Water voles (genus Arvicola Lacépède, 1799) are extraordinary among the Palaearctic rodents for their outstanding phenetic and ecological plasticity. Two morphological types can be distinguished, the aquatic and the fossorial, each with different living habits (Meylan 1977). This variability has caused a long-standing dispute over the number of species within the genus. Whereas Ellerman and Morrison-Scott (1951) clumped a wide array of morphological forms under one nominal species, A. terrestris (Linnaeus, 1758), Hinton (1926) recognized four species and Miller (1912) listed seven species for Western Europe only. Since 1970, the majority of authors have accepted a division into two species: A. sapidus Miller, 1908 with a small range in Western Europe, and a widespread and polytypic A. terrestris (Corbet 1978, Niethammer and Krapp 1982 Gromov and Polyakov 1992, Shenbrot and Krasnov 2005). Within the latter, Ognev (1964) distinguished two species, the fossorial A. scherman (Shaw, 1801) and the aquatic A. terrestris. Ognev’s taxonomic arrangement was largely ignored, but gained credit after being adopted in the influential compilation by Musser and Carleton (2005). The genus Arvicola is currently regarded as consisting of two aquatic (sapidus, amphibius) and one fossorial species (scherman). Musser and Carleton (2005) even anticipated “that future revisionary research will […] converge towards Miller’s (1912) recognition of biodiversity”, i.e., in an increase in the species of water voles. Evidently, our understanding of species limits in the genus Arvicola is still far from final.
Arvicola sapidus, which is endemic to the Pyrenean Peninsula and France (Shenbrot and Krasnov 2005), possesses a unique set of chromosomes (Matthey 1956) and is therefore well defined taxonomically. We shall subsequently focus on two species that result from splitting A. terrestris (sensu Corbet 1978) into A. amphibius (Linnaeus, 1758) and A. scherman (Musser and Carleton 2005). The names amphibius and terrestris are synonymous and the former has priority based on the principle of first reviser (Corbet 1978). Both names were used interchangeably in the past. To avoid confusion, we shall subsequently use amphibius sensu stricto (s.s.) in the sense of Musser and Carleton (2005), and amphibius sensu lato (s.l.) to contain Musser and Carleton’s amphibius s.s. and scherman.
The range of Arvicola amphibius s.s. stretches from Western Europe to the River Lena in eastern Siberia (Batsaikhan et al. 2008). The geographic scope of A. scherman is more restricted, but it is also poorly resolved. Hinton (1926) believed that its range extends over “Central Europe from the Baltic southwards to the Pyrenees”, also encompassing the Alps. Panteleyev (2001) and Amori et al. (2008a) mapped A. scherman for the mountainous regions in northern Spain and the Pyrenees, the Alps, the mountains of Central Europe, and the Carpathians. The two species are presumably allopatric in the south, but show overlapping ranges in the north (e.g., Meylan 1977).
Arvicola voles, which typically possess rootless molars, presumably evolved from the extinct rhizodont Mimomys Forsyth Major, 1902, and have been known in the fossil record since the beginning of the Early Pleistocene (Gromov and Polyakov 1992). Therefore, the taxonomic richness in Arvicola results from a relatively recent radiation and the species may still be in an ongoing speciation process. In such cases, which are common in arvicolines (e.g., Jaarola et al. 2004), molecular data provide vital insight into past cladogenetic events and current species limits. In the present study, we used mitochondrial cytochrome b (cytb) gene sequences to reconstruct phylogenetic relationships between the fossorial and the aquatic water voles from various regions of their European and Asiatic range. Our aim was to test the taxonomic arrangement of A. amphibius s.l. Our null hypothesis predicted the reciprocal monophyly of the aquatic and the fossorial morphotypes. If our hypothesis would not be rejected, the results will support the current tripartite taxonomic arrangement of the genus Arvicola.
Materials and methods
We studied the mitochondrial genetic makeup of water voles from Switzerland, Austria, Hungary, Slovenia, Bosnia and Herzegovina, Serbia, Romania, Turkey, and Russia (Figure 1, Table 1). Voucher specimens (skins and skulls, or wet specimens) were preserved for the majority of sequenced individuals. They are deposited in the Slovenian Museum of Natural History (PMS; Ljubljana, Slovenia), Naturhistorisches Museum Wien (NMW; Vienna, Austria), “Grigore Antipa” National Museum of Natural History (Bucharest, Romania), and the Department of Biology, Selçuk University (Konya, Turkey). Tissue samples are deposited in the PMS and NMW.
