Mitochondrial Phylogeny of Arvicolinae Using Comprehensive Taxonomic Sampling Yields New Insights

Biological Journal of the Linnean Society, 2008, 94, 825–835. With 2 ﬁgures

Mitochondrial phylogeny of Arvicolinae using comprehensive taxonomic sampling yields new insights

ELENA V. BUZAN1*, BORIS KRYSTUFEK1*, BERND HÄNFLING2 and 2

WILLIAM F. HUTCHINSON Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021

1University of Primorska, Science and Research Centre of Koper, Garibaldijeva 1, 6000 Koper, Slovenia 2Molecular Ecology and Fisheries Genetics Laboratory, Department of Biological Sciences, University of Hull, Hull HU6 7RX, UK

Received 16 July 2007; accepted for publication 11 October 2007

Comprehensive taxonomic sampling can vastly improve the accuracy of phylogenetic reconstruction. Here, we present the most inclusive phylogenetic analysis of Arvicolinae (Mammalia, Rodentia) to date, combining all published cytochrome b gene sequences of greater than 1097 bp and new sequences from two monotypic genera. Overall, the phylogenetic relationships between 69 species of voles and lemmings, representing 18 genera and 10 tribes, were studied. By applying powerful modern approaches to phylogenetic reconstruction, such as maximum likelihood and Bayesian analysis, we provide new information on the early pulse of evolution within the Arvicolinae. While the position of two highly divergent lineages, Phenacomys and Ondatra, could not be resolved, the tribe Lemmini, appeared as the most basal group of voles. The collared lemmings (Dicrostonychini) grouped together with all of the remaining tribes. The two previously unstudied monotypic genera Dinaromys and Prometheomys form a moderately well-supported monophyletic clade, possibly a sister group to Ellobius (Ello- biusini). Furthermore, with one exception, all tribes (sensu Musser & Carleton, 2005) proved to be monophyletic and can thus be regarded as meaningful evolutionary entities. Only the tribe Arvicolini emerged as paraphyletic in both analyses because of the unresolved phylogenetic position of Arvicola terrestris. Steppe voles of the genus Lagurus were solidly supported as a sister group to the Microtus and allies clade. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 825–835.

ADDITIONAL KEYWORDS: Arvicolinae early radiation – Arvicolinae tribes – cytochrome b gene – Dinaromys – molecular phylogeny.

INTRODUCTION 1999; Martin et al., 2000; Michaux, Reyes & Catzeflis, 2001; Jaarola et al., 2004) and a synthesis of these Voles and lemmings (subfamily Arvicolinae) are a independent sets of evidence (Chaline & Graf, 1988; prolific and species-rich monophyletic group of muroid Musser & Carleton, 2005). Current taxonomic rich- rodents (Muroidea) that dominate grassland and ness in the subfamily presumably results from two Arctic habitats throughout the Holarctic (Musser & main pulses of radiation: an early pulse during the Carleton, 2005; Shenbrot & Krasnov, 2005). Phyloge- Miocene that gave rise to tribes and a more recent netic reconstructions of arvicolines were initially radiation leading to the species richness of prolific based on morphology, with adjustments being made genera such as Microtus and Myodes (Chaline et al., as new data became available from fossil evidence 1999; Conroy & Cook, 1999; Musser & Carleton, (Gromov & Ya Polyakov, 1992; Chaline et al., 1999), 2005). Because of irresolvable polytomies disclosed in molecular markers (Modi, 1996; Conroy & Cook, phylogenetic evaluation of mitochondrial DNA (Conroy & Cook, 1999) and the lack of fossil evidence *Corresponding author. E-mail: [email protected], prior to the early Pliocene (Musser & Carleton, 2005), [email protected] suprageneric relationships and consequently the

© 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 825–835 825 826 E. V. BUZAN ET AL. number of tribes within the subfamily remains sequences of the largely complete mitochondrial controversial (Musser & Carleton, 2005; Shenbrot & cytochrome b (cyt b) gene representing all arvicoline Krasnov, 2005). Phylogenetic reconstructions are tribes. By combining published data from previous further biased by a lack of genetic data for several studies, which ensured broad multispecies represen- monotypic and presumably primitive genera with tation of the various tribes, with new cyt b sequences small geographical ranges. of the genus Dinaromys, presumably the only surviv- Two such genera, Prometheomys and Dinaromys, ing member of Pliomyini tribe (Musser & Carleton, show no clear morphological affinities to any living 2005), and applying a powerful Bayesian approach to arvicoline genus. While their relative isolation within phylogenetic reconstruction, we provide new infor- the Arvicolinae is generally accepted (Gromov & Ya mation on the early pulse of evolution within the Polyakov, 1992; Musser & Carleton, 2005), their phy- Arvicolinae. Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 logenetic position has remained controversial because of inconclusive fossil evidence and missing molecular data. Thus, based on morphological data, Prome- MATERIAL AND METHODS theomys was classified together with Ellobius into a SAMPLES separate subfamily Prometheomyinae by Repenning, Radiation within arvicoline rodents was assessed Fejfar & Heinrich (1990), but it was later placed into using sequences from 69 species across 18 genera a tribe of its own, Prometheomyini, by most authors (Table 1), representing 10 out of the 11 recognized (Gromov & Ya Polyakov, 1992; Pavlinov & Rossolimo, arvicoline tribes (Musser & Carleton, 2005). As our 1998; Musser & Carleton, 2005; Shenbrot & Krasnov, aim was to address the early radiation pulse within 2005). Dinaromys bogdanovi was first described as a the Arvicolinae (Conroy & Cook, 1999), a subset of member of the snow voles (Chionomys; Martino & species was chosen for the in-group in order to rep- Martino, 1922), but was subsequently transferred resent all major deep lineages identified in previous into the fossil genus Dolomys by Hinton (1926). phylogenetic studies. In addition to sequences down- Hinton (1926) believed that Dolomys, which also loaded from GenBank, we sequenced cyt b gene for included the fossil Pliomys, was ancestral to the two monospecific genera: Dinaromys bogdanovi (Mt Mimomys lineage, a fossil group of voles with rooted Zelengora, Bosnia and Herzegovina) and Prome- molars that gradually evolved into Arvicola during theomys schaposchnikowi (Cam Gecidi near Ardahan, the Pleistocene (Kowalski, 2001). Kretzoi (1955) allo- Turkey). Cricetulus barabensis (formerly C. griseus) cated Dinaromys bogdanovi, a genus in its own right, from the subfamily Cricetinae and Peromyscus truei and placed Dinaromys, along with Pliomys and from the subfamily Neotominae (previously Sigmo- Dolomys, into the arvicoline tribe Ondatrini, with its dontinae), the possible sister groups to Arvicolinae nearest living relative in the Nearctic Ondatra zibe- (Michaux, Reyes & Catzeflis, 2001), were used as thicus. However, Dinaromys was more frequently out-groups. regarded to be in the tribe Myoidini (formerly Clethri- onomyini; Kowalski, 2001), although because of simi- larities with the fossil genus Pliomys (Koenigswald, DNA EXTRACTION, PCR AMPLIFICATION 1980) in the microstructure of molar enamel, Din- AND SEQUENCING aromys was recently shifted into the tribe Pliomyini A2¥ 2 mm fragment of ethanol preserved tissue (Musser & Carleton, 2005). was air dried in sterile conditions to remove the A recent study of Galewski et al. (2006) provided ethanol and the DNA extracted using a ’Wizard(r) the first attempt to include information from nuclear Genomic DNA Purification Kit’ (Promega; D. genes into a phylogenetic reconstruction of Arvicoli- bogdanovi) or QIAamp(r) DNA Mini Kit (QIAgen; nae and to assess the phylogenetic position of Prome- P. schaposchnikowi). theomys. While the power of this analysis benefited Two overlapping cyt b fragments of 623 bp and from the inclusion of two independent genes (nuclear 772 bp were amplified from the D. bogdanovi sample, and mitochondrial) and thus significantly advanced using mammalian universal primers L14724B and our knowledge of the general structure of Arvicolinae, H15149, and L14841 and H15915 (Irwin, Kocher & it was restricted by a relatively limited taxonomic Wilson, 1991). The alignment of these fragments was sampling. Such incomplete sampling not only limits used to design D. bogdanovi-specific primers, which the possibility to assess the monophyly of certain amplified three small overlapping cyt b fragments lineages but can also create serious problems for (150–200 bp), for a related study using museum skins phylogenetic reconstruction through what is known (Krystufek et al., 2007). As the universal primers as ’long branch attraction’ (Baldauf, 2003). yielded a weak amplification with the P. schaposchni- The aim of this paper was therefore to reconstruct kowi sample, the D. bogdanovi-specific primers were the phylogeny of Arvicolinae using all published vole used to amplify a problematic central section of the

