© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta,

37

, 6, November 2008, pp 571–590

571

Robovsk

y

, J.,

R

i

c

ánková, V. & Zrzav

y

, J. (2008). Phylogeny of Arvicolinae (Mammalia,Cricetidae): utility of morphological and molecular data sets in a recently radiating clade. —

Zoologica Scripta

,

37

, 571–590.Phylogenetic relationships within the Arvicolinae are examined based on two genes(mitochondrial cytb, nuclear GHR exon 10) and 296 morphological, developmental, behavioural,ecological and cytogenetic characters. To inspect the phylogenetic ‘behaviour’ of individualtaxa, basic maximum-parsimony and Bayesian phylogenetic analyses were accompanied byexperiments based on different data-partition combinations, ‘slow–fast’ character weighting,and inclusion/exclusion of individual problematic taxa.

Ellobius

,

Prometheomys

and

Lagurus

arethe most basal arvicolines;

Dicrostonyx

,

Phenacomys

and

Arborimus

form a clade (Dicrostonychinis.lat.); the ‘core arvicolines’ include three subclades: Lemmini (

Synaptomys

,

Lemmus

,

Myopus

),Clethrionomyini (

Eothenomys

,

Myodes

) and Arvicolini (

Arvicola

,

Chionomys

,

Stenocranius

and

Microtus

, the last with six monophyletic subgenera:

Alexandromys

, ‘

Neodon

’,

Mynomes

,

Lasiopodomys

,

Terricola

, and

Microtus

s.str.). Position of

Ondatra

and

Dinaromys

is uncertain, probably com-promised by highly homoplastic morphological characters.Corresponding author:

Jan Zrzav

¥

, Department of Zoology, Faculty of Science, University of SouthBohemia, Brani

6

ovská 31, 370 05

1

eské Bud

e

jovice, Czech Republic. E-mail: zrzavy@centrum.czJan Robovsk

¥

& V

e

ra

‰

i

ç

ánková, Department of Zoology, Faculty of Science, University of SouthBohemia, Brani

6

ovská 31, 370 05

1

eské Bud

e

jovice, Czech Republic. E-mails: jrobovsky@seznam.cz,ricankova@seznam.cz

Blackwell Publishing Ltd

Phylogeny of Arvicolinae (Mammalia, Cricetidae): utility of morphological and molecular data sets in a recently radiating clade

J

AN

R

OBOVSK

Y

, V

E

RA

R

I

C

ÁNKOVÁ

& J

AN

Z

RZAV

Y

Submitted: 22 November 2007Accepted: 28 April 2008doi:10.1111/j.1463-6409.2008.00342.x

Introduction

The Arvicolinae Gray 1821 (voles, lemmings, muskrats, etc.)represent one of the most fascinating rapid radiations amongplacental mammals in the temperate and cold ecosystems ofNorthern Hemisphere. They include approximately 150living species in 30 genera (for a review see Musser & Carleton2005). The arvicolines exhibit numerous key innovations thathave enabled them to adapt to the highly abrasive diet(grasses, forbs and mosses). They include derived mandiblecharacters (Repenning 1968), complicated enamel microstructure,derived molar morphology (von Koenigswald 1980) withhigher crowns (hypsodonty), and common reduction of themolar roots. The Arvicolinae are characterized by variousdegrees of adaptations to the subterranean life, and byremarkable diversity in social organization and matingsystems (e.g. Tamarin

et

al

. 1990; Solomon 1994a,b; Nowak1999; Smorkatcheva 1999; Burda

et

al

. 2000; Evdokimov2003;

R

i

c

ánková

et

al

. 2007; and references therein). Thegroup has very rich Late Cenozoic fossil record (Chaline1987; Repenning

et

al

. 1990; Fejfar

et

al

. 1997; Chaline

et

al

.

1999; Repenning 2001). The earliest indisputable arvicolinesare represented by early Pliocene fossils, and several lineagesof the probably related ‘microtoid cricetids’ appeared in lateMiocene and survived up to Pleistocene (reviewed byMcKenna & Bell 1997).

Despite many attempts to resolve relationships within theArvicolinae, their phylogeny remains uncertain. The previouslypublished phylogenetic analyses of arvicolines were based onmorphology and anatomy (Stein 1986, 1987; Martin 1987,1995; Chaline

et

al

. 1999), cytogenetics (Modi 1987), allozymegenetic distances (Nadler

et

al

. 1978; Graf 1982; Gill

et

al

.1987; Mezhzherin

et

al

. 1995), DNA hybridization (Catzeflis

et

al

. 1987), interspersed repetitive elements (Modi 1996;Triant & DeWoody 2008), and nuclear and mitochondrialDNA sequences (Conroy & Cook 1999, 2000; Suzuki

et

al

.1999; Haring

et

al

. 2000; Conroy

et

al

. 2001; Cook

et

al

.2004; Jaarola

et

al

. 2004; Luo

et

al

. 2004; Bellinger

et

al

. 2005;Galewski

et

al

. 2006; Triant & DeWoody 2006, 2007, 2008).The morphological characters are widely suspected of being

‘subjective’, prone to selective convergence and homoplasy in

Phylogeny of Arvicolinae

•

J. Robovsk

¥

et al.

572

Zoologica Scripta,

37

, 6, November 2008, pp 571–590 • © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters

general (reviewed, e.g. by Baker & Gatesy 2002). In therapidly radiating clades that include numerous closely relatedspecies, the homoplastic morphological characters might beparticularly abundant. As the arvicolines are highly importantfor the Cenozoic palaeoecology, a robust phylogeny of theclade is required. If the arvicoline morphology were really sohomoplastic and cladistically uninformative as commonlybelieved, evolutionary relationships of the fossil arvicolinescould not be reconstructed reliably and the evolutionaryprocesses involved could hardly be estimated. Most recentpalaeomorphological views (e.g. Repenning

et

al

. 1990;Chaline

et

al

. 1999) still attempt to derive the arvicolineevolutionary relationships from a few ‘spectacular’ characters(like the incisor length, used to separate ‘true voles’ from‘lemmings’), not from data sets attempting to explicitlydescribe the whole available ‘morphospace’. Moreover, thearvicoline palaeontologists are confident to directly observenumerous gradual phyletic lineages with few or no splittingevents, and they hence tend to construct replacementchronograms or ‘morphotype-spectra’ instead of trees (e.g.Rabeder 1981, 1986; Chaline 1987, 1990; Martin 1987).Only Martin (1995) used the phylogenetic methodology formorphological characters, albeit with a rather poor taxa sample.

The molecular phylogenetics of the Arvicolinae waslimited to the mitochondrial cytochrome

b

(cytb) gene untilrecently. Several studies recovered star-like multifurcationsamong species and/or genera of the Arvicolinae, which wouldindicate rapid, near simultaneous radiations of multipleclades (‘hard polytomy’). However, an alternative hypothesissuggests that cytb sequences have undergone substitutionsaturation, leading to a loss of the original phylogenetic signal(‘soft polytomy’). Tests for saturation among arvicolinemtDNA cytb revealed evidence of saturation at both transitions(which has been reported previously in the animal mitochon-drial genome) and — surprisingly — also transversions (Triant& DeWoody 2008). The

Microtus

mitochondrial genomeswere found to evolve more rapidly than in any othermammalian lineage, including the other arvicoline genera(Triant & DeWoody 2006). On the contrary, some nucleargenes (growth hormone receptor (GHR) exon 10; Galewski

et

al

. 2006) and numt pseudogenes (

ψ

cytb; Triant & DeWoody2008) could be more useful for resolving relationships ofrecently radiating animals (less heterogeneity among sites,slower evolution to avoid substitutional saturation).

In the present paper we attempt:

(1)

to provide a well-corroborated phylogenetic hypothesison the species-level relationships within the Arvicolinae,based on combination of available non-sequence characters(morphological, behavioural, ecological, developmental andcytogenetic; ‘MOR’ hereinafter) and two well-sampledmolecular protein-coding sequences, mitochondrial cytb andnuclear GHR exon 10;

(2)

to identify problematic species whose phylogeneticposition is unstable (because of lack of relevant information,highly conflicting signals in individual data partitions, and/ornumerous aberrant character states);

(3)

to analyse behaviour of the three highly different datapartitions (MOR, cytb, GHR) in the simultaneous analyses,and their relative influence on the combined-tree topology.

Materials and methods

Taxonomy, characters, and data combination

Altogether 106 species of the recent muroid rodents wereselected for the present analysis. They included 95 arvicolinesand 11 non-arvicoline outgroups, namely, eight non-arvicolinecricetids (Cricetinae:

Cricetulus

,

Cricetus

,

Mesocricetus

,

Phodopus

;Sigmodontinae:

Reithrodon

,

Sigmodon

; Neotominae:

Neotoma

,

Peromyscus

), one murid (

Meriones

), one nesomyid (

Brachytarsomys

),and one spalacid (

Myospalax

). The living arvicolines wereselected to include 89 species whose cyb and/or GHR genesequences were known, plus seven important ‘non-molecular’species (

Blanfordimys afghanus

,

Eolagurus luteus

,

Hyperacriusfertilis

,

Lasiopodomys brandtii

,

Lemmiscus curtatus

,

Neofiberalleni

,

Proedromys bedfordi

). Moreover, 34 more fossil specieswere included in the original analyses (see http://www.blackwellpublishing.com/ZSC). Phylogeny of the fossils willbe analysed and discussed elsewhere in details (J. Robovsk

y

,in prep.); here they were used exclusively to test phylogeneticrelationships among recent groups.

