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New insight into the colonization processes of common voles: inferences from molecular and fossil evidence.

Tougard C, Renvoisé E, Petitjean A, Quéré JP - PLoS ONE (2008)

Bottom Line: Elucidating the colonization processes associated with Quaternary climatic cycles is important in order to understand the distribution of biodiversity and the evolutionary potential of temperate plant and animal species.Species can experience heterogeneous evolutionary histories over their geographic range.Multidisciplinary approaches should therefore be preferentially chosen in prospective studies, the better to understand the impact of climatic change on past and present biodiversity.

View Article: PubMed Central - PubMed

Affiliation: UMR CNRS/uB 5561 Biogéosciences-Dijon, Université de Bourgogne, Dijon, France. Christelle.Tougard@univ-montp2.fr

ABSTRACT
Elucidating the colonization processes associated with Quaternary climatic cycles is important in order to understand the distribution of biodiversity and the evolutionary potential of temperate plant and animal species. In Europe, general evolutionary scenarios have been defined from genetic evidence. Recently, these scenarios have been challenged with genetic as well as fossil data. The origins of the modern distributions of most temperate plant and animal species could predate the Last Glacial Maximum. The glacial survival of such populations may have occurred in either southern (Mediterranean regions) and/or northern (Carpathians) refugia. Here, a phylogeographic analysis of a widespread European small mammal (Microtus arvalis) is conducted with a multidisciplinary approach. Genetic, fossil and ecological traits are used to assess the evolutionary history of this vole. Regardless of whether the European distribution of the five previously identified evolutionary lineages is corroborated, this combined analysis brings to light several colonization processes of M. arvalis. The species' dispersal was relatively gradual with glacial survival in small favourable habitats in Western Europe (from Germany to Spain) while in the rest of Europe, because of periglacial conditions, dispersal was less regular with bottleneck events followed by postglacial expansions. Our study demonstrates that the evolutionary history of European temperate small mammals is indeed much more complex than previously suggested. Species can experience heterogeneous evolutionary histories over their geographic range. Multidisciplinary approaches should therefore be preferentially chosen in prospective studies, the better to understand the impact of climatic change on past and present biodiversity.

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Estimated expansions of Microtus arvalis before (A), during (B) and after (C) the LGM.The black star locates the most likely origin of the species from fossil and genetic evidence. Solid arrows indicate the southwestward and northeastward gradual range expansion during warm periods, while dotted arrows are for more or less irregular expansion (Ù glacial survival in isolated populations or ä bottleneck events) during cold periods. Shaded areas (B) correspond to the estimated extension of ice cover.
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pone-0003532-g005: Estimated expansions of Microtus arvalis before (A), during (B) and after (C) the LGM.The black star locates the most likely origin of the species from fossil and genetic evidence. Solid arrows indicate the southwestward and northeastward gradual range expansion during warm periods, while dotted arrows are for more or less irregular expansion (Ù glacial survival in isolated populations or ä bottleneck events) during cold periods. Shaded areas (B) correspond to the estimated extension of ice cover.

Mentions: The phylogeographic history of the common vole is characterized by a deep genetic differentiation of the five main evolutionary lineages (Western, Freiburg, Central, Eastern and Italian; Figures 2 and 4). Similarities with phylogeographic patterns of M. arvalis data from several genetic markers (cytb, CR, microsatellites) [33], [34], as well as data from other temperate species [3], [13], [42]–[45] suggest that the distribution of populations between Western and Eastern Europe reflects the evolutionary history of populations rather than genetic marker genealogy. Molecular dating indicates that the population divergence, from the lineage origin to the origin of the Spanish clade of M. arvalis, occurred during the Middle and Late Pleistocene (0.475–0.086 Myr), and thus predated the LGM widely. These molecular dating results coincide with warm or pre- and postglacial periods between the Late Cromerian and the LGM (Figure 4). The C and E lineages have a shallow regional genetic structure. Low nucleotide diversity (0.53% and 0.62%, respectively), star-like topologies (Figure 2) and analyses of demographic history indicating sudden expansion (Figure 3) provide evidence for a past bottleneck event followed by probable post-LGM population expansion [45]–[47]. The oldest major W lineage presents a higher level of nucleotide diversity (1.31%) suggestive of relatively large population sizes, and shows a hierarchical phylogeographic structure (NE and SW sublineages) as observed in the field vole [43]. However, these sublineages found on either side of the Loire River (France) also have different topological tree structures, reflecting different genetic structures (Table 1). The NE sublineage experienced to a lesser extent the effect of periglacial climatic conditions, while the SW populations located between the Atlantic and Mediterranean coasts were under milder climatic conditions (Figures 2, 5 and S1). The closer the populations were to the ice front, the more significant was the loss of genetic diversity.