We examined museum specimens of water voles for their morphology. Included in the study were individuals sequenced for cytb but also museum vouchers of unknown genetic makeup from the same site as the genotyped material. Swiss and German sequences were downloaded from GenBank and their morphotype was not reported (Pfunder et al. 2004, Schlegel et al. 2012b). Swiss samples were from the range of a subspecies scherman (Meylan and Saucy 1995) and were assigned on this ground to the fossorial morphotype. German water voles were not classified into the morphotype.
Identification was based on character states and five linear measurements (three external and two cranial) that are used in determination keys (see references in the next paragraph). Measurements were scored only in full grown voles (age groups V and VI of Hinton 1926) with complete skulls: H&B – length of head and body; TL – length of tail; HF – length of hind foot (without claws); condylobasal length of skull (CbL); and length of molar tooth-row (MxT). External measurements were obtained from specimen tags and skull dimensions were measured using a dial calliper to the nearest 0.1 mm.
Morphological differences between the morphotypes were compiled from Miller (1910), Hinton (1926), Ognev (1964), and Panteleyev (2001). In line with these authors, the aquatic morphotype attains larger dimensions (H&B >165 mm, HF ≥28 mm, CbL >36 mm, MxT ≥9 mm), has a longer tail (>98 mm), less reduced palmar and plantar pads, orthodont upper incisors, and nearly vertically truncated occiput. The fossorial morphotype is smaller (H&B ≤160 mm, HF ≤27 mm, CbL ≤36 mm, MxT ≤9 mm), with a shorter tail (TL ≤98 mm), more reduced palmar and plantar pads, protruding (proodont) incisors that are less concealed by the lips, and the occiput is inclined.
This study consisted of 69 Arvicola samples from 29 localities in Austria, Hungary, Slovenia, Bosnia and Herzegovina, Serbia, Romania, Turkey, and Russia. A further 15 haplotypes from Germany and Switzerland and five haplotypes of A. sapidus (FJ539341-5; Centeno-Cuadros and Godoy 2010) were downloaded from the GenBank database (Table 1).
DNA was extracted from muscle samples preserved in 96% ethanol using a QIAamp DNA Mini kit (Qiagen, Valencia, CA, USA). A 1117-bp mitochondrial cytb fragment was amplified using a polymerase chain reaction combining the following primers: L14725 (Steppan et al. 1999); L14931 (Harrison et al. 2003); H15915-SP (Jaarola and Searle 2002); L15162Marv, L15408Marv (Haynes et al. 2003); and H15497-SP (Jaarola et al. 2004). Forward and reverse sequencing was performed on an ABI PRISM 3130 Genetic Analyzer (Applied Biosystems, Foster City, CA, USA) using BigDye chemistry (Applied Biosystems). The sequences were checked for the absence of stop-codons and chimeric sequences.
Nucleotide, amino acid composition, and genetic distances were analyzed assuming a Kimura 2 parameter (K2P) sequence evolution with 104 bootstraps in the MEGA v. 6 program (Tamura et al. 2013). The most appropriate models of DNA substitution for the data were identified using MRMODELTEST 2.3 (Nylander 2004). Both the Akaike information criterion (AIC) and the hierarchical likelihood ratio test (hLRT) were used. Phylogenetic analysis was conducted with the Bayesian inference (BI), using the program MRBAYES 3.1.2 (Huelsenbeck and Ronquist 2001, Ronquist and Huelsenbeck 2003), and maximum likelihood (ML) as implemented in the program PhyML 2.4.5 (Guindon and Gascuel 2003, Anisimova and Gascuel 2006).
The phylogenetic inferences were performed with a general time-reversible model (GTR) + gamma distribution (G) + proportion of invariable sites (I) (G=0.6125 and I=0.5557). Four Monte Carlo Markov chains were run simultaneously for 6.5×106 generations, with the resulting trees sampled every 500 generations. Bayesian posterior probabilities (BPP) were used to assess branch support of the BI tree. Convergence for posterior probabilities was checked by examining the generation plot visualized with TRACER v1.4 (Rambaud and Drummond 2007).
