- Research article
- Open Access
The evolutionary radiation of Arvicolinae rodents (voles and lemmings): relative contribution of nuclear and mitochondrial DNA phylogenies
© Galewski et al; licensee BioMed Central Ltd. 2006
Received: 19 May 2006
Accepted: 09 October 2006
Published: 09 October 2006
Mitochondrial and nuclear genes have generally been employed for different purposes in molecular systematics, the former to resolve relationships within recently evolved groups and the latter to investigate phylogenies at a deeper level. In the case of rapid and recent evolutionary radiations, mitochondrial genes like cytochrome b (CYB) are often inefficient for resolving phylogenetic relationships. One of the best examples is illustrated by Arvicolinae rodents (Rodentia; Muridae), the most impressive mammalian radiation of the Northern Hemisphere which produced voles, lemmings and muskrats. Here, we compare the relative contribution of a nuclear marker – the exon 10 of the growth hormone receptor (GHR) gene – to the one of the mitochondrial CYB for inferring phylogenetic relationships among the major lineages of arvicoline rodents.
The analysis of GHR sequences improves the overall resolution of the Arvicolinae phylogeny. Our results show that the Caucasian long-clawed vole (Prometheomys schaposnikowi) is one of the basalmost arvicolines, and confirm that true lemmings (Lemmus) and collared lemmings (Dicrostonyx) are not closely related as suggested by morphology. Red-backed voles (Myodini) are found as the sister-group of a clade encompassing water vole (Arvicola), snow vole (Chionomys), and meadow voles (Microtus and allies). Within the latter, no support is recovered for the generic recognition of Blanfordimys, Lasiopodomys, Neodon, and Phaiomys as suggested by morphology. Comparisons of parameter estimates for branch lengths, base composition, among sites rate heterogeneity, and GTR relative substitution rates indicate that CYB sequences consistently exhibit more heterogeneity among codon positions than GHR. By analyzing the contribution of each codon position to node resolution, we show that the apparent higher efficiency of GHR is due to their third positions. Although we focus on speciation events spanning the last 10 million years (Myr), CYB sequences display highly saturated codon positions contrary to the nuclear exon. Lastly, variable length bootstrap predicts a significant increase in resolution of arvicoline phylogeny through the sequencing of nuclear data in an order of magnitude three to five times greater than the size of GHR exon 10.
Our survey provides a first resolved gene tree for Arvicolinae. The comparison of CYB and GHR phylogenetic efficiency supports recent assertions that nuclear genes are useful for resolving relationships of recently evolved animals. The superiority of nuclear exons may reside both in (i) less heterogeneity among sites, and (ii) the presence of highly informative sites in third codon positions, that evolve rapidly enough to accumulate synapomorphies, but slow enough to avoid substitutional saturation.
During the last decade, molecular phylogenetics based on the comparative analysis of markers from mitochondrial and nuclear genomes allowed for the revision of mammalian systematics [1, 2]. Sequencing efforts initially focused on mitochondrial DNA (mtDNA) due to the availability of conserved primers, the presence of rapidly evolving sites, and a reduced effective population size inducing the rapid fixation of variants between subsequent speciation events. Some protein-coding genes such as cytochrome b [CYB] have emerged as central tools in investigating intraspecific [e.g. [3–6]] to ordinal-level [e.g. [7–9, 6]] evolutionary relationships. To date (January 2006), ca. 5,000 complete CYB entries are available for mammals in public data bases, and furthermore, another mitochondrial gene – the cytochrome c oxidase I – has been proposed as the marker for animal DNA barcoding . However, the strong nucleotide saturation encountered at third codon positions as well as a high sensitivity to taxon sampling soon caused the questioning of the utility of mitochondrial protein-coding genes in general, and CYB in particular for resolving deep phylogenies [11, 12]. Owing to their different evolutionary patterns – a less biased base composition and lower saturation than mitochondrial genes [13, 14] – nuclear genes have represented a reasonable alternative to mtDNA for reconstructing deep-level mammalian phylogenies [[15–21]; but see ]. By providing complementary information, mitochondrial and nuclear genes are thus generally employed at different levels, low-level phylogeny and taxonomy for the former, and deeper-level for the latter.