In the present paper, the tribe- and genus-level classificationwas adopted from Musser & Carleton (2005) as follows:Ellobiusini:

Ellobius; Lagurini: Eolagurus, Lagurus; Prome-theomyini: Prometheomys; Phenacomyini: Arborimus, Phenacomys;Dicrostonychini: Dicrostonyx; Pliomyini: Dinaromys; Lemmini:Lemmus, Myopus, Synaptomys; Neofibrini: Neofiber; Ondatrini:Ondatra; ‘Myodini’ (note that Myodini Kretzoi 1969 is a juniorsynonym of Clethrionomyini Hooper & Hart 1962): Alticola,Caryomys, Eothenomys, Hyperacrius, Myodes (= Clethrionomys);Arvicolini: Arvicola, Blanfordimys, Chionomys, Lasiopodomys,Lemmiscus, Microtus, Neodon, Phaiomys, Proedromys, Volemys.For species- and genus-level nomenclature see http://www.blackwellpublishing.com/ZSC; no species of Caryomys andVolemys sensu Musser & Carleton (2005) were analysed here.

In total, 466 morphological, cytogenetic, ontogenetic,ecological and behavioural (MOR) characters were obtainedfrom the literature and by original observation of the collec-tion and captive specimens, originated usually from the wild(for details see http://www.blackwellpublishing.com/ZSC).Some characters were originally assessed but then excludedas being poorly sampled or of uncertain homology (e.g.unusual sex-determination: see Vogel et al. 1998; Hoekstra& Hoekstra 2001; B-chromosomes: see Orlov & Bulatova1983; Zima & Král 1984). Original observations of thebehavioural and developmental characters were conducted in

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© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 6, November 2008, pp 571–590 573

captivity under conditions comparable to other behaviouralstudies (e.g. Dewsbury 1990; Salo et al. 1993; for details seeRicánková et al. 2007).

For the dentition characters, polymorphic coding wasapplied where necessary (note that species not higher taxa wereused as terminal units), as the arvicoline molars are widelyconsidered highly polymorphic (see, e.g. Angermann 1974;Nadachowski 1982; Brunet-Lecomte & Chaline 1992;Contoli et al. 1993). In some species, we preferred to scorepredominant morphotype(s); the influence of differentpolymorphism scoring will be analysed elsewhere in moredetails (J. Robovsky, in prep.). Arvicoline molar morphologyis much complicated and only few characters have been usedfor comparative morphology and phylogenetics yet (e.g.complexity of the anteroconid complex of first lower molar,posteroconid complex of the third upper molar; see Chaline1987; Horácek 1990; Martin 1995; Kaneko 2002). Consequently,we initially described a complete molar morphology withno ‘traditional’ apriorisms to form ‘Data Matrix I’ (see http://www.blackwellpublishing.com/ZSC). However, the molarcharacters were strongly overweighed in that data set, owing toevident serial homology of numerous metameric characterswithin a molar row (cf. Young & Hallgrímsson 2005). Tolimit this differential weighting, we fused all the seriallyhomologous molar structures (anticlines, synclines) perupper/lower molar rows to single characters (‘DataMatrix II’; see Appendix). For details and references seehttp://www.blackwellpublishing.com/ZSC.

Nucleotide sequences of cytb and GHR genes wereobtained from GenBank (for accession numbers see http://www.blackwellpublishing.com/ZSC) and inspected not toinclude ψcytb pseudogenes (nuclear sequences of mitochon-drial origin, or numts; Triant & DeWoody 2008). They werealigned using multiple alignment program MALIGN (Wheeler& Gladstein 1994). However, alignments of both protein-coding genes were trivial (no gaps included). The unweightednucleotide sequences (transition cost = transversion cost),weighted nucleotide sequence (transition : transversion = 1 : 3;a transition : transversion bias of 3.4 was estimated byConroy & Cook 2000), amino acid sequences of both genes,as well as combined nucleotide-amino acid data sets (seeFreudenstein et al. 2003) were compared with MOR data set(using the incongruence length difference (ILD) metrics; seebelow) to find the least incongruent molecular data set.

The different data partitions to be combined in simultaneousanalyses covered different species spectrums (106 speciesfor MOR, 99 for cytb, 33 for GHR). In the original analyses,272 individual vouchers‘ sequences (see http://www.blackwellpublishing.com/ZSC) were combined with the species-specific MOR character scores and analysed simultaneously(maximum parsimony method). To reduce number of terminaltaxa, all species that were found monophyletic in the maximum

parsimony analysis in the original analyses were lumped to singleterminals (by inserting polymorphic coding where necessary).Six species appeared as non-monophyletic (Lemmus sibiricus,Eothenomys miletus, Myodes andersoni, M. imaizumii, M. rufocanus,M. smithii). For further analyses, two molecular terminals(##AF367078 and AB104505) were excluded as vouchermisidentification could not be ruled out. All Lemmus spp.,E. miletus–eleusis, and M. smithii–M. andersoni–M. imaizumiiterminals were lumped to single, albeit formally ‘supraspecific’terminal units (‘Lemmus spp.’, ‘E. miletus’, and ‘Myodes spp.’,respectively). Then we performed (i) separate analyses forindividual data partitions; (ii) combined analyses of all mor-phological characters and sequences of all the 99 ‘molecular’taxa, introducing missing values for the absent sequences(= ‘all-species strategy’; ‘99spp tree’ hereinafter); (iii) combinedanalyses of all character partitions and 33 species for whichboth cytb and GHR sequences are available (= ‘complete-speciesstrategy’; ‘33spp tree’ hereinafter). In the 99spp combineddata set, there were altogether 2351 characters, covering 296MOR (including 254 cladistically informative), 1140 cytb(including 544 informative), and 915 GHR (including175 informative). The combined data set included 37.1%of ambiguous (unknown, inapplicable, or polymorphic)character states.

Phylogenetic analysesThe maximum-parsimony (MP) analysis was applied to MOR,molecular, and combined data matrices (NONA version 2.0;Goloboff 1999: heuristics, option ‘hold10000 mult*100 hold/100’, unconstrained search strategy with TBR branch swapping).Bremer (decay) indices of branch support (BS) and bootstrapsupport values were calculated by NONA (options ‘bsupport10000’and ‘mult*100 hold/10’ with 1000 replications, respectively).The data sets’ quality in separate analyses was compared bycomparison of numbers of resolved nodes in the strict consensusof all minimum-length topologies, consistency (CI) and reten-tion indices (RI), and by total Bremer support (TBS). Thesame criteria were examined in the combined trees (Gatesy2002). To determine the effects of individual data partitionson the total-evidence topology, the ILD (NONA: 100 replica-tions) and partitioned Bremer support (PBS; PAUP version 4;Swofford 2003) were calculated.

In addition, two ‘experimental’ MP analyses were performedin context of 99spp data set.(1) The modified ‘slow–fast’ method (see Brinkmann &Philippe 1999) was used to remove characters (both MORand molecular) that were supposedly responsible for stochasticinformation noise. New data sets were constructed, in whichonly characters with no observed variability within one of the17 well-supported clades were included. The analysed cladesincluded Cricetinae, Ellobius, Dicrostonyx, Phenacomyini,Lemmini, ‘Myodini’, Chionomys, Microtus s.str., M. (Terricola),

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574 Zoologica Scripta, 37, 6, November 2008, pp 571–590 • © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters

M. (Pitymys), M. (Alexandromys), M. pennsylvanicus group(M. oregoni, longicaudus, montanus, pennsylvanicus, canicaudus,townsendii), M. xanthognathus group (M. xanthognathus, miurus,abbreviatus), M. richardsoni group (M. richardsoni, cabrerae), M.guatemalensis group (M. guatemalensis, oaxacensis), B. bucharensis–Neodon juldaschi group, and Phaiomys leucurus-M. clarkei–Neodonirene group. All reduced data sets were then combined to anew, weighted data set, in which each original characterreceived a weight from 17 (36 characters invariable within allselected clades) to 1 (six characters variable within all but oneclade no character was variable within all clades). Moreover,all characters with more than 80% of ambiguous (unknown,inapplicable, or polymorphic) character states were excluded.(2) The species/clades whose position was highly unstable,and/or whose presence/absence caused important topologicalchanges were identified (see Results section). Topological effectsof including/removing the species identified as ‘problematic’were tested by constructing a ‘backbone tree’ that includedonly the ‘unproblematic species’ (see Results section), towhich individual ‘problematic’ species were appended in one-by-one manner (cf. Siddall & Whiting 1999).