New insight into the colonization processes of common voles: inferences from molecular and fossil evidence.

Tougard C, Renvoisé E, Petitjean A, Quéré JP - PLoS ONE (2008)

Estimated expansions of Microtus arvalis before (A), during (B) and after (C) the LGM.The black star locates the most likely origin of the species from fossil and genetic evidence. Solid arrows indicate the southwestward and northeastward gradual range expansion during warm periods, while dotted arrows are for more or less irregular expansion (Ù glacial survival in isolated populations or ä bottleneck events) during cold periods. Shaded areas (B) correspond to the estimated extension of ice cover.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2570793&req=5

pone-0003532-g005: Estimated expansions of Microtus arvalis before (A), during (B) and after (C) the LGM.The black star locates the most likely origin of the species from fossil and genetic evidence. Solid arrows indicate the southwestward and northeastward gradual range expansion during warm periods, while dotted arrows are for more or less irregular expansion (Ù glacial survival in isolated populations or ä bottleneck events) during cold periods. Shaded areas (B) correspond to the estimated extension of ice cover.
Mentions: The phylogeographic history of the common vole is characterized by a deep genetic differentiation of the five main evolutionary lineages (Western, Freiburg, Central, Eastern and Italian; Figures 2 and 4). Similarities with phylogeographic patterns of M. arvalis data from several genetic markers (cytb, CR, microsatellites) [33], [34], as well as data from other temperate species [3], [13], [42]–[45] suggest that the distribution of populations between Western and Eastern Europe reflects the evolutionary history of populations rather than genetic marker genealogy. Molecular dating indicates that the population divergence, from the lineage origin to the origin of the Spanish clade of M. arvalis, occurred during the Middle and Late Pleistocene (0.475–0.086 Myr), and thus predated the LGM widely. These molecular dating results coincide with warm or pre- and postglacial periods between the Late Cromerian and the LGM (Figure 4). The C and E lineages have a shallow regional genetic structure. Low nucleotide diversity (0.53% and 0.62%, respectively), star-like topologies (Figure 2) and analyses of demographic history indicating sudden expansion (Figure 3) provide evidence for a past bottleneck event followed by probable post-LGM population expansion [45]–[47]. The oldest major W lineage presents a higher level of nucleotide diversity (1.31%) suggestive of relatively large population sizes, and shows a hierarchical phylogeographic structure (NE and SW sublineages) as observed in the field vole [43]. However, these sublineages found on either side of the Loire River (France) also have different topological tree structures, reflecting different genetic structures (Table 1). The NE sublineage experienced to a lesser extent the effect of periglacial climatic conditions, while the SW populations located between the Atlantic and Mediterranean coasts were under milder climatic conditions (Figures 2, 5 and S1). The closer the populations were to the ice front, the more significant was the loss of genetic diversity.

Bottom Line: Elucidating the colonization processes associated with Quaternary climatic cycles is important in order to understand the distribution of biodiversity and the evolutionary potential of temperate plant and animal species.Species can experience heterogeneous evolutionary histories over their geographic range.Multidisciplinary approaches should therefore be preferentially chosen in prospective studies, the better to understand the impact of climatic change on past and present biodiversity.

View Article: PubMed Central - PubMed

Affiliation: UMR CNRS/uB 5561 Biogéosciences-Dijon, Université de Bourgogne, Dijon, France. Christelle.Tougard@univ-montp2.fr

ABSTRACT
Elucidating the colonization processes associated with Quaternary climatic cycles is important in order to understand the distribution of biodiversity and the evolutionary potential of temperate plant and animal species. In Europe, general evolutionary scenarios have been defined from genetic evidence. Recently, these scenarios have been challenged with genetic as well as fossil data. The origins of the modern distributions of most temperate plant and animal species could predate the Last Glacial Maximum. The glacial survival of such populations may have occurred in either southern (Mediterranean regions) and/or northern (Carpathians) refugia. Here, a phylogeographic analysis of a widespread European small mammal (Microtus arvalis) is conducted with a multidisciplinary approach. Genetic, fossil and ecological traits are used to assess the evolutionary history of this vole. Regardless of whether the European distribution of the five previously identified evolutionary lineages is corroborated, this combined analysis brings to light several colonization processes of M. arvalis. The species' dispersal was relatively gradual with glacial survival in small favourable habitats in Western Europe (from Germany to Spain) while in the rest of Europe, because of periglacial conditions, dispersal was less regular with bottleneck events followed by postglacial expansions. Our study demonstrates that the evolutionary history of European temperate small mammals is indeed much more complex than previously suggested. Species can experience heterogeneous evolutionary histories over their geographic range. Multidisciplinary approaches should therefore be preferentially chosen in prospective studies, the better to understand the impact of climatic change on past and present biodiversity.

Show MeSH
Related in: MedlinePlus