Several mtDNA-based studies of mammalian systematics have shed light on the difficulties experienced in using CYB to resolve phylogenies at lower taxonomic levels. Several works at the family level recovered multifurcations among genera or even species, which led to the conclusion of rapid, near-simultaneous divergences of multiple lineages (= star-phylogeny), without any time left for synapomorphies to accumulate in mtDNA. This interpretation has been put forward for some speciose clades of rodents, such as Ctenomyidae , Echimyidae , or Sigmodontinae . The star-phylogeny hypothesis was also supported by the lack of resolution for relationships among genera, contrasting with well-defined nodes above and below multifurcations [23, 24, 26]. However, an alternative hypothesis suggests that CYB sequences have undergone substitution saturation throughout the course of speciation events, leading to a loss of the original phylogenetic signal, and producing a soft-polytomy . In this case, the use of slower-evolving nuclear DNA (nuDNA) might represent a better choice for resolving such recent radiations. Supporting this hypothesis, sequences from such markers, either exons or introns, have recently improved among-families [28–30], or even among-genera [31, 32] phylogenetics of spiny rats, squirrels, whales, weasels, and spiral-horn antelopes.
In the present study, we focused on the evolutionary history of voles, lemmings, and muskrats. These animals belong to the Arvicolinae, one of the six Cricetidae subfamilies of the highly-diverse Muroidea, which encompasses one third of all rodent species. The Arvicolinae represent themselves one of the most impressive placental radiations in the Northern Hemisphere, consisting of 151 species and 28 genera . As stated by , the explosiveness and recency of arvicoline evolution can be dramatically highlighted by the more than 60 species of Microtus and the inconsistency of their systematic treatment. Phylogenetic reconstructions based on mitochondrial sequences (CYB and NADH-dehydrogenase 4 [ND4]) provided unresolved topologies at two different levels: (1) among arvicoline genera, and (2) among species of Microtus [34–36]. These results reinforced observations previously made by paleontologists [37, 38] who concluded that two successive pulses of speciation occurred during the evolutionary course of arvicoline rodents over the last 10 million years (Myr).
Following the encouraging results from recent studies [28–32], we thus compared the relative contribution of a nuclear marker – exon 10 of the growth hormone receptor (GHR) gene – to one of the mitochondrial CYB for inferring phylogenetic relationships among major Arvicolinae lineages. We performed analyses in a probability framework because (i) maximum likelihood (ML) and Bayesian methods are indeed based upon explicit models of sequence evolution, (ii) they allow the definition of independent models to reflect the contrasting substitution patterns among the three codon positions of GHR and CYB, and (iii) they have proven to be robust to a number of systematic biases during phylogenetic reconstruction [39–41]. In addition to such inter-sites comparisons, we evaluated the amount of saturation at each codon position. Using the variable-length bootstrap method, we also estimated the amount of sites required by mitochondrial, CYB-like, and nuclear, GHR-like data to resolve recent and deeper nodes of the evolution of voles and lemmings.
Results and discussion
1. Mitochondrial and nuclear phylogenies of the Arvicolinae
(i) Contribution of CYB
(ii) Contribution of GHR exon 10
Branching patterns recovered with ML and Bayesian methods are identical. GHR sequences provide much more resolved topologies (Figure 1B) than those based upon CYB sequences, with eight strongly and four moderately supported nodes. All clades previously identified in the CYB tree are recovered with higher support, excepted for the sister-clade relationship between Microtus arvalis and M. guentheri not found in GHR trees. A better resolution involves all taxonomic levels from internal suprageneric relationships to intra-Microtus nodes (Figure 1B). New, well-supported clades include: (i) the monophyly of the subgenus Alexandromys (Microtus kikuchii, M. oeconomus, and M. middendorffi); (ii) the monophyly of a Microtus sensu lato clade (Neodon, Phaiomys, Blanfordimys, Lasiopodomys, and Microtus) but excluding Chionomys; (iii) the grouping of Arvicola + Chionomys + Microtus s.l.; (iv) the association of Eothenomys with Myodes (= Myodini); and (v) a sister-clade relationship between Myodini and Arvicolini. At the amino acids level, 16 % of the GHR sites are parsimony informative among arvicolines, and the corresponding topology is poorly resolved (three nodes are supported by BPML > 70).