Bayesian phylogenetic analysis was conducted with aMetropolis-coupled Markov chain Monte Carlo algorithm(Altekar et al. 2004) as implemented in MRBAYES version 3.1.2(Huelsenbeck & Ronquist 2001; Ronquist & Huelsenbeck2003). MRMODELTEST version 2.2 (Nylander 2004), a simplifiedversion of MODELTEST 3.06 (Posada & Crandall 1998), andPAUP* version 4.0b10 (Swofford 2003) were used to estimatethe best-fitting substitution models: GTR + I + Γ for cytb(based on both AIC and hLRT criteria) and HKY + Γ forGHR (AIC; K80 + Γ based on hLRT, the former preferredbecause of higher number of free parameters). Morphologicalcharacters were treated as unordered, with standard discretemodel assuming Γ-shaped rate variation and variable codingbias. Model parameters were unlinked across partitions. Twoindependent runs of combined analysis with 10 Markovchains each were conducted for 3 000 000 generations with asample frequency of 100 (heating 0.2). The first 1200 treesfrom each run were discarded as burn-in; convergencebetween the two runs was estimated using diagnostics criteriaproduced by the ‘sump’ command in MRBAYES (PSRF[TL] = 1.008). The remaining 57 600 trees were used forreconstruction of a 50% majority-rule consensus tree.Multiple repeating of the analysis with alternating heatingparameter and implementing K80 + Γ model for GHRresulted in identical consensus tree topology with similarposterior probabilities.

ResultsCongruence and relative quality of data partitionsAll the three data partitions (MOR, cytb, and GHR) wereanalysed (maximum parsimony) in the framework of the

‘complete-species’ 33spp data set (including 26 arvicolinespecies and seven outgroups). The MOR data set wassignificantly incongruent with both molecular data sets(MOR × cytb: ILD 0.0174; MOR × GHR: ILD 0.0384),while the molecular data sets were not significantly incongruentone to another (ILD 0.0096). The unweighted (transitioncost = transversion cost) nucleotide sequences of both geneswere identified as most congruent with the MOR data set.Similarly, the ‘Data Matrix II’ of MOR characters (with theserially homologous molar characters fused) were foundslightly more congruent with the molecular partitions thanthe original ‘Data Matrix I’ and used in further analyses. Inthe separate analyses, MOR consistently ranked relativelypoorly as the partition having the least resolved strict con-sensus tree and the lowest TBS (60% of resolved nodes; CI0.37; RI 0.51; TBS +42). The highest-ranking data partitionwas GHR with well-resolved consensus tree and the highestCI and RI (resolution 73%; CI 0.55; RI 0.69; TBS +70). Thecytb data set was the least internally congruent but has thehighest total support (resolution 73%; CI 0.28; RI 0.31; TBS+135).

In the combined three-partition tree, the individual partitionsbehaved differently (Fig. 1). The combined-tree topologywas mostly supported by MOR (ΣPBS +265) whereas cytband GHR were in conflict with the combined topology(ΣPBS –68 and –39, respectively). Altogether 28, 10 and 14clades (out of 30) were supported (or not contradicted) byMOR, cytb, and GHR, respectively. Six clades were supported(or at least not contradicted) by all data partitions (theyinclude Arvicolinae as a whole, ‘Myodini’ and both itssubclades, Phaiomys leucurus–Neodon irene clade, and Microtuskikuchii-M. oeconomus clade). Notably, domination of theMOR partition in the clade support is not due to unequalnumber of characters, as the combined data set was dominatedby cytb (57% of informative characters), not by MORcharacters (22%).

Phylogeny of the ArvicolinaeThe unweighted MP analysis. In the two minimum-lengthcombined trees (length 8724; CI 0.18; RI 0.45; Figs 2 and3A), Ellobius was placed most basally, followed by Prometheomys,Lagurus, Dicrostonyx–Phenacomyini clade, and the supercladeincluding Arvicola–Ondatra, Lemmini, Dinaromys, ‘Myodini’and Microtus s.lat. (with basal most M. gregalis–M. ochrogasterand Chionomys).

The weighted (‘slow–fast’) MP analysis. The genus-level topologyof the 99spp tree (length 64 003, CI 0.20, RI 0.49; Fig. 3B)was almost identical to the unweighted tree. However, therewere obvious differences within Microtus above the Chionomys–M. gregalis level. Whereas the Nearctic and Palearctic speciesdid not form clades in the unweighted tree, there were three

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© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 6, November 2008, pp 571–590 575

major, largely biogeography-consistent groups, two primarilyPalearctic and one primarily Nearctic, in the weighted tree.

The taxon-exclusion MP analyses. Ten species/clades were identifiedas the strongest ‘attractors’ whose presence/absence obviouslyinfluenced tree topology (Ondatra, Phenacomys–Arborimus,M. gregalis, M. arvalis group, Pitymys, M. richardsoni group, B.bucharensis–Neodon juldaschi clade, M. chrotorrhinus, M. agrestis).Phylogenetic position of the following eleven species/cladeswere most heavily affected by presence/absence of the‘attractors’: Lagurus, Arvicola, Dinaromys, M. richardsoni group,Phaiomys leucurus–Neodon irene–M. clarkei clade, M. umbrosus,M. agrestis, Lasiopodomys, M. ochrogaster, M. mexicanus and M.californicus. In summary, the ‘backbone tree’ included Ellobius,Prometheomys, Dicrostonyx, Phenacomyini, Lemmini, ‘Myodini’,Chionomys, M. gregalis, M. socialis group, M. arvalis group, M.(Alexandromys), M. guatemalensis group, M. xanthognathusgroup, M. pennsylvanicus group, Blanfordimys, Neodon juldaschiand M. (Terricola), and the remaining, ‘problematic’, as well as

the ‘non-molecular’ taxa were re-included in one-by-onemanner. In the tree (backbone tree: length 6868; CI 0.22; RI0.49; Fig. 3C), a few differences between original unweighted‘all-taxa’ and the ‘taxon-exclusion’ trees appeared, mostobviously the Arvicola–Ondatra clade was fragmented and allAmerican Microtus species grouped within a single clade(except for more basal M. ochrogaster). The ‘non-molecular’arvicolines grouped as follows: Eolagurus with Lagurus;Hyperacrius with Prometheomys; L. brandtii with L. mandarinus;Neofiber with Ondatra; B. afghanus and P. bedfordi withinthe Palearctic Microtus subclade (including B. bucharensis,N. juldaschi, M. socialis and M. arvalis groups); Lemmiscus in theLemmini–‘Myodini’–Microtus s.lat. superclade (unresolved).

The Bayesian analysis. The Bayesian tree (Fig. 4) was, in general,similar to the MP ones. The most important differences were(i) fragmentation of the Arvicola–Ondatra clade in the Bayesiantree (Arvicola a sister group of Microtus s.lat., Ondatra a sistergroup of Dinaromys) (ii) more basal position of Dinaromys(iii) monophyly of the Ellobius–Prometheomys clade, and(iv) monophyly of M. agrestis–Lasiopodomys–Blanfordimys-N. juldaschi clade.

DiscussionPhylogeny of the ArvicolinaeThe general tree topology. Comparison of different combinedmorphological–molecular trees revealed that tree topologywas quite robust to method selection and parameter changes.In all trees, Ellobius, Prometheomys, Hyperacrius and Laguriniwere the basal arvicolines; Dicrostonyx was a sister group ofPhenacomyini; Lemmini, ‘Myodini’ and Microtus s.lat.formed the major arvicoline clade (see Fig. 5). The mostunstable components included placement of Dinaromys,Arvicola and Ondatra, interrelationships among the basalmostgenera (Ellobius, Prometheomys and Lagurus), and relationshipswithin Microtus s.lat.

Basal arvicolines. The basal position of Ellobius, Prometheomys(+ Hyperacrius), and probably also Lagurini (all Palearctic) issupported by all combined trees and is not affected bypresence/absence of outgroup taxa (only if the transversionswere overweighted, Lagurus would be attracted towards theArvicola–Ondatra clade; see following section). No artefactualattraction of the subterranean arvicolines towards theconvergently similar, subterranean Myospalax (Spalacidae)has been detected (there are no important differencesbetween rooted and unrooted trees), and Ellobius appearsconsistently as a basal arvicoline, not as a cricetid unrelated tothe arvicolines (as proposed Gromov & Polyakov 1992).However, the basal most relationships among Ellobius,Prometheomys–Hyperacrius clade, Lagurini, and the rest of theArvicolinae are unstable (Bayesian analysis found basalmost

Fig. 1 Unweighted combined MP tree of all character partitions(MOR + cytb + GHR) and 33 species for which both cytb and GHRsequences are available (strict consensus of two most parsimonioustrees of length 4054, CI 0.32, RI 0.38). Bootstrap values (higher than50%) are above and partitioned Bremer support values (MOR/cytb/GHR) below the branches.

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576 Zoologica Scripta, 37, 6, November 2008, pp 571–590 • © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters

Fig. 2 Unweighted combined MP tree of all character partitions (MOR + cytb + GHR) and 99 species for which at least cytb sequences areavailable. Bootstrap values (higher than 50%) are above and Bremer support values below the branches.

J. Robovsk¥ et al. • Phylogeny of Arvicolinae

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Ellobius–Prometheomys clade, followed by Lagurus; MPanalyses tended to support successive ‘ladder-like’ topology).Some morphological characters (like well-formed nail of theforelimb thumb, five plantar tubercles, auditory bullae withoutsponge tissue, naked stapedial artery) support close relation-ships between Prometheomys and Hyperacrius; on the contrary,the Hyperacrius–Alticola clade (see Musser & Carleton 2005and references therein) is not supported by the available data.Some morphological characters joining Ellobius, Prometheomysand Hyperacrius (e.g. small pinnae and eyes, simplified molarshapes, ‘primitive’ Schmelzmuster of the enamel; see vonKoenigswald 1980; Gromov & Polyakov 1992) might beassociated with the secondarily (and parallelly?) evolved

subterranean mode of life; however, this phylogenetic patterncould also imply subterranean life in the ancestral arvicolines.The basal clade(s) of the Arvicolinae are characterized also byrelatively high degrees of sociality (Nowak 1999; Evdokimov2003).