Table 1. Species included in the phylogenetic analysis. Tribal division follows Musser & Carleton (2005)

Reference number Species Arvicoline tribe in GenBank Source

Dinaromys bogdanovi Pliomyini EU190891 This study Prometheomys schaposchnikowi Prometheomyini EU190892 This study Ellobius tancrei Ellobiusini AF119270 Conroy & Cook (1999) Ellobius fuscocapillus Ellobiusini AF126430 Conroy & Cook (1999) Ondatra zibethicus Ondantrini AF119277 Conroy & Cook (1999)

Myodes glareolus Myodini AY309421 Cook, Runck & Conroy (2004) Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 Myodes rutilus Myoidini AY513845 Jaarola et al. (2004) Myodes rufucanus Myoidini AY309418 Cook (2004) Myodes gapperi Myoidini DQ323950 Triant & DeWoody (2008) Myodes smithii Myoidini AB104508 Iwasa & Suzuki (2003) Alticola macrotis Myoidini AY309411 Cook (2004) Eothenomys melanogaster Myoidini AY426681 Luo et al. (2004) Eothenomys miletus Myoidini DQ981395 Liu & Wang in rewiew Arvicola terrestris Arvicolini AF119269 Conroy & Cook (1999) Microtus arvalis Arvicolini AY220766 Haynes, Jaarola & Searle (2003) Microtus levis Arvicolini AY513821 Jaarola et al. (2004) Microtus subterraneus Arvicolini AY513832 Jaarola et al. (2004) Microtus agrestis Arvicolini AY167187 Jaarola & Searle (2002) Microtus chrotorrhinus Arvicolini DQ323938 Triant & DeWoody (2008) Microtus abbreviatus Arvicolini DQ323935 Triant & DeWoody (2008) Microtus californicus Arvicolini DQ323937 Triant & DeWoody (2008) Microtus daghestanicus Arvicolini AY513792 Jaarola et al. (2004) Microtus dogramacii Arvicolini AY513795 Jaarola et al. (2004) Microtus duodecimcostatus Arvicolini AM392400 Galewski et al. (2006) Microtus felteni Arvicolini AY513798 Jaarola et al. (2004) Microtus gerbei Arvicolini AY513802 Jaarola et al. (2004) Microtus gregalis Arvicolini AY513803 Jaarola et al. (2004) Microtus guatemalensis Arvicolini AF410262 Conroy et al. (2001) Microtus guentheri Arvicolini AY513807 Jaarola et al. (2004) Microtus kikuchii Arvicolini DQ323939 Triant & DeWoody (2008) Microtus kirgisorum Arvicolini AY513810 Jaarola et al. (2004) Microtus liechtensteini Arvicolini AY513811 Jaarola et al. (2004) Microtus longicaudatus Arvicolini AF187230 Conroy & Cook (2000) Microtus lusitanicus Arvicolini AY513813 Jaarola et al. (2004) Microtus majori Arvicolini DQ841704 Martinkova et al. (2007) Microtus miurus Arvicolini DQ323941 Triant & DeWoody (2008) Microtus mexicanus Arvicolini DQ323940 Triant & DeWoody (2008) Microtus middendorffii Arvicolini AF163898 Conroy & Cook (2000) Microtus montebelli Arvicolini AF163900 Conroy & Cook (2000) Microtus multiplex Arvicolini AY513818 Jaarola et al. (2004) Microtus oaxacensis Arvicolini AF410260 Conroy et al. (2001) Microtus pinetorum Arvicolini DQ323947 Triant & DeWoody (2008) Microtus oeconomus Arvicolini DQ452142 Brunhoff et al. (2006) Microtus pyrenaicus Arvicolini AJ972916 Tougard et al. in review Microtus richardsoni Arvicolini AF163905 Conroy & Cook (2000) Microtus thomasi Arvicolini AY513844 Jaarola et al. (2004) Microtus tatricus Arvicolini DQ841702 Martinkova et al. (2007) Microtus townsendii Arvicolini DQ323948 Triant & DeWoody (2008) Microtus socialis Arvicolini AY513831 Jaarola et al. (2004) Microtus savii Arvicolini AY513828 Jaarola et al. (2004) Microtus xanthognathus Arvicolini DQ323949 Triant & DeWoody (2008) Microtus quasiater Arvicolini AF410259 Conroy et al. (2001) Microtus umbrosus Arvicolini AF410261 Conroy et al. (2001)