We also scanned the GHR alignment for potential indel signatures. A 3-bp deletion at position 1,925 of the GHR sequence of Rattus norvegicus (Accession number NM_017094) is diagnostic for the monophyly of Arvicolinae. A 3-bp in-frame insertion – a direct AGC repeat – at position 1,778 of Rattus norvegicus (Accession number NM_017094) is shared by Neodon + Phaiomys, and independently by Blanfordimys + Lasiopodomys.
Independent paleontological and molecular studies respectively estimated that divergence times among some arvicoline genera occurred 3–5 Myr ago (Mya)  to 5–9 Mya [30, 34, 42]. The adaptive radiation of Microtus has been dated to approximately 2 Myr by most paleontologists [37, 43] but there is molecular evidence for splits between 2.6 to 4.4 Mya . The GHR topology is here more resolved than the CYB one for intergeneric speciation events, corresponding to mean uncorrected pairwise divergences of 3.8 % ± 0.9 (GHR) versus 14.2 % ± 1.6 (CYB). For the 2–5 Myr old Microtus radiation, corresponding to divergences of 2.2% ± 0.6 (GHR) and 11.7 % ± 1.2 (CYB), the GHR topology is at least as resolved as the CYB one. These results emphasize previous conclusions  that highlighted the superiority of nuclear genes over mitochondrial genes even for divergences spanning the last 5–10 Myr.
(iii) Combination of CYB and GHR genes
Clades moderately to strongly supported in the GHR tree data benefit from similar support values after the combination of GHR and CYB sequences. Actually, a substantial increase of support is found for nodes defining the basal position of Prometheomys, and the monophyly of Microtus s.l. is reinforced. On the opposite, the sister-clade relationship recovered between Myodini and Arvicolini is less supported in the combined tree than in the GHR one. Expectedly, the M. arvalis + M. guentheri clade, recovered by CYB data, is similarly supported in the combination.
To summarize, the combination of CYB and GHR sequences provides a phylogeny where two-third of the nodes benefit from a medium to high support (Figure 2). The addition of nuclear sequences also allows the division of a single, multi-taxa polytomy into two noticeably smaller multifurcations. The first includes Arvicolini, Ondatra, Lemmus, Dicrostonyx, and Phenacomys, although the latter two genera are consistently found as sister-group across the different reconstructions performed. The second multifurcation includes phylogenetic relationships among Microtus s.l. subclades with evidence for a deeper divergence of the Neodon + Phaiomys lineage.
2. Systematics of voles, lemmings, and muskrats
(i) Interrelationships of major genera
For the first time, and contrary to phylogenies based on mitochondrial data alone , the use of a nuclear DNA exon sheds light on the systematics of arvicoline rodents. The validation of the Arvicolini tribe is one of the most striking results. The molecular evidence for a clade including Arvicola, Chionomys, and Microtus s.l. (Figure 2) – with the water vole emerging at first – agrees with paleontology. Actually, the genera Microtus and Chionomys are supposed to be linked to Allophaiomys which represents an early split from the lineage Mimomys that led to Arvicola . Our results concur with other research [45, 46] that red-backed voles form a complex of closely related species as suggested by the strong support recovered for the grouping of Myodes, (i.e., Clethrionomys and Phaulomys sensu ) with Eothenomys.
In addition, a first molecular evidence is here provided for the phylogenetic position of enigmatic genera suspected to have differentiated early within the arvicoline radiation. The long-clawed mole-vole, Prometheomys, currently localised in the Caucasus Mountains, was considered as a relic of an archaic lineage formerly widespread throughout most of Eurasia [33, 48–51]. This view is corroborated by its first emergence in the GHR and combined phylogenetic trees (Figures 1B and 2). The collared lemming, Dicrostonyx as well as the heather vole, Phenacomys, exhibit plesiomorphic morphological traits which have compromised their systematic affiliation to other arvicolines. Dicrostonyx was initially grouped with true lemmings whereas Phenacomys was included in either Arvicolini or Myodini . By obtaining a moderately supported sister-taxa relationship between Dicrostonyx and Phenacomys, our study is in accordance with previous result from the analysis of highly repetitive DNA (LINE-1) elements . Although unexpected, this clade might find a biogeographical explanation as these two taxa are primarily known – from a palaeontological viewpoint – in the Arctic region of Eurasia and North America [37, 53, 54].