Phenacomyini–Dicrostonyx clade. The sister group of all remain-ing arvicolines is the originally North American Dicrostonyx–(Phenacomys–Arborimus) clade. Whereas sister-group relation-ships of Phenacomys and Arborimus (Phenacomyini) is highlystable, well-supported, and has never been doubted (bothwere even considered congeneric by Hinton 1926; Gromov& Polyakov 1992; McKenna & Bell 1997), monophyly of

Fig. 3 A–C. Experimental MP analyses ofarvicoline relationships. —A. Simplifiedunweighted combined tree of all characterpartitions (MOR + cytb + GHR) and 99species (see Fig. 2). —B. Simplified weighted(‘slow–fast’) combined tree of all characterpartitions (MOR + cytb + GHR) and 99species. —A, B. Black and white ellipsehashmarks indicate presence of the clade inpurely molecular (cytb + GHR) and MORtrees, respectively (functionally monotypictaxa are not hashmarked). —C. Results of thetaxon-exclusion analyses; the ‘backbone tree’(simplified unweighted combined tree of allcharacter partitions and 80 species) is inblack, the ‘problematic taxa’ appended inone-by-one manner are in grey.

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Fig. 4 Bayesian analysis of arvicoline relationships, with posterior probabilities on the branches.

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Fig. 5 The preferred phylogeny and proposed classification of the Arvicolinae (in black; outgroups in grey).

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the Dicrostonyx–Phenacomyini clade is supported just bycongruence of the MOR and GHR partitions. AlthoughPhenacomyini were considered to be closely related to Microtus(Gromov & Polyakov 1992) or to the ‘Myodini’ (McKenna &Bell 1997), numerous characters (e.g. the positively differen-tiated enamel symmetry, short incisors, styloid process of themastoid bone exposed to the auditory bulla, anatomy ofdiastemal palate, very small musculus temporalis, discoglandularstomach) favour their Dicrostonyx affinities (see also Modi1996).

Lemmings. The two groups of ‘lemmings’ (Dicrostonychiniand Lemmini) are only distantly related, as the Lemmini areconsistently close to the ‘Myodini’–Microtus s.lat. superclade.Within the Lemmini, whose monophyly has been proposedby nearly all students (but see Martin et al. 2003), Synaptomys(for its monophyly see Triant & DeWoody 2007) is a sistergroup of the Lemmus–Myopus subclade.

‘Myodini’. Within this well-supported and evidently mono-phyletic clade, three subclades are consistently present (seealso Lebedev et al. 2007). The most basal one includes EastPalearctic Eothenomys, the second one several Palearctic Myodesspecies (Craseomys, including M. rex, regulus, rufocanus, andandersoni–imaizumii–smithii complex), and the third subcladecovers Alticola and the rest of Myodes (M. glareolus, gapperi,californicus, rutilus), including all Nearctic Myodes species.Such results support paraphyly of the traditional Myodes(Clethrionomys), as well as Musser & Carleton (2005) refusalof Phaulomys and Eothenomys designation for M. andersoni,M. imaizumii and M. smithii. According to comprehensive cytbanalysis by Lebedev et al. (2007), both Myodes (called ‘Clethrionomys’therein) and Alticola are not monophyletic: basal Craseomyssubclade is followed by Alticola s.str. (including Platycranius),Alticola (Aschizomys) lemminus, and Myodes s.str. (includingalso Alticola macrotis). The ‘Alticola-type’ voles thus haveoriginated several times from Myodes, perhaps as a result ofconvergent adaptations to mountain habitats.

Microtus s.lat. The present phylogenetic analysis (as well asprevious ones; see Jaarola et al. 2004; Galewski et al. 2006)suggests that most genera that have recently been split offMicrotus s.lat. are actually deeply nested within the lattergenus. Only Chionomys is consistently placed as a sister groupof the rest of Microtus, and M. gregalis is most probably a sistergroup of Chionomys or, alternatively, another basal lineage.The basal position of Chionomys and M. gregalis in relation toother Microtus species is well-supported by their morphologyand fossil record (cf. Fejfar & Horácek 1983); the Chionomys–‘Myodini’ relationship (proposed by Mezhzherin et al. 1995)is not supported by the present analyses. Interrelationships ofthe remaining Microtus s.lat. species seem to be strongly

affected by the ‘attraction artefacts’ caused predominantlyby the convergent MOR characters. The weighted andtaxon-exclusion MP and Bayesian analyses (as well as thepurely molecular trees) suggest that there are two major ‘coreMicrotus’ groups, namely, Palearctic (M. arvalis group, M. socialisgroup, Terricola, Lasiopodomys, Blanfordimys, N. juldaschi,M. agrestis) and Nearctic (including Pitymys and SW EuropeanM. cabrerae), plus two minor more basal taxa, namely,Alexandromys and the Phaiomys-N. irene-M. clarkei clade. Inthe Bayesian tree, however, Lasiopodomys, Blanfordimys, N.juldaschi and M. agrestis form a clade which is sister to theAmerican Microtus clade. Position of North American M.ochrogaster is unstable: it belonged to basalmost Microtus s.lat.species in some MP trees, whereas it was deeply nested withinthe Nearctic clade in the weighted MP and Bayesian tree (seeJaarola et al. 2004). The putatively ancestral complex ofLasiopodomys, Blanfordimys, Neodon and Phaiomys (see Gromov& Polyakov 1992; Nadachowski & Zagorodnyuk 1996) isevidently diphyletic and their ‘archaic dentition’ has to be —at least partly — secondarily evolved. Position of Proedromys(no molecular data) is uncertain as well, with possible placementwithin the Lasiopodomys–Blanfordimys–N. juldaschi clade. Thebasal subclades of Microtus s.lat. are Palearctic and the wholegroup is evidently of the Palearctic origin.

Dinaromys and Lemmiscus. The endemic Balkan snow volerepresents an isolated group of the Arvicolinae, probably asister group of the ‘Myodini’–Microtus s.lat. superclade(maximum parsimony), or (together with Ondatra) a sistergroup of the more inclusive Lemmini–‘Myodini’–Microtuss.lat. superclade (Bayesian tree). Despite its ‘archaic’ enamelcharacteristics, there are no signs of closer relationshipsbetween Dinaromys and Prometheomys (Pavlinov et al. 1995;see also Kretzoi 1969; von Koenigswald 1980; Zagorodnyuk1990; Chaline et al. 1999). Moreover, Dinaromys is not closelyrelated to the ‘Myodini’ (McKenna & Bell 1997), and pre-liminary results of the pilot studies including 34 fossil arvicolinessuggested no closer relationships between Dinaromys andprobably more basal †Pliomys or †Dolomys (cf. Kretzoi 1969;Chaline 1975; Gromov & Polyakov 1992; Chaline et al.1999). Lemmiscus (without available molecular data) seems tobelong to the Lemmini–‘Myodini’–Microtus s.lat. superclade,but its precise phylogenetic affinities remain uncertain (forpossible close relationships between Lemmiscus and Microtussee Carleton 1981; Modi 1996). The expected Lemmiscus–Lagurini clade (Chaline et al. 1999; for a review see Musser& Carleton 2005) has never been retrieved.

Water voles (Arvicola, Neofiber, Ondatra). The taxon-exclusionMP tree suggested that position of Arvicola might be heavilyinfluenced by the presence/absence of Ondatra. In its absence,Arvicola is placed next to Microtus s.lat., a conclusion compatible

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with the Bayesian tree and with results of most previousauthors as well (for a review see Musser & Carleton 2005).No close affinities between Arvicola and M. richardsoni(Musser & Carleton 2005 and references therein) were foundhere. Ondatra groups as a sister group of the Lemmini in thetaxon-exclusion MP analysis, a position supported by a fewcharacters (strongly reduced anticlinal tip enamel, long breedingperiod, plus three possible molecular autapomorphies), or asa sister group of Dinaromys just above the Lemmini in theBayesian tree. Both Ondatra and Dinaromys share some dentalcharacters (deep fourth syncline in the first lower molar,narrow connection between fifth and sixth triangle in lowermolars, absence of the Mimomys–Schmelzmuster), nakedstapedial artery, inter-orbital crest, postorbital prominencesin the form of a broad shelf, long gestation period, and 11possible molecular autapomorphies. Although there are nomolecular data for the round-tailed muskrat, morphological,cytogenetic and ecological characters (see Repenning et al.1990; Modi 1996) seem to support sister-group relationshipbetween Neofiber and Ondatra. In conclusion, adaptations tothe water and riparian habitats evolved convergently duringthe evolution of Arvicolinae.

Classification of the ArvicolinaeIn recent years, two taxonomical trends are obvious in theclassification of Arvicolinae: (i) proliferation of family groupnames, practically a one-to-one correspondence with recognizedgenera (e.g. Ellobiusini, Prometheomyini, Dicrostonychini,Ondatrini, Neofibrini) and (ii) proliferation of genus-levelnames within Microtus s.lat. (e.g. Lasiopodomys, Blanfordimys,Chionomys, Neodon, Phaiomys, Proedromys, Volemys) and the‘Myodini’ (e.g. Aschizomys, Eothenomys, Phaulomys, Caryomys,Craseomys). Most arvicoline genera whose monophyly hasbeen tested by the present analysis were found monophyletic(Ellobius, Dicrostonyx, Arborimus, Lemmus, Chionomys). However,two clades, ‘Myodini’ and Microtus s.lat., should be stronglyreclassified to fit the phylogenetic relationships (Fig. 5).