Table 1. Continued

Reference number Species Arvicoline tribe in GenBank Source

Microtus pennsylvanicus Arvicolini DQ323946 Triant & DeWoody (2008) Microtus oregoni Arvicolini DQ323945 Triant & DeWoody (2008) Microtus ochrogaster Arvicolini DQ432008 Triant & DeWoody (2008) Chionomys nivalis Arvicolini AY513845 Jaarola et al. (2004) Chionomys roberti Arvicolini AY513851 Jaarola et al. (2004)

Blanfordimys bucharensis Arvicolini AM392369 Galewski et al. (2006) Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 Neodon irene Arvicolini AM392370 Galewski et al. (2006) Neodon juldaschi Arvicolini AY513808 Jaarola et al. (2004) Lagurus lagurus Lagurini AF429818 Dekonenko et al. (2003) Dicrostonyx groenlandicus Dicrostonychini AF119268 Conroy & Cook (1999) Dicrostonyx torquatus Dicrostonychini AF119275 Conroy & Cook (1999) Lemmus trimucronatus Lemmini AF119276 Conroy & Cook (1999) Myopus schisticolor Lemmini AF119263 Conroy & Cook (1999) Synaptomys borealis Lemmini AF119259 Conroy & Cook (1999) Synaptomys cooperi Lemmini DQ323957 Triant & DeWoody (2008) Phenacomys intermedius Phenacomyini AF119260 Conroy & Cook (1999) Cricetulus barabensis Cricetinae AB033693 Suzuki, Tsuchiya & Takezaki (2000) Peromyscus truei Peromyscini AF108703 Smith & Patton (1999) cyt b gene for this sample. The resulting products, (version 4.0; Thompson et al., 1997) implemented in totalling 555 bp, were aligned with the two fragments the MEGA package (version 4.0, Tamura et al., 2007) ampliﬁed using the ’universal’ primers. The align- in combination with Bioedit (version 7.09; Hall, 2004). ment of these fragments yielded high-quality Nucleotide and amino acid composition was analysed sequence data for the entire cyt b gene (1143 bp). using the program MEGA. The total number of base Ampliﬁcation of the larger DNA fragments was frequencies in each position was estimated with the performed using a 10 mL reaction volume containing program DAMBE (version 4.2.13, Xia, 2000; Xia &

2.5 mM MgCl2, 0.5 mM of forward and reverse primer, Xie, 2001). 0.25 mM of dNTPs and 1 unit of Bioline Taq, in the supplied ammonium buffer. Cycling conditions included an initial stage of 95 °C for 5 min, followed PHYLOGENETIC ANALYSIS by 40 cycles of denaturation (40 s at 94 °C), primer Phylogentic relationships were reconstructed using annealing (40 s at 48 °C) and extension (1 min at maximum likelihood (ML) methods and Bayesian (BI) 72 °C). Ampliﬁcation of the short fragments (c. 150– analyses. The Akaike Information Criterion (AIC), 200 bp) was performed using a 20 mL reaction volume hierarchical likelihood ratio test (hLRT) and Bayesian containing 2.5 mM MgCl2,50mM KCl, 0.3 mM of Information criterion (BIC) implemented in the forward and reverse primer, 0.25 mM of dNTPs and program Modeltest 3.7 (Posada & Crandall, 1998) 3 units of Bioline Taq in the supplied buffer. Cycling were used to identify the most appropriate model of conditions included an initial stage of 95 °C for 5 min, DNA substitution for the data. The model selected by followed by 40 cycles of denaturation (40 s at 94 °C), all three approaches was the general time reversible primer annealing (10 cycles at 52 °C, 10 cycles at model with gamma distributed shape parameter and 51 °C and 20 cycles at 50 °C, each for 40 s), and DNA used the proportion of invariable sites (GTR + G + I). extension (1 min at 72 °C). Sequencing was performed Genetic distances among arvicoline genera estimated on a Beckman Coulter multicapillary sequencer using under a K2P model were calculated by PAUP their DTCS Quick Start Sequencing kit. (version 4.0b10; Swofford, 2002). The ML tree was constructed using the GTR + G + I substitution model, in which the parameters were SEQUENCE ANALYSES estimated using the software PhyML (version 2.4.4; The program CodonCode Aligner (version 1.63; Ewing Guindon & Gascuel, 2003). Branch support of the et al., 1998) was used to align forward and reverse ML tree was inferred using the non-parametric sequences. The resulting consensus sequences for Shimodaira–Hasegawa-like (SH) aLRT provided by each individual were aligned using ClustalW PhyML (Anisimova & Gascuel, 2006). The SH-aLRT

© 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 825–835 PHYLOGENY OF ARVICOLINAE 829 procedure is conservative and thus we considered values of > 90% as a cut-off value to indicate a ‘good’ support and 80–90% as ‘moderate’ support. The program MrBayes (version 3.1; Huelsenbeck & Ronquist, 2001) was used to apply a Bayesian approach to phylogenetic reconstruction (Rannala & Yang, 1996; Yang & Rannala, 1997; Mau, Newton & Larget, 1999). The GTR + G + I distribution model of DNA substitution was used with the Markov chain started from a random tree with random branch lengths. Four Markov Chain Monte Carlo (MCMC) Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 chains were run simultaneously for 4 million generations, with the resulting trees sampled at every hundred generations (saving 40 000 trees). The ﬁrst 10 000 trees were discarded as a conservative measure to avoid the possibility of including random, suboptional trees. The remaining results were used to compute a 50% majority rule consensus tree. Baye- sian posterior probabilities (BPP) were used to assess branch support of the BI tree. Given the liberal nature of this procedure we consider, in line with other authors, a BPP > 0.95 as ’good’ and 0.9–0.95 as moderate.