To summarize our results from a taxonomic standpoint, the phylogenetic relationships discussed above agree with the tribal recognition of Lemmini (Lemmus), Ondatrini (Ondatra), Dicrostonychini (Dicrostonyx), Phenacomyini (Phenacomys), Prometheomyini (Prometheomys), Myodini (Myodes and Eothenomys) and Arvicolini (Arvicola, Chionomys, Microtus, Neodon, Phaiomys, Blanfordimys, and Lasiopodomys) .
(ii) Systematics of Microtus
Thanks to the sampling of new taxa and nuclear DNA data, our phylograms helped to test the accuracy of systematic treatment of Microtus taxa and close genera. Some taxa – Blanfordimys, Chionomys, Lasiopodomys, Neodon, Phaiomys – have indeed been split from Microtus because they retain distinctive and plesiomorphic morphological/caryological traits . However, except for Chionomys (snow voles), other taxa are interspersed among "true" Microtus lineages in our nuclear or combined topologies, giving no support to their generic recognition.
Actually, three lineages are clearly identified within Microtus. Firstly, strong evidence is provided for a Neodon + Phaiomys subgenera clade, contradicting former studies  which, using molar and other external and cranial contrasts, rejected any close phylogenetic affinity between them. Secondly, Microtus kikuchii, M. oeconomus, and M. middendorffi form a well-supported association. Independent source of phylogenetic data – here nuclear GHR sequences – thus confirm the "Asian lineage" recently identified on the basis of mitochondrial phylogenies and chromosomal data [35, 36, 55], as well as the monophyly of the subgenus Alexandromys, as redefined in . The five nearctic species included in our analysis and representatives of various subgenera (Aulacomys, Mynomes, Pedomys, as well as Microtus longicaudus and M. chrotorrhinus whose systematic status is unclear) are associated with some support in the combined analysis. The recognition of an American clade within Microtus strengthens previous results from biochemical analyses  and mitochondrial phylogenies [35, 36]. Third, some support for a Terricola + Microtus clade is recovered, suggesting close phylogenetic affinities among Western Palaearctic taxa, and reinforcing the conclusions of .
3. Compared molecular evolution of CYB and GHR in arvicolines
(i) Characteristics of substitution patterns
Bayesian estimates of DNA substitution model parameters for CYB, GHR, and their codon positions.
α (Γ 8 )
(ii) Contrasted substitution patterns among codon positions
As generally pointed out for nuclear genes relative to mitochondrial ones, GHR exhibited a less contrasted substitution pattern during its evolutionary course. For instance, more heterogeneity among codon partitions is observed for CYB relative to GHR for two parameter sets. (i) Evolutionary rates – as measured by total branch lengths (TBL) on ML phylograms – are highly heterogeneous among CYB codon positions, with CYB3 (TBL = 58.20) evolving respectively about 24 and 166 times faster than CYB1 (TBL = 2.39), and CYB2 (TBL = 0.35). On the contrary, evolutionary rates are moderately contrasted among GHR codon positions, with GHR3 (TBL = 1.17) evolving three times faster than GHR1 (TBL = 0.41) and GHR2 (TBL = 0.34). (ii) Base composition also appears more heterogeneous among CYB codon positions (Table 1), with 11.7% and 3.8% of G for CYB2 and CYB3 respectively. By contrast, only GHR2 shows such a low value of G (14.6%). An excess of T in CYB2 (41.4%) and A in CYB3 (43.2%) is also noticed. Moreover, all GHR codon positions pass the 1% chi-square test that compares the nucleotide composition of each sequence to the frequency distribution assumed in the ML model, whereas Microtus oeconomus and M.middendorffi CYB third codon positions violate it.
(iii) Partitioned likelihood analyses
Akaike Information Criterion (AIC) sensitivity analyses about the effect of model parameters on log-likelihood gains provided by codon partitions.
Model of DNA evolution
No codon partition
BC + GTR + Γ + BL effect
4. Identification of promising nucleotide sites for arvicoline phylogenetics
Although some studies have elucidated the limited phylogenetic utility of individual nuclear genes at low taxonomic level because of their low variability [29, 32, 57], we provide here a well-resolved GHR tree among Arvicolinae. We will now explore why GHR performs better than CYB for deeper nodes – the inter-generic arvicoline radiation –, and also provides increased support to more recent nodes – the Microtus sublineages.