Within the ‘Myodini’, the two-genus classification includingEothenomys (sensu Musser & Carleton 2005) and Myodes s.lat.(including Craseomys, Alticola, Aschizomys and Myodes sensuMusser & Carleton 2005) is possible. We prefer not to split‘Myodini’ into numerous genera, as recently proposed byLebedev et al. (2007).

Within Microtus s.lat., Arvicola and Chionomys should beclassified as separate genera, and elevation of M. gregalis tothe full-genus status (Stenocranius Kastchenko 1901) seems tobe the least problematic taxonomic solution. Neodon Horsfield1841 is evidently diphyletic: ‘N’. juldaschi is a stronglysupported sister species of B. bucharensis; N. irene (and probablyalso the type species, N. sikimensis; see Musser & Carleton2005) belongs to the well-supported Phaiomys–M. clarkeiclade. Most Nearctic species (including Pitymys, M. richardsoni

and M. ochrogaster) form a clade for which MynomesRafinesque 1817 is a useful name. The clade including mostPalearctic species is to be split into three monophyleticsubgenera: Microtus s.str. (M. arvalis group and M. socialisgroup), Lasiopodomys s.lat. (including Blanfordimys, ‘N’. juldaschi,and possibly also Proedromys), and Terricola. Position ofM. agrestis is unstable: Bayesian and ‘slow–fast’ MP analysesidentified it as a sister group of Lasiopodomys s.lat., in thetaxon-exclusion MP tree it belonged—more traditionally—to Microtus s.str. Two more Palearctic clades, Alexandromyss.lat. and N. irene–Phaiomys–M. clarkei, are both well supported;however, their phylogenetic positions are rather unstable.The correct name for the last subgenus is impossible to deter-mine at present; ‘Neodon’ would be useful, depending on theprecise position of N. sikimensis (not analysed here).

The proposed tribal classification of the Arvicolinae(Fig. 5) is based on the Bayesian and ‘slow–fast’ MP trees, andincludes four well-supported and stable clades. They areDicrostonychini Kretzoi 1955 (Dicrostonyx, Arborimus,Phenacomys), Lemmini Gray 1825 (Synaptomys, Lemmus,Myopus), Clethrionomyini Hooper & Hart 1962 (Eothenomys,Myodes) and Arvicolini Gray 1821 (Arvicola, Chionomys,Stenocranius stat.n., Microtus). The remaining genera areleft as ‘incertae sedis’ at present because of their unstableposition.

Morphology and evolution of the ArvicolinaeParsimony optimization of the MOR character diversity onvarious tree topologies indicated very high levels of parallel-isms and reversals in the characters that were usuallyregarded as evolutionarily most important. For example, the‘positively differentiated’ enamel (with leading edge thickerthan the trailing one) has originated several times (Lagurus,Dicrostonychini s.lat., Alticola strelzovi, and Microtus s.lat.), andsuch pattern had been reversed to the symmetric or ‘nega-tively differentiated’ enamel at least in M. umbrosus and theM. guatemalensis group. The molar roots seem to have beenreduced three times, in Hyperacrius, Lagurus–Eolagurus, andin the ‘core arvicoline’ superclade, but secondarily reevolvedin Dinaromys, Phenacomyini, Ondatra, and twice within the‘Myodini’. The incisors have been shortened independentlyin the Dicrostonyx and Lemmini. Our results also indicateparallelisms and/or reversals in evolution of characters likeMimomys-Schmelzmuster, cement, auditory bullae with spongetissue, naked stapedial artery, and termination of the palatalsurface.

Evaluation of the relative quality of data partitions andtheir performance in the combined analysis indicated that theMOR data set was highly influential in the simultaneousanalyses of all data partitions. The PBS values in the 33sppcombined tree revealed that, despite the significant in-congruence of the morphological and molecular data partitions,

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the former contributed positively to BS values (= supports) of26 clades (87%) and is negative for (= conflicts with) fourclades (13%) only. It indicates that a strong secondaryphylogenetic signal is hidden in the MOR data matrix, whichmakes it so influential in constructing the combined tree.The support, stability, congruence and resolving power of aparticular data partition may be high in some taxa but not inothers. The conflicts among data partitions most probably donot exist throughout the tree, and differences in the placementof a few taxa are sufficient to create significant incongruence.In the 33spp (i.e. ‘complete-species’) tree, all data partitionssupported monophyletic Arvicolinae, but the basalmostarvicoline topology was supported exclusively by the MORand GHR partitions; the cytb data set was the most powerfultool for recovering interrelationships within the ‘Myodini’;both molecular partitions were in conflict with MOR withinthe Microtus s.lat. By combining all of the data sets, we haveidentified nodes that may potentially change with the additionof new data, that is, nodes where the available data partitionsconflict strongly with each other (basal splitting, position ofOndatra, Dinaromys, Arvicola, M. agrestis), and nodes that areunlikely to change with future new data as all data are inagreement (e.g. Phenacomyini, Lemmini, ‘Myodini’, monophylyof most genera).

In conclusion, some morphological, cytogenetic and‘biological’ features appeared as better descriptors of thearvicoline relationships than expected by previous authors,despite obviously homoplastic nature of many traditionallyapplied, ‘spectacular’ morphological characters that resultedfrom their rapid and often convergent evolution. Out of 254MOR characters that are cladistically informative in the contextof 99spp analysis, 26 were congruent with the molecularinformation, 75 were context-independent, and only aboutone half (134) of the MOR characters are convergent, con-flicting with the molecular information (see Appendix fordetails). If the MOR characters were classified into foursubsets, namely, skeleton–dentition (62 characters), external-soft anatomy (58), cytogenetics (98), and ecology–development–behaviour (36), the last subset seems to be more ‘convergent’(3% congruent, 63% convergent) than the others (skeleton–dentition 10% and 46%, external-soft anatomy 12% and50%, cytogenetics 12% and 34%, respectively).

Phylogenetic analyses of the extant and extinct Arvicolinae,and derivation of ecomorphological, palaeoecological andbiogeographical hypotheses from the robust phylogenies aretherefore quite hopeful. The most fundamental obstacle isneither rapid diversification of the arvicolines during theQuaternary period, nor putative ‘non-tree’ nature of theirevolution, but the lack of many positively scored characters inextinct and even numerous extant species. The most promisingsources of new, hitherto weakly exploited phylogeneticevidence seem to be myology, cytogenetics, reproduction,

and sociobiology (see ‘constant’ and ‘congruent’ but ‘ambiguous’characters in Appendix).

AcknowledgementsAuthors are obliged to M. And´ra, P. Brunet-Lecomte, C. J.Conroy, D. Frynta, Y. Kaneko, D. Mörike, T. Pes, A.Smorkatcheva and V. Vohralík for providing us with thematerial and/or valuable information. Authors would like tothank V. Hypsa, L. Piálek, P. Ríha, and O. Rícan for technicalassistance, and H. Burda, I. Horácek, J. Zima, and twoanonymous referees for discussion of earlier versions of themanuscript. Part of the Bayesian analyses was carried out byusing the resources of the Computational Biology ServiceUnit from Cornell University (partially funded by MicrosoftCorporation). This work was supported by the Czech Ministryof Education and Academy of Sciences grants #6007665801and #KJB601410825, respectively.

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Appendix List of morphological, cytogenetic, developmental, ecological and behavioural (MOR) charactersFor detailed description and discussion of the character scoringand coding (including ‘fused characters’) and references seehttp://www.blackwellpublishing.com/ZSC; the present listof molar characters is ‘Character Matrix II’ (see Material andMethods section). Unless otherwise stated, all multi-statecharacters are unordered. The characters which are cladisticallyuninformative in the context of 99spp combined MOR–cytb–GHR analyses are asterisked (39 characters); ‘ambiguous’characters (with more than 80% of unknown, inapplicable, orpolymorphic character states) are italicized (166 characters).All MOR characters’ retention indices (RI) were computedfor the 99spp morphological, combined, and molecular trees(riMOR, riCOMB and riMOL, respectively; compare Gaubertet al. 2005). The MOR characters were then classified as(i) ‘congruent’ with the molecular ones (riMOR < riCOMB orriCOMB < riMOL) (ii) ‘constant’, or context-independent(riMOR = riCOMB = riMOL), and (iii) ‘convergent’, or conflict-ing with the molecular information (riMOR > riCOMB orriCOMB > riMOL). The 102 ‘constant’ and ‘congruent’ char-acters are boldfaced.

Morphology: dentition0*. Lower molars, first lingual and labial anticline [fusion]:

0, absent; 1, present, U-shaped; 2, present, V-shaped [ordered].1*. Lower molars, second lingual and labial anticline

[fusion]: 0, absent; 1, present, U-shaped; 2, present, V-shaped[ordered].

2*. Lower molars, third lingual and labial anticline [fusion]:0, absent; 1, present, U-shaped; 2, present, V-shaped [ordered].