RESULTS SEQUENCE DATA The only available cyt b sequence for Lagurus lagurus was incomplete, thus restricting the alignment to 1097 bp. A total of 518 (47.2%) variable sites were observed and 448 of these were parsimony informa- tive. The majority of polymorphic sites were at third positions (352, 67.9%), followed by ﬁrst positions (122, 23.6%) and second positions (44, 8.5%). The average ratio of transitions/transversions was 1.9. Nucleotide composition was characterized by a deﬁcit of guanines (13.2%), similar to that described in arvicolines (Conroy & Cook, 2000; Jaarola et al., 2004) as well as other mammals (Irwin et al., 1991). Genetic distances among arvicoline genera, estimated under the K2P model, ranged from 9% (Myodes–Alticola) to 21.8% (Prometheomys–Arvicola; Table 2). Corresponding intrageneric differences varied between 7.1% (Dicrostonyx) and 15.4% (Ello- bius) and overlapped partly with intergeneric differences. Intergeneric distances are comparable with those reported between muroid genera by Martin 123456789101112131415161718 et al. (2000). 16.217.618.1 15.119.1 15.420.0 16.718.7 1.2 12.4 16.319.3 16.2 15.319.4 15.6 16.1 1.221.8 0.9 16.8 14.3 16.619.2 15.8 14.8 17.820.9 1.2 14.4 15.0 1.1 17.218.9 1.1 18.3 15.8 16.2 18.218.6 17.1 1.4 15.5 16.6 15.9 1.319.3 17.4 16.8 1.2 19.2 16.520.6 1.3 15.9 17.2 16.7 1.1 15.6 16.019.1 16.9 1.0 18.6 19.7 14.2 1.0 17.117.8 16.8 18.2 1.1 16.6 15.7 16.8 1.4 1.2 15.5 17.7 20.5 1.1 16.0 15.9 14.2 14.1 1.1 17.7 18.3 16.1 1.2 15.4 16.8 1.1 19.8 1.4 16.9 16.0 12.6 0.9 1.1 15.5 17.1 15.1 0.9 17.5 15.0 17.8 1.0 19.7 16.6 18.0 1.4 1.1 17.6 9.0 1.2 17.3 0.8 15.8 16.5 1.2 1.4 1.0 17.9 20.3 16.7 1.3 1.3 16.1 17.4 1.4 1.2 1.5 16.4 17.6 16.3 15.9 1.3 1.3 1.4 19.9 17.4 1.4 1.4 1.4 1.2 14.7 1.1 1.3 1.4 19.0 1.1 15.8 17.5 16.8 14.2 1.5 1.5 1.1 1.3 21.2 1.2 1.4 1.2 1.1 17.0 16.3 1.5 1.5 1.1 16.4 1.1 1.2 14.8 19.0 17.2 1.3 1.1 1.1 1.2 15.0 16.5 1.6 1.2 1.4 1.1 1.4 16.8 14.0 1.4 1.1 1.2 17.3 1.2 1.3 16.5 15.4 1.3 18.7 1.4 1.2 1.1 1.3 13.4 19.3 1.2 1.1 1.1 1.3 1.1 16.0 18.1 1.2 1.3 1.3 16.5 1.3 1.0 1.3 18.7 15.4 1.4 19.2 1.1 1.1 1.1 1 16.9 16.7 1.5 1.4 1.4 1.2 0.7 20.6 17.8 1.2 1.2 0.9 15.2 1.0 1.2 17.2 16.7 1.3 19.9 1.4 1.2 1.3 16.8 1.1 1.6 0.8 1.2 17.1 17.5 1.3 1.6 1.2 17.1 1.3 20.2 16.4 1.2 1.3 1 16.0 16.5 1.3 1.4 1.3 1.3 1.2 16.1 1.3 11.2 1.2 1.5 16.2 1.2 1.2 15.4 0.9 1.3 14.4 1.2 1.3 1.1

PHYLOGENETIC ANALYSES Phylogenetic relationships among 69 arvicoline species were evaluated by two methods (ML and BI). Genetic distances among arvicoline genera estimated under a K2P model (% below the diagonal). Standard deviations, where applicable, are shown The gamma distributed shape parameter (a) was 0.58 Arvicola Myopus Synaptomys Phenacomys Dicrostonichiny Blanfordimys Neodon Alticola Dinaromys Eotheomys Myodes Ellobius Ondatra Chionomys Lagurus Microtus or 0.57 (with or without out-group) and the proportion Lemmus 1 Prometheomys 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 of invariable sites (I) equalled 0.48 or 0.49 (with or Table 2. above the diagonal

© 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 825–835 830 E. V. BUZAN ET AL. without out-group). For the BI method, the topology three genera of lemmings and a monophyletic lineage of consensus trees, values of posterior probabilities of collared lemmings and all the remaining genera of and parameter estimates were highly similar in all voles. Within the latter clade, a lineage of ﬁve tribes four analyses (Figs 1,2). [Lagurini, Ellobiusini, Pliomyini (i.e. D. bogdanovi), Monophyly of Arvicolinae was well supported in Prometheomyini, Myodini] emerged as a moderately both the ML (98%) and BI (P = 0.97) tree, although supported (P = 0.94) monophyletic group, whilst the former provided unresolved basal topologies the position of Dicrostonychini, Phenacomyini and within some lineages. The BI analysis revealed two Ondatrini was uncertain because of unresolved nodes. strongly supported (P > 0.95) clades within the taxo- Tree topologies revealed by the two algorithms were nomic scope of arvicolines: the tribe Lemmini with congruent at the level of tribes as recognized by Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021

Peromyscus truei

Cricetulus barabensis

Arvicola terrestris Arvicolini

Ondatra zibethicus Ondantrini

Synaptomys cooperi 84 Myopus schisticolor 97 Lemmini Lemus trimucronatus

Synaptomys borealis 87

100 Dicrostonyx groenlandicus D icrostonychini Dicrostonyx torquatus

Phenacomys intermedius Phenacomyini 98 88 Dinaromys bogdanovi Pliomyini Prometheomys schaposchnik owi Prometheomyini

95 Ellobius fuscocapillus Ellobiusini Ellobius tancrei

84 Microtus, Blanfordimys, Chionomys, Neodon Arvicolini

Lagurus lagurus Lagurini

Alticola macrotis

99 Myodes rutilus Myodes gapperi 97 81 Myodes glareolus Myodini Myodes smithii

99 95 Myodes rufocanus Eothenomys miletus

98 Eothenomys melanogaster

0.05

Figure 1. Maximum likelihood tree of cytochrome b sequences for 69 species of Arvicolinae and rooted with Cricetulus barabensis and Peromyscus truei as out-groups. Phylogeny was constructed using the GTR + G + I model of sequence evolution. Numbers on the branches correspond to ML support > 80%. Tribal division follows Musser & Carleton (2005).