(i) Localization of the phylogenetic signal among codon positions
Maximum likelihood bootstrap support for a selection of nodes, computed according to codon positions 1, 2, or 3 of CYB and GHR.
Phyllotis + Mesocricetus + Arvicolinae
(ii) Substitution saturation through time
(iii) The efficiency of GHR third codon positions
By comparing contribution to node resolution, saturation level, and evolutionary patterns inherent to each codon partition, it becomes possible to determine the characteristics of informative versus uninformative molecular sites. We thus realize that GHR3 differed from uninformative CYB2, GHR1, and GHR2 partitions by a faster evolution rate (see above, section 3). In contrast, CYB3 and CYB1 partitions are much less informative than GHR3 despite higher evolutionary rates that would have allowed the accumulation of a larger number of synapomorphies. A high substitution rate thus appears detrimental too, having been more likely to have led to saturation (Figure 3). Moreover, strong biases in base composition and GTR substitutions could also favour substitutional saturation. For instance, although CYB1 and GHR3 share similar evolutionary properties (GC levels, Γ shape, GTR rates: Table 1) – CYB1 is more affected by multiple substitutions because of either a slightly higher evolutionary rate or an excess of C-T over A-G transitions. Our study therefore suggests that third codon positions of GHR are the most suitable sites for resolving the recent evolutionary radiation of arvicoline rodents. The higher efficiency of GHR3 is a result of the trade-off in evolutionary rate, rapid enough to accumulate synapomorphies, yet slow enough to remain unaffected by saturation.
5. Perspectives: Which markers to be used for resolving the arvicoline radiation?
The resolved GHR tree is perhaps a first step in challenging the hypothesis of a hard-polytomy for Arvicolinae genera. As shown for other placental taxa – spiral-horn antelopes , hares , or bears  – our results suggest that phylogenetic signal has been progressively obliterated by higher mtDNA rates whereas it has persisted in at least one slower-evolving nuclear gene. However, the GHR gene tree is based on a single nuclear locus (GHR), and it does not necessarily reflect the organismal history of arvicoline rodents. Actually, the resolution of the polytomy is further complicated by the eventual incongruence of individual gene trees with species trees due to incomplete lineage sorting . Consequently, the comparison of multiple gene trees is the only way to get a central tendency which could be interpreted as the species tree [61–63]. If multiple gene trees agree on a phylogenetic structure, we could then definitively dismiss the star-phylogeny hypothesis for the Arvicolinae. In addition to allowing us to make predictions on the amount of CYB/GHR data required to decipher the phylogeny of the Arvicolinae, variable length bootstrap analyses help us to identify which kind of markers should be considered for further sequencing.
(i) The not-so-evil mitochondrial DNA
The lack of phylogenetic signal as well as strong saturation and large among-sites heterogeneity questions the utility of CYB sequences for investigating phylogenetic relationships among taxa, like voles and lemmings, which have experienced relatively recent and rapid radiations. Actually, we concur with others [64, 65] on the usefulness of CYB sequences – including third codon positions – when they are combined with less saturated sequences. Firstly, we have shown that CYB sometimes holds phylogenetic signal for specific nodes where GHR is non-informative (node O, see Results & Discussion, paragraph 1). Although our study mainly focuses on intergeneric phylogenetic relationships, we could expect that CYB contribution would increase with nodes younger than 2 Myr. Secondly, VLB curves clearly indicate that data combination (CYB + GHR) provides slightly higher bootstrap support than does GHR alone, especially when the number of resampled sites is higher than 2,000 (e.g., nodes L and P: Figure 4). Results of VLB analysis and comparisons of GHR and combined topologies show that the CYB signal does not contradict the GHR one. Moreover, the incorporation of CYB data to nuclear data does not lead to the degradation of phylogenetic signal but slightly improves it, revealing the existence of weak and initially hidden information within CYB. Because complete mitochondrial genomes include sequences undergoing various evolutionary pressures (e.g. CYB, but also COX1, or rRNAs), and are available for an increasing number of taxa, particularly among mammals, we suggest the evaluation of their ability to resolve rapid radiations at low taxonomic level , and a comparison of their efficiency to that of nuclear loci.