The GTRGAMMA model was used for ML analysis. Branch support (BP) in the ML tree was estimated by 103 bootstrap replicates. The topologies resulting from these two methods were compared using a Shimodaira-Hasegawa test (Shimodaira and Hasegawa 1999) implemented in PAUP* 4.010b (Swofford 2002) with 103 bootstrap replicates. In line with other authors, we accepted BPP >0.95 as “good”, and BPP=0.90–0.95 as “moderate” support. For branch support in the ML tree we considered BP >90% as “good” support, and BP=80–90% as “moderate” support.
Trees were rooted with 11 species of Palaearctic arvicolines from three genera, which are probably closely related to Arvicola (Martínková and Moravec 2012): Chionomys gud (Satunin, 1909) (GQ352457; Bannikova et al. 2010), C. roberti (Thomas, 1906) (GQ352459; Bannikova et al. 2010), C. nivalis (Martins, 1842) (AY513848; Jaarola et al. 2004), Microtus arvalis (Pallas, 1778) (GU197810; Martínková et al. 2013), M. agrestis (Linnaeus, 1761) (DQ662099; Schmidt-Chanasit et al. 2010), M. cabrerae (Thomas, 1906) (JX457758; Barbosa et al. 2013), M. duodecimcostatus (de Selys-Longchamps, 1839) (JX457806; Barbosa et al., 2013), M. lusitanicus (Gerbe, 1879) (JX457796 JX457796; Barbosa et al. 2013), M. subterraneus (de Selys-Longchamps, 1839) (JN019755; Rovatsos and Giagia-Athanasopoulou 2012), Neodon irene (Thomas, 1911) (JF906127; Chen et al. 2012), and N. leucurus (Blyth, 1863) (AM392371; Galewski et al. 2006).
We further analyzed the data by SAMOVA 1.0 implemented in Dupanloup et al. (2002). The objective was to find groups of sampling localities that were maximally differentiated from each other. The number of populations that maximized variation among groups (FCT) was the number of populations assumed to be correct. The comparison of all pairwise K2P values and the geographic distances was performed using 1000 permutations in the Mantel test implemented in Rohlf (1994).
Of the 67 adult water voles examined morphologically, 44 individuals were fossorial and 23 were aquatic. There was a good match between the orientation of the upper incisors (Figure 2) and size. In line with published data (see references in Material and methods), voles with proodont upper incisors (fossorial type) were also smaller (CbL=32.42±0.407), whereas the orthodont voles of the aquatic morphotype attained larger dimensions (CbL=36.84±0.622). In addition, the fossorial water voles showed a shorter tail relative to HbL (TL=40–59% of HbL) than aquatic voles (TL=48–82% of HbL). The two morphotypes showed strong geographic associations (Figure 1). In accordance with published evidence (e.g., Panteleyev 2001), our fossorial voles originated from the Alps and the Carpathians, and aquatic voles were collected in southeastern Europe, Turkey in Asia, and western Siberia.
Altogether, 50 new haplotypes were found in our material from Europe and Asia, generating a total dataset of 70 different water vole cytb haplotypes (Pfunder et al. 2004, Centeno-Cuadros and Godoy 2010, Schlegel et al. 2012a,b). Within the 1117-bp long sequences considered here, 106 polymorphic sites were found with a total of 140 mutations, 105 of which were parsimony informative. No stop codons, insertions, or deletions were observed in the alignment. The mean transition/transversion ratio was 5.90. The nucleotide composition was characterized by a deficit of guanines (13.8%), similar to that described in other mammals (Irwin et al. 1991).