3. Lower molars, fourth lingual and labial anticline [fusion]:0, absent; 1, present, U-shaped; 2, present, V-shaped [ordered].

4. First lower molar, fifth lingual and labial anticline[fusion]: 0, absent; 1, present, U-shaped; 2, present,V-shaped [ordered].

5*. First lower molar, sixth lingual and labial anticline[fusion]: 0, absent; 1, present, U-shaped; 2, present, V-shaped[ordered].

6*. Seventh lingual anticline, in first lower molar: 0, absent;1, present, U-shaped; 2, present, V-shaped [ordered].

7*. Lower molars, first lingual and labial syncline [fusion]:0, absent; 1, shallow; 2, deep [ordered].

8*. Lower molars, first lingual and labial syncline [fusion]:0, weakly curved; 1, strongly curved [ordered].

9*. Lower molars, second lingual and labial syncline[fusion]: 0, absent; 1, shallow; 2, deep [ordered].

10. Lower molars, second lingual and labial syncline [fusion]:0, weakly curved; 1, strongly curved.

11. Lower molars, third lingual and labial syncline[fusion]: 0, absent; 1, shallow; 2, deep [ordered].

12. Lower molars, third lingual and labial syncline [fusion]:0, weakly curved; 1, strongly curved.

13. First lower molar, fourth lingual and labial syncline[fusion]: 0, absent; 1, shallow; 2, deep [ordered].

14. First lower molar, fourth lingual and labial syncline[fusion]: 0, weakly curved; 1, strongly curved.

15*. First lower molar, fifth lingual and labial syncline[fusion]: 0, absent; 1, shallow; 2, deep [ordered].

16. First lower molar, fifth lingual and labial syncline[fusion]: 0, weakly curved; 1, strongly curved.

17. Sixth lingual syncline, in first lower molar: 0,absent; 1, shallow; 2, deep [ordered].

18*. Lower molars, connection between lobus posteriorand first triangle [fusion]: 0, narrow; 1, medium-sized, fullyconfluent.

19. Lower molars, connection between first andsecond triangle [fusion]: 0, narrow; 1, medium-sized,fully confluent.

20. Lower molars, connection between second and thirdtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

21. Lower molars, connection between third and fourthtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

22. Lower molars, connection between fourth and fifthtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

23. Lower molars, connection between fifth and sixthtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

24. Connection between sixth and seventh triangle, infirst lower molar: 0, narrow; 1, medium-sized, fullyconfluent.

25. Connection between seventh and eighth triangle,in first lower molar: 0, narrow; 1, medium-sized, fullyconfluent.

26*. Connection between eighth and ninth triangle, in firstlower molar: 0, narrow; 1, medium-sized, fully confluent.

27*. Connection between ninth and tenth triangle, in first lowermolar: 0, narrow; 1, medium-sized, fully confluent.

28. Lower molars, cement in first lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

29. Lower molars, cement in second lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

30. Lower molars, cement in third lingual and labial syncline[fusion]: 0, absent; 1, small amount; 2, large amount [ordered].

31. First lower molar, cement in fourth lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

32. First lower molar, cement in fifth lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

33*. Cement in sixth lingual syncline, in first lower molar:0, absent; 1, small amount; 2, large amount [ordered].

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586 Zoologica Scripta, 37, 6, November 2008, pp 571–590 • © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters

34*. Upper molars, first lingual and labial anticline[fusion]: 0, absent; 1, present, U-shaped; 2, present, V-shaped[ordered].

35*. Upper molars, second lingual and labial anticline[fusion]: 0, absent; 1, present, U-shaped; 2, present, V-shaped[ordered].

36*. Upper molars, third lingual and labial anticline [fusion]: 0,absent; 1, present, U-shaped; 2, present, V-shaped [ordered].

37*. Upper molars, fourth lingual and labial anticline [fusion]:0, absent; 1, present, U-shaped; 2, present, V-shaped [ordered].

38*. Upper molars, fifth lingual and labial anticline [fusion]:0, absent; 1, present, U-shaped; 2, present, V-shaped [ordered].

39*. Upper molars, first lingual and labial syncline [fusion]:0, absent; 1, shallow; 2, deep [ordered].

40. Upper molars, first lingual and labial syncline[fusion]: 0, weakly curved; 1, strongly curved.

41*. Upper molars, second lingual and labial syncline [fusion]:0, absent; 1, shallow; 2, deep [ordered].

42. Upper molars, second lingual and labial syncline [fusion]:0, weakly curved; 1, strongly curved.

43. Upper molars, third lingual and labial syncline [fusion]:0, absent; 1, shallow; 2, deep [ordered].

44. Upper molars, third lingual and labial syncline[fusion]: 0, weakly curved; 1, strongly curved.

45*. Upper molars, fourth lingual and labial syncline[fusion]: 0, absent; 1, shallow; 2, deep [ordered].

46*. Upper molars, fourth lingual and labial syncline [fusion]:0, weakly curved; 1, strongly curved.

47*. Upper molars, connection between lobus posteriorand first triangle [fusion]: 0, narrow; 1, medium-sized, fullyconfluent.

48. Upper molars, connection between first and secondtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

49. Upper molars, connection between second and thirdtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

50. Upper molars, connection between third and fourthtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

51. Upper molars, connection between fourth and fifthtriangle [fusion]: 0, narrow; 1, medium-sized, fully confluent.

52. Upper molars, connection between fifth and sixthtriangle [fusion]: 0, narrow; 1, medium-sized, fullyconfluent.

53*. Connection between sixth and seventh triangle, in thirdupper molar: 0, narrow; 1, medium-sized, fully confluent.

54*. Connection between seventh and eighth triangle, in thirdupper molar: 0, narrow; 1, medium-sized, fully confluent.

55. Upper molars, cement in first lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

56. Upper molars, cement in second lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

57. Upper molars, cement in third lingual and labialsyncline [fusion]: 0, absent; 1, small amount; 2, large amount[ordered].

58*. Upper molars, cement in fourth lingual and labial syncline[fusion]: 0, absent; 1, small amount; 2, large amount [ordered].

59*. Leading edge, enamel: 0, primitive tangential; 1,tangential; 2, lemming lamellar; 3, discrete lamellar; 4, lamellar.

60*. Trailing edge, enamel: 0, primitive tangential; 1, tan-gential; 2, lemming lamellar; 3, discrete lamellar; 4, lamellar.

61*. Synclinal tip, enamel: 0, primitive tangential; 1, tangential;2, lemming lamellar; 3, discrete lamellar; 4, lamellar.

62*. Anticlinal tip, enamel: 0, primitive tangential; 1, tangential;2, lemming lamellar; 3, discrete lamellar; 4, lamellar.

63*. Posterior loop, enamel: 0, primitive tangential; 1, tangential;2, lemming lamellar; 3, discrete lamellar; 4, lamellar.

64. Enamel symmetry: 0, leading edge ≤ trailing edge;1, leading edge > trailing edge.

65. Mimomys–Schmelzmuster: 0, absent; 1, present.66. Anticlinal tip, enamel: 0, not reduced; 1, strongly

reduced.67. Molars: 0, rooted; 1, rootless.68. Molar crown height: 0, brachyodont; 1, mesohypsodont;

2, hypsodont [ordered].69. Lower incisor: 0, relatively short, wholly lingual to the

molars; 1, long, passing from the lingual to the labial side ofthe molars.

70. Longitudinal groove in upper incisors: 0, absent; 1, shallow;2, deep [ordered].

71. First lower molar, enamel island: 0, absent; 1,present.

72. Third upper molar, enamel island: 0, absent; 1,present.

Morphology: mandible73. Ascending ramus obscuring all or part of 2nd lower

molar in labial aspects of the mandible: 0, absent; 1, present.74. Arvicoline groove (sensu Repenning 1968): 0, absent;

1, present.75. Lower masseteric crest relatively long, anteriorly

placed, very shelf-like: 0, absent; 1, present.76. Internal temporal fossa in the form of a broad, shallow,

elongate depression, separates second and third lower molarsfrom the ascending ramus: 0, absent; 1, present.

77. Mandibular condylar process: 0, as high ascoronoid process or lower; 1, elevated above coronoidprocess.

78. Ridge position of condylar process: 0, anteriorlyplaced; 1, intermediate; 2, posteriorly placed [ordered].

Morphology: auditory region79. Auditory bullae, size: 0, small; 1, medium-sized; 2, large

[ordered].

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© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 6, November 2008, pp 571–590 587

80. Auditory bullae: 0, with sponge tissue; 1, withoutsponge tissue.

81. Paroccipital processes: 0, absent or very small; 1,broadly attached to the auditory bullae; 2, directed backwardto the auditory bullae.

82. Malleus, laminal border: 0, complete; 1, emarginate.83. Malleus, anterior process: 0, short; 1, long or very

long.84. Stapedial artery: 0, naked; 1, enclosed in a bony tube.

Morphology: partial skull morphology85. Occipital condyles in lateral view: 0, partly or fully

visible; 1, masked by the mastoid.86. Palatal surface terminating posteriorly as a simple

transverse shelf: 0, present; 1, absent.87. Zygomatic plate: 0, narrow; 1, wide.88. Inter-orbital region: 0, flat; 1, with inter-orbital crest;

2, with depression.89. Postorbital prominences: 0, absent; 1, small; 2, a broad

shelf [ordered].