(ii) The virtues of nuclear DNA
As exemplified in Figure 4, GHR performs better than CYB for most nodes, irrespective of the age of the node. More generally, VLB curves indicate a higher efficiency of GHR relative to CYB sequences for nearly all nodes, i.e., they recover nodes with higher bootstrap support with a lower number of resampled sites. Even for weakly supported nodes in our initial analyses of ca. 1000 GHR sites, only 2,000 to 4,000 GHR additional sites are needed to increase BP values up to 70% or more. We may thus expect a significant improvement in nodal support through the sequencing of nuclear data in an order of magnitude three to five times greater than the size of GHR exon 10. As VLB applies the resampling of sites holding the same phylogenetic signal as GHR, this method may provide conservative predictions on the impact of further sequencing on the overall resolution of the arvicoline phylogenetic tree. By adding nuclear data sampled from different loci, we could expect an improvement in node resolution , in particular for nodes not well-supported by GHR data alone (e.g. nodes P, G). Since genetically independent loci have undergone different substitutional pressures, they may provide complementary resolution of the species tree, and increase the chance of finding molecular synapomorphies that resolve every node [13, 29, 57, 64]. Furthermore, we predict that introns might be equally as efficient for retracing the phylogeny of voles and lemmings – as recently shown for similar recent evolutionary radiations [14, 29, 59] – because of their relaxed substitution constraints and their potentially greater number of informative sites.
Genera and species of Arvicolinae, with cytochrome b (CYB) and Growth Hormon Receptor (GHR) accession numbers and references.
Darwin's leaf-eared mouse
European water vole
European snow vole
Père David's vole
M. (Microtus) arvalis
M. (Aulacomys) chrotorrhinus
M. (Aulacomys) richardsoni
M. (Terricola) duodecimcostatus
Mediterranean pine vole
M. (Microtus) guentheri
M. (Alexandromys) kikuchii
M. (?) longicaudus
M. (Alexandromys) middendorffi
M. (Pedomys) ochrogaster
M. (Alexandromys) oeconomus
M. (Mynomes) pennsylvanicus
Japanese red-backed vole
Chinese scrub vole
P. Giraudoux & J.-P. Quéré
P. Giraudoux & J.-P. Quéré
Western heather vole
Taxonomic sampling and molecular biological methods
Our study is based on a total of 25 arvicoline species representing 14 of the 28 genera and 7 of the 10 tribes according to . For the genus Microtus, we included 12 specimens belonging to different subgenera or species whose taxonomic status is questionable [35, 36] (see Table 1). We used as outgroups, representatives of two lineages phylogenetically close to the Arvicolinae, Mesocricetus auratus (Cricetinae), and Phyllotis darwinii (Sigmodontinae) [42, 71, 30]. Two other taxa belonging to different subfamilies of Muridae, Rattus norvegicus (Murinae) and Meriones sp. (M. shawi + M. unguiculatus; Gerbillinae), were chosen as more distant outgroups.
All ethanol-preserved arvicoline samples were stored in the mammalian tissue collection of the Institut des Sciences de l'Evolution de Montpellier . Total DNA was extracted using the QIAamp DNA mini kit (Qiagen). Part of the GHR exon 10 was amplified and sequenced using the primers GHR5 forward (5' GGCRTTCATGAYAACTACAAACCTGACYTC 3') and GHR6 reverse (5' GAGGAGAGGAACCTTCTTTTTWTCAGGC 3'), and GHR3 forward (5' GACTTTATGCYCARGTRAG 3') and GHR4 reverse (5'-CTYACYTGRGCATAAAAGTC 3'). PCR conditions were 95°C 5 min, followed by 95°C 30 sec, 61°C 30 sec, 72°C 1 min (5 times), then 95°C 30 sec, 59°C 30 sec, 72°C 1 min (5 times), followed by 95°C 30 sec, 57°C 30 sec, 72°C 1 min (5 times), then 95°C 30 sec, 55°C 30 sec, 72°C 1 min (5 times), and then 95°C 30 sec, 53°C 30 sec, 72°C 1 min (20 times), with a final extension at 72°C 5 min.