Phylogenetic relationships among Arvicola haplotypes that were reconstructed by the two different methods (ML and BI) yielded highly similar results, and the Shimodaira–Hasegawa test did not reveal significant differences between them (SH=0.23). Consequently, only the BI tree is shown (Figure 3). In line with published results (Taberlet et al. 1998), both trees retrieved strongly (BP=100%, PP=1.00) supported basal dichotomy into A. sapidus and A. amphibius s.l. Within the latter, a branching pattern yielded congruent results at terminal nodes but presented inconsistency at deeper nodes. Fossorial water voles from Switzerland hold a sister position against the remaining haplotypes, which demonstrated strong support (PP=0.99) in the BI analysis. The basal position of the Turkish haplotypes was evident in both trees, but remained unresolved due to poor branch supports. The next major branching was a supported (PP=0.95) divergence into the Siberian and European lineages. The prevailing pattern within the European lineage was a supported (PP=0.99) polytomy. Geographic association was particularly obvious in a cluster of Austrian and German haplotypes that radiated further into a number of sublineages. The Turkish and Siberian lineages contained only aquatic water voles, whereas the only monophyletic lineage of purely fossorial water voles was the Swiss lineage. The major European lineage contained both large aquatic and small fossorial water voles. These morphotypes were strictly allopatric in our samples.
The highest percentage of variance among groups (67.2%) was obtained when samples of Arvicola amphibius s.l. were classified into three groups, which corresponded to the three lineages retrieved in the above phylogenetic analyses: Swiss, Turkish, and European + Siberian combined. The results were therefore in congruence with the haplotype geographic distribution and supported strong association of haplotypes with geographic location.
The highest K2P genetic distance (in percentages) was between Arvicola sapidus and the remaining lineages (6.2±0.9). Within A. amphibius s.l., K2P genetic distances were not correlated with geographical distances among samples (matrix correlation r=0.136, t=0.479, p=0.68). The K2P value was the highest (4.1±0.72) between the fossorial Swiss water voles and the remaining samples, the lowest (1.6±0.3) between the Siberian and the European lineages, and intermediate (2.3±0.5) between the Turkish and the combined Siberian + European lineages. Within-group divergence was the highest in the European lineage (1.2±0.2), lowest in the Siberian (0.5±0.2) and Turkish lineages (0.6±0.3), and intermediate in the Swiss fossorial lineage (0.9±0.2).
Species of water voles
Molecular reconstructions of extant water voles retrieved four major evolutionary lineages (Taberlet et al. 1998, and our results) instead of three clusters as predicted by the current taxonomic arrangement (Musser and Carleton 2005). Topology of phylogenetic trees provided no support for basal aquatic-fossorial dichotomy in Arvicola amphibius s.l., and instead suggests multiple origins of small proodont water voles. Similarly, the pattern of variation in the distribution and amount of constitutive (C-) heterochromatin variation is not related to a morphotype of individual populations of A. amphibius (Arslan et al. 2011). Basal dichotomy in Arvicola between A. sapidus (having 40 chromosomes) and the remaining water voles with 36 chromosomes (e.g., Meylan 1977) is undoubtedly indicative of a speciation event. The two cytotypes are broadly sympatric in Spain and France (Shenbrot and Krasnov 2005), and the genetic variation from the mitochondrial cytb gene (7.6% in Taberlet et al. 1998, 6.2% in our results) is within the range for interspecific differences in rodents (Baker and Bradley 2006). Furthermore, there is no evidence of mitochondrial gene flow between A. sapidus and A. amphibius s.l. in their zone of contact (Centeno-Cuadros et al. 2009). K2P divergence between A. terrestris italicus (sensu Taberlet et al. 1998; hereafter the Italian lineage) and the remaining lineages of A. amphibius s.l. is tentatively estimated from Taberlet et al. (1998) to be about 5%, and the divergence of the Swiss fossorial lineage in our study accounts for 4.1%. In rodents, genetic divergences of ≤4.1% are tentatively indicative of intraspecific variation and those of ≥4.9% putatively suggest interspecific variation (Baker and Bradley 2006). Therefore, major divergences in A. amphibius s.l. can be equally well interpreted as high intraspecific or low interspecific variation. Graf (1982) reached similar conclusions in a study based on the electrophoresis of allozymes. Captive crossbreeding between two morphotypes from Switzerland (putatively representing the fossorial Swiss lineage in our results, and the Italian lineage) retrieved partial sterility of the F1 progeny, therefore suggesting some reproductive isolation between major phylogeographic lineages of A. amphibius (Saucy et al. 1994). Conversely, Kleist (1996) successfully crossbred aquatic and fossorial water voles originating from Germany.