Cricetulus barabensis

Peromysculus truei

Lemmus trimucronatus

0.99 Myopus schisticolor 0.93 Lemmini Synaptomys borealis

Synaptomys cooperi

Dicrostonyx groenlandicus 1.00 Dicrostonychini Dicrostonyx torquatus 0.97 Phenacomys intermedius Phenacomyini Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021

Ondatra zibethicus Ondantrini

0.97 1.00 Microtus, Blanfordimys, Chionomys, Neodon Arvicolini 0.97

Lagurus lagurus Lagurini 0.94 Arvicola terrestis Arvicolini

1.00 Ellobius fuscocapillus Ellobiusini Ellobius tancrei

Dinaromys bogdanovi Pliomyini

0.96 Prometheomys schaposchnik owi Prometheomyini

0.94 Myodes gapperi

Myodes glareolus 1.00 Alticola macrotis 1.00 0.94 Myodes rutilus Myodini Myodes smithii

1.00 1.00 Myodes rufocanus

Eothenomys miletus 1.00 Eothenomys melanogaster

0.05

Figure 2. Fifty per cent majority rule consensus tree of 90 000 trees from a Bayesian analysis of cytochrome b sequences for 69 species of Arvicolinae, rooted with Cricetulus barabensis and Peromyscus truei as out-groups. Numbers above branches represent posterior probability values (P > 0.90). Tribal division follows Musser & Carleton (2005).

Musser & Carleton (2005). Thus, four major nodes were considered in earlier traditional taxonomy to be beneﬁt from good support (Ն 95% or P > 0.95) indi- part of Microtus (Ellerman & Morrison-Scott, 1966; cating unambiguous monophyly of four tribes in both Corbet, 1978; Gromov & Ya Polyakov, 1992). Steppe trees: Lemmini (with Lemmus, Myopus and Synapto- voles (L. lagurus, tribe Lagurini) emerged as a sister mys), Dicrostonychini (Dicrostonyx), Ellobiusini (Ello- genus of the clade with Microtus and its close allies; bius) and Myodini (Myodes, Alticola, Eothenomys). support for the monophyly of Microtus–Lagurus clade Note that Myodes in its current scope is paraphyletic was good in both analyses (91% and P = 1.0 in ML (cf. also Conroy & Cook, 1999) and the monophyly of and BI, respectively). Synaptomys received no support. Most surprisingly, Prometheomys and Dinaromys Both analyses provided support for the monophyly formed a moderately supported monophyletic clade in of a clade with a specious Microtus and its allies the ML tree (88%) and the BI algorithm provided (Blanfordimys, Chionomys and Neodon; 84% and good support (96%) for the monophyly of these two P = 1.0 in ML and BI, respectively). These genera genera and Ellobiusini.

Following traditional taxonomy (Hinton, 1926; The monophyly of the four tribes, Leminini, Ellerman & Morrison-Scott, 1966; Corbet, 1978) and Dicrostonychini, Ellobiusini and Myodini, was well recent tribal division by Musser & Carleton (2005), supported in our analysis by both algorithms, which Arvicola was expected to be a sister genus to the clade is consistent with morphological and fossil data of Microtus and its close relatives, which, however, (Musser & Carleton, 2005). While the exact relation- was not the case. The phylogenetic position of Arvi- ship of taxa within Lemmini could not be resolved, cola was actually poorly resolved. BI analysis our analyses indicated that this group is an assem- revealed moderate support (P = 0.94) for the mono- blage of highly divergent lineages. Furthermore, Syn- phyly of Arvicola, the Microtus clade, Ellobiusini, aptomys appears to be paraphyletic, thus supporting Lagurini, Dinaromys and Prometheomys. Contrary to the generic level of Synaptomys s.str. (with S. cooperi) this, ML placed Arvicola, together with Ondatra, into and Mictomys (S. borealis; cf. Kretzoi, 1969). In spite Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 a weakly supported monophyletic clade (73%) of of their morphological similarity (Miller, 1912), unresolved position within the subfamily. Lemmus and Myopus did not form a supported mono- The phylogenetic positions of two further genera phyletic clade, which caused some authors to consider (Ondatra and Phenacomys), each aligned to a tribe in them as being congeneric (e.g. Chaline et al., its own right (Musser & Carleton, 2005), were unre- 1999). solved in both trees. It is thought that the closest The scope of Arvicolini, a tribe represented in our living relatives of Phenacomys are possibly Microtus study by Microtus, Chionomys, Blanfordimys, Neodon voles (Hinton, 1926; Gromov & Ya Polyakov, 1992). and Arvicola, is more ambiguous. Monophyly of Arvi- In our results, ML provided moderate support (87%) colini, which has mainly been based on morphological for the inclusion of Phenacomys into the clade of and palaeontologic evidence (Hinton, 1926; Gromov & Lemmini and Dicrostonychini, while BI weakly Ya Polyakov, 1992), was recently given additional supported Phenacomys as part of a monophyletic support by an analysis of the GHR nuclear gene clade with Dicrostonychini (P = 0.7). The position of sequence (Galewski et al., 2006). Supporting evidence Ondatra is even more puzzling and the only valid from cyt b and ND4 molecular markers was previ- interpretation from the BI tree is that this genus is ously either entirely absent (Conroy & Cook, 1999) or part of a monophyletic clade encompassing all arvi- weak as a result of incomplete taxonomic sampling coline genera except those from the tribe Lemmini (Martin et al., 2000). In our analyses, Lagurus (tribe (P = 0.86). Lagurini), rather than Arvicola, consistently emerged as a sister lineage to the clade Microtus and allies. Such a phylogenetic scenario contradicts earlier views on the phylogenetic position of Lagurus. Pavlinov & DISCUSSION Rossolimo (1998) placed it within the tribe Prome- While the monophyly of the Arvicolinae is well sup- theomyini on the basis of morphological evidence, ported in both BI and ML analyses, the topologies of whilst Mezhzherin, Morozov-Leonov & Yu Kuznetsova both trees are not entirely congruent with regard to (1995) placed it in Myodini based on allozymic the basal nodes, which receive strong support in the data. BI analysis but are only weakly or moderately sup- The phylogenetic position of the genera Ondatra ported in the ML analysis. However, the two analyses and Phenacomys remains irresolvable. Both genera are not strictly incongruent and we consider the inter- have attracted conﬂicting views on their taxonomic pretation of the BI tree as more reliable. The BI tree position (Musser & Carleton, 2005) and this instabil- provides important new insights into the early radia- ity is also evident from our results. For example, tion of arvicolines, an event which previously was Mezhzherin et al. (1995) suggest that Ondatra should reported to be obscured by irresolvable polytomyes occupy a basal position in arvicolines on the basis of (Conroy & Cook, 1999; Musser & Carleton, 2005). allozymic evidence, while Galewski et al. (2006) pro- Most importantly, lemmings (Lemmini) emerged in posed it to be a sister taxon to Lemmini. Phenacomys, the BI tree as a sister clade to the remaining arvi- with its primitive molar condition, was considered as colines, which is partly supported by morphological part of Myodini (McKenna & Bell, 1997), or as sister evidence (Hinton, 1926; Gromov & Ya Polyakov, genus to Dicrostonychini (Galewski et al., 2006). 1992). Lemmings were also among a group of basal Repenning & Grady (1988) have proposed Phen- taxa in a recent analysis involving both the growth acomys to originate from Mimomys, a fossil genus hormone receptor (GHR) nuclear gene and partial which is generally believed to also be the ancestor of cyt b sequences (Galewski et al., 2006). The exact Arvicola (Kowalski, 2001; Musser & Carleton, relationship among basal taxa was, however, poorly 2005). Our results, however, do not suggest resolved in that study, possibly as a result of incom- close phylogenetic links between Arvicola and plete taxonomic sampling. Phenacomis.

