -400 -400 -500 -500 -600 -600 -700 -700 -800 -800 T ime (kyr) T ime (kyr) -3 -3 -2-2 -1-1 00 11 22 33 Marine
Marine δδ1818O S.D. StackO S.D. Stack warm warm high high cool cool low low climate climate sea level sea level A A B B C C
Prospects
Prospects
ReferencesBrunet-Lecomte P (1988) Unpublished PhD thesis, Univ. de Bourgogne. Chaline J (1987) Evolutionary Biology, 21: 237-310.
Fink S, Excoffier L, Heckel G (2004) Molecular Ecology, 13: 3501-3514. Haynes S, Jaarola M, Searle J (2003) Molecular Ecology, 12: 951-956.
Heckel G, Burri R, Fink S, Desmet JF, Excoffier L (2005) Evolution, 59: 2231-2242.
Hewitt GM (2004) Philosophical Transactions of the Royal Society of London, B, 359: 183-195.
Imbrie J et al. (1984) in Milankovitch and Climate. Part I (eds Berger AL, Imbrie J, Kukla G, Saltzman B), pp 269-305. D. Reidel Publishing Company.
Laplana C, Montuire S, Brunet-Lecomte P, Chaline J (2000) Geodiversitas, 22: 255-267. Le Louarn H, Quéré JP (2003) Les rongeurs de France. INRA Editions.
Mitchell-Jones AJ et al. (2002) The atlas of European mammals. Poyser Natural History. Nadachowski A (1991) Acta Theriologica, 36: 1-45.
Taberlet P, Fumagalli L, Wust-Saucy AG, Cosson JF (1998) Molecular Ecology, 7: 453-464.
Aknowledgements
We are grateful to Patrick Brunet-Lecomte for providing us with some tissue and tooth samples. This work is a contribution of the team "Différenciation et Espèces" from the UMR CNRS 5561 Biogéosciences-Dijon and EPHE, and to the GDR "Morphométrie et Evolution des Formes".
Indexe description Abbreviated name Formula
Relative length of the anterior part LRPA 100*[(V6-V3)/V6]
T2-T3 labio-lingual asymetry IAT2T3 100*(V26/V27)
T4-T5 labio-lingual asymetry IAT4T5 100*(V24/V21)
Closure of the antérior part BA 100*[(V20V18)/V21]
Length/width ratio V6V21 V6/V21
T6 heigth V10-9 100*[(V10-V9)/V6]
T7 heigth V12-11 100*[(V12-V11)/V6]
Tilt of the anterior part closure V12-10 100*[(V12-V10)/V6]
T6 width V18-17 100*[(V18-V17)/V21]
T7 width V20-19 100*[(V20-V19)/V21]
After this study, at least two prospects of investigation can be conceivable: 1) the 5' peripheral After this study, at least two prospects of investigation can be conceivable: 1) the 5' peripheral domain of the control region is sufficiently variable to extend this parameter in ancient DNA domain of the control region is sufficiently variable to extend this parameter in ancient DNA study and 2) biometric variables, associated with modularity variations, can be used on fossil study and 2) biometric variables, associated with modularity variations, can be used on fossil record of vole m1 to underline shape variations. Both approaches will complete temporally and record of vole m1 to underline shape variations. Both approaches will complete temporally and spatially our understanding of
spatially our understanding of Microtus arvalisMicrotus arvalis migrations and evolutionary history during the migrations and evolutionary history during the last Quaternary glaciations.