The amplification and sequencing of the CYB were conducted using primers MVZ05 and MVZ14  and additional internal ones MVZ16  and H8 . PCR products for GHR and CYB were purified from 1% agarose gels using Amicon Ultrafree-DNA columns (Millipore) and sequenced on both strands using automatic sequencing (Big Dye Terminator cycle kit) on an ABI 310 (PE Applied Biosystems).
All taxa included in our study were represented by both CYB and GHR sequences. A 921 bp segment of the exon 10 of GHR was sequenced for 22 specimens and the complete CYB (1140 bp) for 7 specimens. The arvicoline sequences new to this study have been deposited in the EMBL data bank, and we also used previously published sequences when available (see Table 1).
Sequence alignment and phylogenetic analyses
Sequences were manually aligned with the ED editor of the MUST package . Non-sequenced positions as well as introduced gaps were treated as missing data in subsequent analyses. Heterozygotic bases found in GHR sequences were coded following the IUPAC nucleotide ambiguity code.
Phylogenetic analyses of CYB and GHR alignments were conducted under the maximum likelihood (ML) and Bayesian methods, using PAUP*  version 4b10, PHYML  version 2.4.4, and MrBayes version 3.04 . Moreover, MrBayes provided the opportunity to run analyses assuming different models of sequence evolution for each predefined partition, thus permitting the parameters estimated for each model of sequence evolution to be directly compared among codon positions and between genes. When CYB and GHR sequences were combined, sequences from different specimens of the same species were sometimes used. We assumed that the phylogeographic structure detected in some arvicoline species [45, 79] was negligible as compared to the level of genetic divergence between the distinct Microtus subgenera and even arvicoline tribes here compared.
The program Modeltest  version 3.06, was used to determine the sequence evolution model that best fits our data using the Akaike Information Criterion (AIC). This program examined the fit of 56 models, with either a proportion of invariable sites (I), a gamma distribution of among-sites variation of substitution rates (Γ), or both (I + Γ). The best-fitting substitution models were TrN93 + Γ + I  for the GHR data set, and GTR + Γ + I  for the CYB data set. However, to run the same model of sequence evolution under PHYML and MrBayes, GTR was chosen for all phylogenetic analyses (the optimal GHR topology was not model-dependent, as it appeared that both GTR and TrN93 topologies were identical). To allow a fair comparison of α estimates of Γ-shape among genes and partitions, we did not use a proportion of invariable sites, but rather assigned eight discrete Γ categories (Γ8). The Γ distribution allows some sites to evolve at a very low rate, and the incorporation of a fraction of invariable sites does not necessarily lead to a significant increase in likelihood .
To avoid excessive calculation times, our PAUP* ML analyses were conducted in two steps. First, we estimated ML parameters on a neighbor-joining (NJ) starting tree. Second, a ML heuristic search was conducted by Tree Bisection Reconnection (TBR) branch swapping to identify the optimal tree under these constrained GTR + Γ8 parameter estimates. This tree was re-used for a new round of parameter estimation/branch swapping, and the procedure was repeated until there was a stabilization of both topologies and parameters. The stability of nodes was estimated by ML bootstrap percentages (BPML) , computed by PHYML after 100 replicates of site resampling, with BioNJ starting trees. Because of its rapidity, PHYML was preferred over PAUP* for bootstrap analyses. To assess the amount of phylogenetic signal contained within an individual partition (each codon position of each gene), 500 replications of ML bootstrapping were also independently performed for each partition.