Based on mitochondrial cyt b sequences, Prome- CONCLUSIONS theomys and Dinaromys emerged as two strongly 1. BI and ML analyses of the cyt b gene in 69 species divergent sister genera of a monophyletic clade. Such of voles and lemmings, representing 18 genera a phylogenetic scenario challenges earlier hypotheses from 10 tribes as recognized by Musser & Carleton supporting a close phylogenetic relationship of (2005), provide poorly resolved phylogenies with Dinaromys with Arvicola (Hinton, 1926), Myodes major lineages (tribes) arising from a polytomy. In (Shenbrot & Krasnov, 2005) and Ondatra (Kretzoi, spite of this, the monophyly of tribes (sensu 1955). Prometheomys was typically considered to be Musser & Carleton, 2005) mainly receives robust an isolated lineage within Arvicolinae (Musser & Car- support. Only the tribe Arvicolini emerged as para- leton, 2005) and Repenning et al. (1990) even removed

phyletic in both analyses as a result of the unre- Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 it from the taxonomic scope of the subfamily. Phylog- solved phylogenetic position of Arvicola. eny based on the combination of cyt b and nuclear 2. Lemmings (tribe Lemmini) are possibly a sister GHR sequences suggests Prometheomys to be one of group to the collared lemmings (Dicrostonychini) the most basal arvicolines (Galewski et al., 2006). and all the remaining voles. Within the scope of Musser & Carleton (2005) retain Dinaromys and Lemmini, the genus Synaptomys is paraphyletic. Prometheomys in separate tribes (Pliomyini and 3. Steppe voles Lagurus (tribe Lagurini) are a sister Prometheomyini, respectively), as their only recent genus to a clade encompassing Microtus, Chiono- monospecific genera, but Pavlinov, Ya Yakhontov & mys, Blanfordimys and Neodon. Aghadzhanyan (1995) placed them both into the tribe 4. The phylogenetic position of two genera with Prometheomyini. The tribal name Prometheomyini rooted molars (Phenacomys and Ondatra) was not (Hooper & Hart, 1962) has priority over Pliomyini resolved. We propose that they be left in tribes in (Kretzoi, 1969). their own right (Phenacomyini and Ondatrini, The phylogenetic position of the genus Ellobius, respectively). which emerged in this study as a putative closest 5. Two monospecific genera with rooted molars (Din- relative of the Dinaromys–Prometheomys clade, was aromys and Prometheomys) form a moderately previously also controversial. Because of its aberrant well-supported monophyletic clade, which can be molar pattern, some authors (Gromov & Ya Polyakov, formally recognized as a tribe Prometheomyini. 1992; Gromov & Erbajeva, 1995) placed Ellobius in This tribe is possibly a sister group to Ellobius Cricetinae (sensu Musser & Carleton, 2005), together (Ellobiusini). with true hamsters (Cricetus, Mesocricetus, Cricetu- lus, etc.). Our results thus demonstrate monophyletic roots for at least two ancient vole genera (Dinaromys and Prometheomys) and suggest a possible origin ACKNOWLEDGEMENT from the same lineage for the morphologically We would like to thank David Lunt for help with the aberrant Ellobius. phylogenetic analyses. Fossils provide no evidence in support of an ancient origin of either Prometheomys or Dinaromys. The oldest fossil clearly attributed to Prometheomys REFERENCES is from the middle Pleistocene (Gromov & Ya Polya- kov, 1992), whereas Dinaromys fossils are known Anisimova M, Gascuel O. 2006. Approximate likelihood from the late Pliocene onwards (Gliozzi et al., 1997). ratio test for branches: a fast, accurate and powerful alter- Interpretations of older records are contradictory. native. Systematic Biology 55: 539–552. Stachomys has been attributed to the Prometheomys Baldauf SL. 1998. Phylogeny for the faint of heart. Trends in lineage from the early Pleistocene (Gromov & Bara- Genetics 19: 345–351. Baldauf SL. 2003. Phylogeny for the faint heart: a tutorial. nova, 1981), while the presence of Pliomys and Pli- Trends in Genetics 19: 345–351. olemmus putatively allows tracing of the Dinaromys Brunhoff C, Yuccoz NG, Imes RA, Jaarola M. 2006. lineage to the late Middle Pliocene (Gromov & Ya Glacial survival or late colonization? Phylogeography of the Polyakov, 1992). Considering that the early pulse of root vole (Microtus oeconomus) in north-west Norway. arvicoline diversification has been estimated to have Journal of Biogeography 33: 2136–2144. taken place 3–5 million years ago (based on fossil Chaline J, Brunet-Lecomte P, Montuire S, Viriot L, evidence; Chaline & Graf, 1988) or 5.7 ± 0.6 Myr ago Courant F. 1999. Anatomy of the arvicoline radiation (based on cyt b sequences; Conroy & Cook, 1999), (Rodentia): palaeographical, palaeoecological history and there is a missing link of approximately 2–3 million evolutionary data. Annales Zoologici Fennici 36: 239–267. years between these earliest fossils and a hypo- Chaline J, Graf JD. 1988. Phylogeny of the Arvicolinae thetical common ancestor to Prometheomys and (Rodentia): biochemical and paleontological evidence. Dinaromys. Journal of Mammalogy 69: 22–33.