Clearly, further sampling is essential to define geographic limits of major phylogroups and explore zones of contact or overlap between them. Molecular results that have been obtained thus far and discussed above suggest that the taxonomy of A. amphibius s.l. is a complex issue that cannot be resolved by a simple division into the aquatic and fossorial species. The data presented herein make it very unlikely that A. scherman forms a single monophyletic taxon. However, a very recent split between fossorial and aquatic morphotypes in the European lineage may still be detected after analyzing additional genes and obtaining a larger dataset of sequences.
Survival in refugia
The four lineages of water voles bear witness to the main cladogenetic events during the evolutionary history of the genus Arvicola. Considering the time of split of the common ancestor of A. sapidus and A. amphibius s.l., which is estimated at about 252 kya (Centeno-Cuadros et al. 2009), the lineages of the latter must have diverged during the last two major glacial-interglacial cycles, the Saalian (Riss) and the Vistulian (Würm). Clearly, the phylogeographic architecture in water voles is a legacy of Quaternary climatic dynamics. Just as it was the case with numerous temperate taxa (Taberlet et al. 1998, Hewitt 2000), the range of Arvicola was repeatedly fragmented by expanding glaciers and isolated populations began to diverge in relatively small refugial areas.
Deeply divergent lineages of water voles were retrieved only at the extreme western edge of the extensive range of the genus, suggesting that Western and southwestern Europe have acted as a major centre for the diversification of Arvicola. Namely, the more ancient the lineage, the more westward it tends to be located. Therefore, A. sapidus occupies the extreme western border of Arvicola, being followed further east by two ancient lineages, the Swiss and the Italian. Phylogeographic studies of widespread Palaearctic arvicolines repeatedly retrieved high genetic diversity in Western and Central Europe, which contrasts the genetic uniformity in Eastern Europe and Asia. Although each species has its own geographic pattern of genetic architecture, a west-to-east decay in distribution of genetic diversity is clearly evident in various arvicolines, e.g., Clethrionomys glareolus (Wójcik et al. 2010), Microtus oeconomus (Brunhoff et al. 2003), Microtus agrestis (Jaarola and Searle 2002, Herman and Searle 2012), and Microtus arvalis (Haynes et al. 2003, Tougard et al. 2008).
Many authors report fossorial water voles for higher altitudes and aquatic populations for lower altitudes (see Panteleyev 2001), which suggests the competitive advantage of a particular morphotype under certain environmental conditions. However, the reality is more puzzling and fossorial water voles are also frequently encountered in the lowlands (Meylan 1977), whereas aquatic animals occupy mountains in some parts of Europe (e.g., the Balkans) and Asia (Asia Minor, Caucasus, Altai; authors’ field observations). The issue is further complicated by morphological forms “which are [not] solely fossorial” (Meylan 1977).
The fossorial morphotype presumably originated from the aquatic one through a heterochronic process of accelerated dwarfism (Cubo et al. 2006). Although some populations remain morphologically stable across years, others are more plastic in this respect (Panteleyev 2001). Namely, water voles can show considerable ecological adaptation and respond morphologically even to seasonal dynamics in resources, e.g., those occupying the banks of large rivers change morphologically in response to floods (Panteleyev et al. 1978). It is intriguing to speculate that fossorial and aquatic water voles might be at the extremes of a putative phenotypic continuum, rather than representing two discrete morphotypes. Well-controlled morphometric analyses must be an integral part of any comprehensive taxonomic assessment of this interesting rodent genus.
We would like to thank Mrs. Karolyn Close for the English editing and Mr. Peter Glasnović for his help with Figure 1.
The Appendix is aimed to assist the reader with the nomenclatural component of our study by listing main synonyms and those taxonomic names that are related to our sampling localities. Names are given chronologically and follow the taxonomic arrangement of Musser and Carleton (2005). Junior synonyms of Arvicola amphibius and A. scherman (sensu Musser and Carleton 2005) are listed as trinomials but with no intention of implying their actual taxonomic status. Therefore, trinomials are the available species group names although they do not necessarily merit a subspecific rank. If not indicated otherwise, type localities are from Ellerman and Morrison-Scott (1951). Chromosomal data follow Zima and Král (1984).