Bayesian analyses were performed with one distinct GTR + Γ8 model per gene and codon position, with unlinking base frequencies, GTR, and Γ parameters. Metropolis-Coupled Markov chain Monte Carlo (MCMCMC) sampling was conducted during 10,000,000 generations with five incrementally heated chains. We used Dirichlet priors for base frequencies (1,1,1,1) and for GTR parameters (1,1,1,1,1) scaled to the G-T rate, a Uniform(0.05,50.00) prior for the Γ shape, and an Exponential(10.0) prior for branch lengths. Bayesian posterior probabilities (PP) were computed from trees sampled every 100 generations, after removing the 50,000 first trees as the "burn-in" stage. In order to discriminate between moderately and strongly supported nodes – for which initial PP were superior to 0.95 – we also calculated bootstrapped Bayesian posterior probabilities (BPbay) as suggested by  and . Due to computing time limitations, BPbay were only computed for the combined data set (GHR + CYB). First, 100 bootstrap pseudo-replicates were independently generated from each of the six partitions (the three CYB and the three GHR codon positions) using the SEQBOOT program 3.6a2.1  of the PHYLIP package. Second, for each of the 100 concatenated bootstrap data sets, MCMCMC sampling of trees was performed as previously described for the original data under the six GTR + Γ8 partitioned model, except that trees were sampled every 100 generations for only 500,000 generations. To maximize the probability that the chains reached stationarity in each bootstrap replicate, one-half of the 5,000 trees sampled from the posterior probability distribution was systematically removed as the burnin . BPbay resulted from the overall 50% majority rule consensus of the 500,000 saved trees.
Following , sequences were also analyzed at the amino-acid level. We respectively used the JTT + Γ + I and mtREV + Γ + I ML models of protein evolution for GHR and CYB sequences as implemented in PHYML.
We performed sensitivity analyses using PAUP* to assess the relative contribution of the various model parameters to the log-likelihood increase when more complex models are considered. To take the evolutionary properties of each codon position into account, nucleotide sites were categorized into each of the three codon positions. The procedure was conducted separately for CYB and GHR sequences. All sets of parameters – base composition (BC), substitution rate matrix (GTR), heterogeneity of substitution rate among sites (Γ), and branch lengths (BL) – were estimated independently for each codon partition. AIC values were compared to assess the significance of likelihood variation between global and partitioned models. For instance, to test the contribution of BC, only BC parameters were computed for each partition whereas other parameter values (GTR, Γ, BL) were fixed for the whole gene.
Evaluation of the saturation of nucleotide substitutions
The nucleotide saturation of the phylogenetic markers was assessed graphically according to the procedure of , by plotting the number of observed differences as a function of the ML inferred number of substitutions for all 351 pairwise comparisons for 27 sequences (the partial CYB sequence of Lasiopodomys mandarinus was removed). The inferred number of substitutions was estimated from the ML tree as the sum of the branch lengths linking two terminals. The level of saturation was estimated by the slope (S) of the linear regression between the observed and inferred substitutions. Substitutions saturation is evidenced when the number of inferred substitutions increased, whereas the number of observed differences remained constant. We performed saturation analyses independently for each phylogenetic marker and for each codon position. ML branch lengths were obtained for each partition using PAUP* and by enforcing the topology as identical to the combined CYB + GHR tree.
Variable Length Bootstrap
To compare the phylogenetic resolving power of GHR and CYB at varying taxonomic levels, we used the variable-length bootstrap (VLB). In this method, bootstrap support is estimated as a function of a variable number of resampled characters . For each data set, nucleotide sites were resampled to generate bootstrap pseudomatrices of 100, 250, and until 5000 characters with increasing steps of 250 sites. All bootstrap searches were then performed using ML analyses with PAUP*.
The authors wish to thank Francois Catzeflis who provided most of tissue samples for this study, Pierre-André Crochet, David Duneau and Johan R. Michaux who also contributed to increase our taxa set, Patrick Giraudoux, Jean-Pierre Quéré, and the European "Human cystic and alveolar echinococcosis in northwest China" STD TS3-CT94-0270 and National Institute of Health and National Science Fondation (USA) "Parasitic zoonosis transmission in China"IR01TW01565-01 programs for some precious samples of Chinese voles. TG acknowledges the financial support of a MENRT Doctoral grant. This work has also been supported by the "Institut Français de la Biodiversité", the "ACI Informatique-Mathématique-Physique en Biologie Moléculaire [ACI IMP-Bio]", the IFR119 "Biodiversité Continentale Méditerranéenne et Tropicale" (Montpellier), and benefited from discussions around the European Marie Curie project HOTSPOTS "Understanding and Conserving Earth Biodiversity" (contract MEST-CT-2005-020561). The authors wish to thank Andrew Rodrigues for his help, and two anonymous reviewers whose comments and suggestions greatly improved the paper. This publication is the contribution N° 2006-057 of the Institut des Sciences de l'Evolution de Montpellier (UMR 5554 – CNRS).
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