Conroy CJ, Cook JA. 1999. MtDNA evidence for repeated the common vole (Microtus arvalis) with particular empha- pulses of speciation within arvicoline and murid rodents. sis on the colonization of the Orkney archipelago. Molecular Journal of Mammalogyalian Evolution 6: 221–245. Ecology 12: 951–956. Conroy CJ, Cook JA. 2000. Molecular systematics of a Hinton MAC. 1926. Monograph of voles and lemmings holarctic rodent (Microtus: Muridae). Journal of Mammal- (Microtinae) living and extinct. London: British Museum ogy 81: 344–359. (Natural History). Conroy CJ, Hortelano Y, Cervantes FA and Cook JA. Hooper ET, Hart BS. 1962. A synopsis of recent North 2001. The phylogenitic position of southern relictual species American Microtine rodents. Miscellaneous Publications, of Microtus (Muridae: Rodentia) in North America. Mam- Museum of Zoology, University of Michigan 120: 1– malian Biology 66: 332–344. 68. Cook JA, Runck AM and Conroy CJ. 2004. Historical Huelsenbeck JP, Ronquist F. 2001. MrBayes: Bayesian Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 biogeography at the crossroads of the northern continents: inference of phylogeny. Bioinformatics 17: 754–755. Molecular phylogenetics of red-backed voles (Rodentia: Arvi- Irwin DM, Kocher TD, Wilson AC. 1991. Evolution of colinae). Molecular Phylogenetics and Evolution 30: 767– the cytochrome b gene of mammals. Journal of Molecular 777. Evolution 32: 128–144. Corbet GB. 1978. The mammals of the palaearctic region: Iwasa MA, Suzuki H. 2003. Intra- and interspecific genetic a taxonomic review. London: British Museum (Natural complexities of two Eothenomys species in Honshu, Japan. History). Zoological Science 20: 1305–1313. Dekonenko A, Yakimenko V, Ivanov A, Morozov V, Jaarola M, Martínková N, Gündüz I, Brunhoff C, Zima Nikitin P, Khasanova S, Dzagurova T, Tkachenko E, J, Nadachowski A, Amori G, Bulatova NS, Chon- Schmaljohn C. 2003. Genetic similarity of Puumala dropoulos B, Fraguedakis-Tsolis S, González-Esteban viruses found in Finland and Western Siberia and of the J, López-Fuster MJ, Kandaurov AS, Kefelioglu H, mitochondrial DNA of their rodent hosts suggests a common Mathias MD, Villate I, Searle JB. 2004. Molecular phy- evolutionary origin. Infection, Genetics and Evolution 3: logeny of the speciose vole genus Microtus (Arvicolinae, 245–257. Rodentia) inferred from mitochondrial DNA sequences. Ellerman JR, Morrison-Scott TCS. 1966. Checklist of Molecular Phylogenetics and Evolution 33: 647–663. Palaearctic and Indian Mammals 1758–1946, 2nd edn. Jaarola M, Searle JB. 2002. Phylogeography of field voles London: British Museum (Natural History). (Mocrotus agrestis) in Eurasia inferred from mitochondrial Ewing B, Hillier L, Wendl MC, Green P. 1998. Base-calling DNA sequences. Molecular Ecology 11: 2613–2621. of automated sequencer traces using Phred. I. Accuracy Koenigswald von W. 1980. Schemltzstruktur und Morpholo- assessment. Genome Research 8: 175–185. gie in den Molaren der Arvicolidae (Rodentia). Gesellschaf: Galewski T, Tilak M, Sanchez S, Chevret P, Paradis E, Abhandlungen des Senckenberg Naturforsch, 539: 1–129. Douzery EJP. 2006. The evolutionary radiation of Kowalski K. 2001. Pleistocene rodents of Europe. Folia Arvicolinae rodents (voles and lemmings): relative contri- Quaternaria 72: 1–389. bution of nuclear and mitochondrial DNA phylogenies. Kretzoi M. 1955. Dolomys and Ondatra. Acta Geologica BMC Evolutionary Biology 6: 1–17. Hungarica 3: 347–355. Gliozzi E, Abbazzi L, Argenti P, Azzaroli A, Caloi L, Kretzoi M. 1969. Skizze einer Arvicoliden-Philogenie. Capasso Barbato L, Di Stefano G, Esu D, Ficcarelli G, Vertebrata Hungarica 11: 155–193. Girotti O, Kotsakis T, Masini F, Mazza P, Mezzabotta Krystufek B, Buzan EV, Hutchinson WF, Hänfling B. C, Palombo MR, Petronio C, Rook L, Sala B, Sardella 2007. Phylogeography of the rare Balkan endemic Martino’s R, Zanalda E, Torre D. 1997. Biochronology of selected vole, Dinaromys bogdanovi, reveals strong differentiation mammals, molluscs and ostracods from the Middle Pliocene within the western Balkan Peninsula. Molecular Ecology to the Late Pleistocene in Italy. The state of art. Rivista 16: 1221–1232. Italiana di Paleontologia e Stratigrafia 103: 369–388. Luo J, Yang D, Suzuki H, Wang Y, Chen WJ, Campbell Gromov IM, Baranova GI. 1981. Katalog Mlekopitayush- KL, Zhang YP. 2004. Molecular phylogeny and biogeogra- chikh SSSR (Pliocen – Sovremenost). Leningrad: Nauka. phy of Oriental voles: genus Eothenomys (Muridae, Mam- [Catalogue of mammals of the USSR (Pliocene – Recent)]. malia). Molecular Phylogenetic and Evolution 33: 349– Gromov IM, Erbajeva MA. 1995. The mammals of Russia 362. and adjacent territories: lagomorphs and rodents. St. Peters- Martin Y, Gerlach G, Schlötterer C, Meyer A. 2000. burg: Russian Academy of Sciences, Zoological Institute. Molecular phylogeny of European muroid rodents based on Gromov IM, Ya Polyakov I. 1992. Fauna of the USSR: complete cytochrome b sequences. Molecular Phylogenetics mammals: voles (Microtinae). Leiden: EJ Brill. and Evolution 1: 37–47. Guindon S, Gascuel O. 2003. A simple, fast, and accurate Martinkova N, Zima J, Jaarola M, Macholan M, Spitzen- algorithm to estimate phylogenies by maximum likelihood. berger F. 2007. The origin and phylogenetic relationships Systematic Biology 52: 696–704. of Microtus bavaricus based on karyotype and mitochondrial Hall T. 2004. Bioedit 7.0.0. Raleigh: North Carolina State DNA sequences. Folia Zoologica 56: 39–49. University. Martino V, Martino E. 1922. Note on a new vole from Haynes S, Jaarola M, Searle JB. 2003. Phylogeography of Montenegro. Annals and Magazine of Natural History 9: 413.