Morphology: anatomy of diastemal palate90. Anterior longitudinal ridge: 0, absent; 1, present.91. Inflexi of upper lips: 0, less developed, without contact;

1, developed and non-fused; 2, developed and fused[ordered].

Morphology: baculum and glans penis92. Baculum, median process: 0, absent; 1, present.93. Baculum, lateral processes: 0, absent; 1, smaller

than median process; 2, equal to or larger than medianprocess [ordered].

94. Glans penis (sensu Hooper & Hart 1962): 0, Ellobius-type;1, group I; 2, group II; 3, group III.

95. Penis, dorsal papilla: 0, absent; 1, present, with a singleconule; 2, present, with two conules; 3, present, with three conules;4, present, with four conules [ordered].

96. Penis, lobes of the urethral process: 0, one; 1, two; 2, three;3, four; 4, five; 5, six; 6, seven [ordered].

97. Penis, crater rim: 0, smooth; 1, non-papillose; 2,papillose [ordered].

Morphology: masticatory and limb myology98. Musculus masseter superficialis, insertion: 0, posterior;

1, anterior.99. Musculus masseter lateralis profundus: 0, undivided;

1, divided.100. Musculus masseter lateralis profundus with V-like

posterior portion of the Y-shaped aponeurosis: 0, present;1, absent.

101. Superficial temporalis: 0, large; 1, small; 2, very small[ordered].

102. Deep lateral temporalis: 0, less distinct; 1, distinct.103. Postorbital crest tendon of the deep medial

temporalis: 0, absent; 1, present.104. Main tendon of the deep lateral temporalis: 0, distinct; 1,

less distinct.105. Musculus pterygoideus internus: 0, small; 1, large.106. Sesamoid: 0, shared by radial collateral ligament

and supinator tendon; 1, exclusively in the supinator tendon.107. Abductor pollicis longus: 0, with three tendons of insertion;

1, with two tendons.108. Angle of the falciform with a horizontal axis through the

palm: 0, 45–60º; 1, 75–80º.109. Extensor digitorum communis tendons: 0, do not possess

sesamoids; 1, do possess sesamoids.110. Tendon originating from the ulnar division of the extensor

digitorum communis and inserting on the ulnar side of digit III:0, absent; 1, present.

111. Tendon of third head of flexor digitorum profundus:0, larger than that of the other two heads; 1, not larger.

112. Flexor digitorum profundus: 0, sends a tendinousslip to digit I; 1, this slip is reduced or absent.

113. Pronator quadratus: 0, well developed; 1, reduced.114. Digit I of the manus: 0, claw; 1, nail.115. Abductor pollicis brevis: 0, absent; 1, present.116. Flexor pollicis brevis: 0, absent; 1, present.117. Adductor pollicis: 0, absent; 1, present.118. Adductor digiti secundi: 0, absent; 1, present.119. Abductor digiti quinti: 0, absent; 1, present.120. Origin of the adductor digiti quinti: 0, is superficial

to and between interossei III and IV; 1, has shifted to theulnar side of common interossei origin.

121. Adductor digiti quinti: 0, absent; 1, present.122. Opponens digiti quinti inserts: 0, on both sides of the base

of digit V; 1, on the ulnar side only.123. Lumbrical II: 0, absent; 1, present.124. Interossei: 0, reduced to six; 1, full complement of

seven.125. The palmaris brevis: 0, reduced to absent; 1, well-

developed.

Morphology: glands126. Meibomian glands: 0, small and numerous; 1,

large and sparse.127. Sebaceous glands: 0, absent; 1, caudal; 2, rump; 3,

hips; 4, flanks.

Morphology: stomach128. Incisura angularis: 0, shallow; 1, intermediate; 2,

deep [ordered].129. Bordering fold: 0, smooth; 1, with processes

concentrated on the left rim of fold; 2, with processesencompassing the entire rim of fold [ordered].

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588 Zoologica Scripta, 37, 6, November 2008, pp 571–590 • © 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters

130. Glandular zone (sensu Carleton 1981): 0, hemi-glandular; 1, intermediate grade I; 2, intermediate gradeII; 3, intermediate grade III; 4, discoglandular [ordered].

Cytogenetics (from Modi 1987)131. Chromosome number: 0, 15–20; 1, 21–26; 2, 27–32;

3, 33–38; 4, 39–44; 5, 45–50; 6, 51–56; 7, 57–62; 8, 63–68;9, 69 or more [ordered].

132. X chromosome: 0, acrocentric–telocentric; 1,submetacentric–subtelocentric; 2, metacentric.

133. X chromosome: 0, small; 1, medium-sized; 2, large[ordered].

134. Y chromosome: 0, acrocentric–telocentric; 1,submetacentric–subtelocentric; 2, metacentric.

135. Y chromosome: 0, small; 1, medium-sized; 2, large[ordered].

136. Number of autosomal arms: 0, 30–35; 1, 36–41;2, 42–47; 3, 48–53; 4, 54–59; 5, 60–65; 6, 66–71; 7, 72–77; 8,78–83; 9, 84 or more [ordered].

137. Sex chromosomes pairing: 0, synaptic; 1, asynaptic.138. Cytotype: 0, glareolus; 1, rufocanus.139. Chromosome 1, primitive condition: 0, absent; 1, present.140. Chromosome 1, proximal deletion: 0, absent; 1, present.141. Chromosome 1, reciprocal translocation with 9:

0, absent; 1, present.142. Chromosome 1, tandem fission into medium-sized acrocentrics

and deletion of some material: 0, absent; 1, present.143. Chromosome 1, tandem fission and deletion: 0, absent;

1, present.144. Chromosome 1, tandem fission and deletion: 0, absent;

1, present.145. Chromosome 1, centric fusion of 1f with 5: 0, absent;

1, present.146. Chromosome 2, primitive condition: 0, absent; 1, present.147. Chromosome 2, interstitial addition: 0, absent; 1, present.148. Chromosome 2, proximal deletion: 0, absent; 1, present.149. Chromosome 2, centric transposition: 0, absent; 1, present.150. Chromosome 3, primitive condition: 0, absent; 1, present.151. Chromosome 3, paracentric inversion: 0, absent;

1, present.152*. Chromosome 3, centric fusion with chromosome 33:

0, absent; 1, present.153. Chromosome 3, centric fusion with 8: 0, absent; 1, present.154. Chromosome 4, primitive condition: 0, absent; 1, present.155. Chromosome 4, centric transposition: 0, absent; 1, present.156. Chromosome 4, proximal addition: 0, absent; 1, present.157. Chromosome 4, large proximal addition: 0, absent;

1, present.158. Chromosome 4, centric fusion with 37: 0, absent; 1, present.159. Chromosome 5, primitive condition: 0, absent; 1, present.160. Chromosome 5, centric transposition: 0, absent;

1, present.

161. Chromosome 5, centric fusion with one product of 1f:0, absent; 1, present.

162. Chromosome 6, primitive condition: 0, absent; 1, present.163. Chromosome 6, centric fusion with 7: 0, absent; 1, present.164. Chromosome 7, primitive condition: 0, absent; 1, present.165. Chromosome 7, proximal addition: 0, absent; 1, present.166. Chromosome 7, centric fusion with 6: 0, absent; 1, present.167. Chromosome 8: 0, absent; 1, present.168. Chromosome 8, primitive condition: 0, absent; 1, present.169. Chromosome 8, centric fusion with 3: 0, absent; 1, present.170. Chromosome 9, primitive condition: 0, absent; 1, present.171. Chromosome 9, centric fusion with 15/21: 0, absent;

1, present.172. Chromosome 9, non-reciprocal translocation with

distal region of 1: 0, absent; 1, present.173. Chromosome 10: 0, absent; 1, present.174. Chromosome 10, primitive condition: 0, absent;

1, present.175. Chromosome 10, tandem fusion with 22: 0, absent;

1, present.176. Chromosome 10, tandem fusion with 18: 0, absent;

1, present.177. Chromosome 11, primitive condition: 0, absent; 1, present.178*. Chromosome 11, centric transposition: 0, absent; 1, present.179. Chromosome 11, centric fusion with 14: 0, absent; 1, present.180. Chromosome 12, primitive condition: 0, absent; 1, present.181. Chromosome 12, tandem fusion with 13: 0, absent;

1, present.182. Chromosome 13: 0, absent; 1, present.183. Chromosome 13, centric fusion of 13/12 with another

product of 1f: 0, absent; 1, present.184. Chromosome 13, tandem fusion with 12: 0, absent;

1, present.185. Chromosome 14, primitive condition: 0, absent; 1, present.186*. Chromosome 14, centric transpositions: 0, absent; 1, present.187. Chromosome 14, interstitial deletion: 0, absent; 1, present.188. Chromosome 14, tandem fusion with 64: 0, absent; 1, present.189. Chromosome 14, centric fusion with 11: 0, absent; 1, present.190. Chromosome 15: 0, absent; 1, present.191. Chromosome 15, primitive condition: 0, absent; 1, present.192. Chromosome 15, tandem fusion with 21: 0, absent;

1, present.193. Chromosome 16: 0, absent; 1, present.194. Chromosome 16, primitive condition: 0, absent; 1, present.195. Chromosome 16, pericentric inversion: 0, absent; 1,

present.196. Chromosome 16, tandem fusion with 17: 0, absent;

1, present.197. Chromosome 17: 0, absent; 1, present.198. Chromosome 17, primitive condition: 0, absent; 1, present.199. Chromosome 17, tandem fusion with 16: 0, absent;

1, present.