Arvicola amphibius (Linnaeus, 1758)
Type locality: England.
Notes: The oldest available species group name in the genus, which is based on large, orthodont and strictly aquatic water voles (Miller 1912) with 36 chromosomes. Precedence of amphibius over terrestris is legitimized by the Principle of the First Reviser (Article 24.2. of the International Code of Zoological Nomenclature, 4th ed.) and follows Blasius (1857) (cf. Corbet 1978).
Arvicola terrestris (Linnaeus, 1758)
Type locality: Upsala, Sweden.
Notes: Moderately large aquatic voles with a skull showing “a decided tendency to assume a fossorial structure.” “[H]abits both aquatic and mole-like” (Miller 1912). Priority of terrestris over amphibius was accepted by Ellerman and Morrison-Scott (1951), Ognev (1964), and numerous subsequent authors.
Arvicola scherman (Shaw, 1801)
Type locality: Strasbourg, Bas Rhin, Eastern France.
Notes: Small and proodont water voles adapted to fossorial mode of life. Recognized as species on its own right already by Miller (1912) and Ognev (1964).
Arvicola amphibius italicus Savi, 1838
Type locality: Vicinity of Pisa, Italy.
Notes: Well-defined form of large, orthodont, and strictly aquatic water voles with 36 chromosomes. For 1838 as the year of publication (instead of 1839; cf. Miller 1912) see Gippoliti (2012). Range is restricted to peninsular Italy (Amori et al. 2008b) and Canton Tessin in Switzerland (Meylan and Saucy 1995); borders are not resolved.
Arvicola scherman exitus Miller, 1910
Type locality: St. Gallen, Switzerland.
Notes: Small, proodont, and strictly fossorial water voles (Miller 1912). The name exitus is probably applicable to sequences from Switzerland (pts. 8–10 on Figure 1), which we downloaded from the GenBank.
Arvicola amphibius persicus De Filippi, 1865
Type locality: Sultanieh, south of Elbruz Mountains, Persia (=Iran).
Notes: Contains large, orthodont, and strictly aquatic water voles (Kryštufek and Vohralík 2005) with 36 chromosomes (Arslan et al. 2013). This is the oldest name for water voles from the Middle East and is applicable to our samples from Anatolia (pts. 25 and 26 on Figure 1). Taxonomic scope is not resolved unambiguously but persicus probably contains as junior synonyms Microtus terrestris armenius Thomas, 1907 (Type locality: Van, 5000 ft., Eastern Asia Minor) and Arvicola terrestris hintoni Aharoni, 1932 (Type locality: Island of Tel el Sultan, Antioch Lake, Northern Syria) (Ellerman and Morrison-Scott 1951, Ognev 1964, Kryštufek and Vohralík 2005).
Arvicola amphibius illyricus (Barrett-Hamilton, 1899)
Type locality: Bosnia (no exact locality).
Notes: Contains large, orthodont, and strictly aquatic water voles (Petrov 1949). Our sample from Kupres (pt. 22 in Figure 1) is topotypical with this name.
Arvicola sapidus Miller, 1908
Type locality: Santo Domingo de Silos, Burgos, Spain.
Notes: A large, orthodont, and strictly aquatic species with 40 chromosomes. Range restricted to Spain, Portugal, and western France; mapped in Ventura (2002) and Shenbrot and Krasnov (2005).
Arvicola amphibius variabilis Ognev, 1933
Type locality: Barabinsk steppes Govt. Tomsk, Siberia.
Notes: Large, orthodont, and aquatic water voles. Arvicola terrestris variabilis Ognev, 1933, is preoccupied by Arvicola arvalis form variabilis Rörig et Börner, 1905 (now a junior synonym of Microtus arvalis) and was renamed Microtus terrestris barabensis Heptner, 1948. This name (sensu Gromov and Erbajeva 1995) is applicable to our samples from Russia (pts. 27–29 on Figure 1).
Arvicola amphibius martinoi Petrov, 1949
Type locality: Vicinity of Belgrade, Serbia (Petrov 1949).
Notes: Includes large and aquatic water voles (Petrov 1949). Our specimen from Dubovac, Serbia (pt. 21 in Figure 1) originates from the vicinity of the type locality for this name.
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