Mau B, Newton MA, Larget B. 1999. Bayesian phylogenetic Fejfar O, Heinrich W-D, eds. International symposium on inference via Markov Chain Monte Carlo methods. Biomet- evolution, phylogeny and biostratigraphy of arvicolids rics 55: 1–12. (Rodentia, Mammalia). Prague: Geological Survey, 385– McKenna MC, Bell SK. 1997. Classification of mammals 417. above the species level. New York: Columbia University Repenning CA, Grady FM. 1988. The microtine rodents of Press. the Cheetah Room Fauna, Hamilton Cave, West Virginia, Mezhzherin SV, Morozov-Leonov S, Yu Kuznetsova IA. and the spontaneous origin of Synaptomys. United States 1995. Biochemical variation and genetic divergence in Pale- Geological Survey Bulletin 1853: 1–32. arctic voles (Arvicolidae): subgenus Terricola, true lemmings Shenbrot GI, Krasnov BR. 2005. An atlas of the geographic Lemmus Link 1795, pied lemmings Dicrostonyx Gloger distribution of the arvicoline rodents of the world (Rodentia, 1841, steppe lemmings Lagurus Gloger 1842, mole voles Muridae, Arvicolinae). Sofia: Pensoft. Downloaded from https://academic.oup.com/biolinnean/article/94/4/825/2701275 by guest on 28 September 2021 Ellobius Fischer von Waldheim 1814. Genetika 31: 788–797. Smith MF, Patton JL. 1999. Phylogenetic relationships and Michaux J, Reyes A, Catzeflis F. 2001. Evolutionary the radiation of sigmodontine rodents in South America: history of the most speciose mammals: molecular phylogeny evidence from cytochrome b. Journal of Mammalian Evolu- of Muroid rodents. Molecular Biology and Evolution 18: tion 6: 89–128. 2017–2031. Suzuki H, Tsuchiya K, Takezaki N. 2000. A molecular Miller GS. 1912. Catalogue of the mammals of Western phylogenetic framework for the Ryukyu endemic rodents Europe (Europe exclusive of Russia) in the collection of Tokudaia osimensis and Diplothrix legata. Molecular Phy- the British Museum. London: British Museum (Natural logenetic and Evolution 15: 15–24. History). Swofford DL. 2002. PAUP*. Phylogenetic Analysis Using Modi WS. 1996. Phylogenetic history of LINE-1 among arvi- Parsimony (*and other methods), Version 4.0b10. Sunder- colid rodents. Molecular Biology and Evolution 13: 633–641. land: Sinauer Associates. Musser GG, Carleton MD. 2005. Superfamily Muroidea. In: Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Wilson DE, Reeder D-AM, eds. Mammal species of the molecular Evolutionary Genetics Analysis (MEGA) software world. A taxonomic and geographic reference, 3rd edn, Vol. version 4.0. Molecular Biology and Evolution 24: 1596– 2. Baltimore, MD: John Hopkins University Press, 894– 1599. 1531. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Pavlinov I, Ya Rossolimo OL. 1998. Sistematika Mlekopit- Higgins DG. 1997. The CLUSTAL-windows interface: flex- ayushchikh SSSR. Moscow: Moscow University Press, [Sys- ible strategies for multiple sequence alignment aided by tematics of the mammals of the USSR]. quality analysis tools. Nucleic Acid Research 25: 4876–4882. Pavlinov I, Ya Yakhontov EL, Aghadzhanyan AK. 1995. Triant DA, De Woody JA. 2008. Molecular analyses of Mlekopitayushschie Evrazii. I. Gryzuny. Moscow: Moscow mitochondrial pseudogenes within the nuclear genome of State University, Archives of the Zoological Museum. arvicoline rodents. Genetica 132: 21–33. [Mammals of Eurasia. I. Rodentia]. Xia X. 2000. Data analysis in molecular biology and evolution. Posada D, Crandall KA. 1998. Modeltest: testing the model Boston, MA: Kluwer Academic Publishers. of DNA substitution. Bioinformatics 14: 817–818. Xia X, Xie Z. 2001. DAMBE: data analysis in molecular Rannala B, Yang Z. 1996. Probability distribution of molecu- biology and evolution. Journal of Heredity 92: 371–373. lar evolutionary trees: a new method of phylogenetic Yang Z, Rannala B. 1997. Bayesian phylogenetic inference inference. Journal of Molecular Evolution 43: 304–311. using DNA sequences: a Markov Chain Monte Carlo Repenning CA, Fejfar O, Heinrich W-D. 1990. Arvicolid method. Molecular Biology and Evolution 14: 717– rodent biochronology of the Northern Hemisphere. In: 724.