J. Robovsk¥ et al. • Phylogeny of Arvicolinae

© 2008 The Authors. Journal compilation © 2008 The Norwegian Academy of Science and Letters • Zoologica Scripta, 37, 6, November 2008, pp 571–590 589

200. Chromosome 18, primitive condition: 0, absent;1, present.

201. Chromosome 18, tandem fusion with 10: 0, absent;1, present.

202. Chromosome 19: 0, absent; 1, present.203. Chromosome 19, primitive condition: 0, absent; 1, present.204. Chromosome 20: 0, absent; 1, present.205. Chromosome 20, primitive condition: 0, absent; 1, present.206. Chromosome 21: 0, absent; 1, present.207. Chromosome 21, primitive condition: 0, absent; 1, present.208. Chromosome 21, tandem fusion with 24: 0, absent; 1, present.209. Chromosome 21, tandem fusion with 15: 0, absent; 1, present.210. Chromosome 21, centric fusion of 15/21 with 9: 0, absent;

1, present.211. Chromosome 22: 0, absent; 1, present.212. Chromosome 22, primitive condition: 0, absent; 1, present.213. Chromosome 22, centric fusion with 10: 0, absent; 1,

present.214. Chromosome 23: 0, absent; 1, present.215. Chromosome 23, primitive condition: 0, absent; 1,

present.216. Chromosome 24: 0, absent; 1, present.217. Chromosome 24, primitive condition: 0, absent; 1,

present.218. Chromosome 24, pericentric inversion: 0, absent; 1, present.219. Chromosome 24, tandem fusion with 21: 0, absent;

1, present.220. Chromosome 25: 0, absent; 1, present.221. Chromosome 25, primitive condition: 0, absent; 1, present.222. Chromosome 25, distal deletion: 0, absent; 1, present.223. Chromosome 26: 0, absent; 1, present.224. Chromosome 26, primitive condition: 0, absent; 1, present.225. Chromosome 27: 0, absent; 1, present.226. Chromosome 27, primitive condition: 0, absent; 1, present.227. Chromosome 28–32: 0, absent; 1, present.228*. Chromosome 33–36: 0, absent; 1, present.229. Chromosome 37–38: 0, absent; 1, present.230. X chromosome, primitive condition: 0, absent; 1, present.231*. X chromosome, pericentric inversion: 0, absent; 1, present.232*. X chromosome, pericentric inversion: 0, absent; 1, present.233. X chromosome, distal deletion: 0, absent; 1, present.234. X chromosome, pericentric inversion: 0, absent; 1, present.235. X chromosome, pericentric inversion: 0, absent; 1, present.236*. X chromosome, pericentric inversion: 0, absent; 1, present.

Morphology: external characters and proportions237. Eyes: 0, large; 1, medium-sized; 2, small [ordered].238. Pinna: 0, small; 1, medium-sized or large.239. Antitragus: 0, absent or poorly developed; 1, small;

2, well-developed [ordered].240. Number of plantar tubercles: 0, six; 1, five; 2, four;

3, three or less [ordered].

241. Number of mammae: 0, 10–22; 1, eight; 2, six; 3, four[ordered].

242. Forelimb, thumb: 0, well-developed; 1, small; 2, stronglyreduced to absent [ordered].

243. Forelimb, thumb nail: 0, well-formed; 1, small;2, strongly reduced to absent [ordered].

244. Forelimb, thumb nail laterally flattened andslightly bifurcate: 0, absent; 1, present.

245. Forelimb, third digit nail strongly bifurcate andenlarged: 0, absent; 1, present.

246. Genal vibrissae: 0, absent; 1, short; 2, long[ordered].

247. Dorsal pelage coloration: 0, grey, silver–grey, brown–grey; 1, fox orange, cinnamon; 2, brown to dark–brown;3, black; 4, ochre.

248. Ventral pelage coloration: 0, white; 1, grey to silver–grey; 2, ochre, buff, brown.

249. Tail: 0, monochromatic; 1, dichromatic.250. Middorsal longitudinal black stripe: 0, absent; 1, present. 251. Yellow snout: 0, absent; 1, present.252. Seasonal exchange of the fur: 0, inconspicuous;

1, well-expressed; 2, bichromatism [ordered].253. Body length (in mm): 0, 50–90; 1, 91–130; 2, 131–170;

3, 171–210; 4, 211–250; 5, 251–290; 6, 291 and more[ordered].

254. Tail length (in mm): 0, 0–30; 1, 31–60; 2, 61–90; 3,91–120; 4, 121–150; 5, 151–180; 6, 181–210; 7, 211 and more[ordered].

255. 1st lower molar length (in mm): 0, 1.3–1.9; 1, 2.0–2.5;2, 2.6–3.1; 3, 3.2–3.7; 4, 3.8–4.3; 5, 4.4–4.9; 6, 5.0 and more[ordered].

256. Hind foot/head-body length (in percent): 0, 11.0–13.9; 1, 14.0–16.9; 2, 17.0–19.9; 3, 20.0–22.9; 4, 23.0–25.9; 5,26.0–28.9 [ordered].

Ecology, development, behavior257. Male/female body mass dimorphism: 0, < 1; 1, 1.0–

1.2; 2, > 1.2 [ordered].258. Male/female body length dimorphism: 0, < 1; 1, 1.0–

1.05; 2, > 1.06 [ordered].259. Testis length/male body length: 0, < 0.08; 1, 0.08–0.1;

2, > 0.1 [ordered].260: Intromission latency: 0, < 200; 1, 200–500; 2, > 500

[ordered].261: Intromission frequency: 0, < 1; 1, 1–5; 2, > 5 [ordered].262. Ejaculation frequency: 0, < 3; 1, ≥≥≥≥ 3.263. Percentage of males that attained satiety after first

ejaculation: 0, < 50; 1, 50–60; 2, 60 [ordered].264. Gestation period (in days): 0, < 20; 1, 20–21; 2, > 21

[ordered].265. Neonate weight (in grams): 0, < 3; 1, 3–10; 2, > 10

[ordered].

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266. Specific reproductive effort (SREn; sensu Bekoff et al.1981): 0, < 0.5; 1 ≥ 0.5.

267. Weaning weight (in grams): 0, < 10; 1 ≥ 10.268. Specific reproductive effort (SREw; sensu Bekoff et al.

1981): 0, < 1.4; 1, 1.4–2; 2, > 2 [ordered].269. Mean litter size: 0, < 3; 1, 3–5.5; 2, > 5.5

[ordered].270. Ear formation (in days): 0, < 3; 1, ≥ 3.271. Eruption of lower incisors (in days): 0, < 5; 1, ≥ 5.272. Eruption of upper incisors (in days): 0, < 5; 1, ≥ 5.273. Development of incisors, timing: 0, lower early;

1, both incisors simultaneous; 2, upper early [ordered]. 274. Separation of forefeet digits (in days): 0, < 9; 1, ≥ 9.275. Separation of hind feet digits (in days): 0, < 10.5; 1, ≥ 10.5.276. Eyes opening (in days): 0, < 11; 1, ≥ 11.277. First solid food (in days): 0, < 14; 1, ≥ 14.278. Age of weaning (in days): 0, < 16; 1, ≥ 16.279. Growth rate (in grams/day): 0, < 0.6; 1, ≥ 0.6.280. Exclusive female territories: 0, absent; 1, present.281. Female groups: 0, absent; 1, female kin clusters (common

home range but exclusive nests); 2, group of two or more usuallyrelative breeding females, sharing one nest [ordered].

282. Male spatial organization: 0, non-territorial; 1, exclusivemale territory; 2, pairs and groups of both sexes defendinga common territory.

283. Male-female breeding unit: 0, absent; 1, facultative;2, obligatory [ordered].

284. Groups: 0, absent; 1, communal groups (unrelated

animals defending a common territory (promiscuous breeding);2, polygynous groups; 3, polyandrous groups.

285. Sociality: 0, no cooperative breeding; only temporalassociation between adults; 1, cooperative breeding, year-roundassociation between adult females with a common territory;2, cooperative breeding, year-round male–female associationwith multigenerational occupancy of the territory (or homerange), two or more reproductive females; 3, cooperativebreeding, year-round male–female association with multi-generational occupancy of the territory (home range), singlereproductive female.

286. Male–female huddling (in min): 0, < 10; 1, 10–30;2, > 30 [ordered].

287. Breeding season (in months): 0, < 5; 1, 6–11; 2, 12[ordered].

288. Group size: 0, < 1; 1, 1.5–2.5; 2, > 3 [ordered].289. Habitat: 0, semidesert, steppe to forest–steppe; 1,

hydrophilous meadows, marshland, riverine habitats; 2, forest;3, forest–tundra to tundra; 3, montane to alpine habitats.

290. Preferred microhabitat: 0, moist; 1, mesic; 2, dry[ordered].

291. Preferred microhabitat: 0, rocky; 1, soil.292. Dominant vegetation in preferred habitat: 0, lichens,

mosses; 1, herbs; 2, graminoids; 3, deciduous trees; 4, coniferous trees.293. Digging: 0, by using claws; 1, by using incisors.294. Nest location: 0, underground; 1, on the ground; 2,

above the ground [ordered].295*. Nest location in water: 0, absent; 1, present.