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The Italian Peninsula Hosts a Divergent Mtdna Lineage of the Water Vole, Arvicola Amphibius S.L., Including Fossorial and Aquatic Ecotypes

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The Italian Peninsula Hosts a Divergent Mtdna Lineage of the Water Vole, Arvicola Amphibius S.L., Including Fossorial and Aquatic Ecotypes Published by Associazione Teriologica Italiana Volume 27 (2): 99–103, 2016 Hystrix, the Italian Journal of Mammalogy Available online at: http://www.italian-journal-of-mammalogy.it doi:10.4404/hystrix–11588 Research Article The Italian peninsula hosts a divergent mtDNA lineage of the water vole, Arvicola amphibius s.l., including fossorial and aquatic ecotypes Riccardo Castiglia1,∗, Gaetano Aloise2, Giovanni Amori3, Flavia Annesi1, Sandro Bertolino4, Dario Capizzi5, Emiliano Mori4, Paolo Colangelo3 1Dipartimento di Biologia e Biotecnologie “Charles Darwin”, Università di Roma “La Sapienza”, 00151 Rome, Italy 2Museo di Storia Naturale della Calabria e Orto Botanico, Università della Calabria, 87036 Rende (CS), Italy 3CNR – Institute of Ecosystem Studies, Viale dell’Università 32, 00185 Rome, Italy 4Dipartimento di Scienze Agrarie, Forestali e Alimentari, Università degli Studi di Torino, 10095 Grugliasco (TO), Italy 5Regione Lazio – Agenzia Regionale per i Parchi, via del Pescaccio 96, 00166 Rome, Italy Keywords: Abstract Italian peninsula phylogeography We characterized eighteen water voles, Arvicola amphibius (s.l.), from five populations along the water vole Italian peninsula by means of mtDNA cytochrome b (Cytb) sequences. The samples included karyotype aquatic voles and one fossorial population from northern Italy. The standard karyotype of four voles from one central Italian population was also analysed and was identical to the one found in Article history: other populations outside Italy. Phylogenetic analyses, including vole Cytb haplotypes from the en- Received: 4 November 2015 tire range, indicated the existence of a wellsupported and highly divergent Italian lineage (4.3%), Accepted: 29 March 2016 sister to all the other haplotypes. The fossorial voles are not genetically differentiated from the aquatic voles from a nearby population and belong to the same taxon. Given the high Cytb diver- gence and the results of previous investigations on allozymes and hybrid fertility, we believe that Acknowledgements the Italian population of water voles belongs to a distinct species, Arvicola italicus Savi, 1838, with We are grateful to the technicians of CReSO Saluzzo and the farmers that gave us some animals and permission to work in their orchards. the type locality near Pisa, although a morphological assessment of the entire skull is necessary to The Parco Fluviale del Po e dell’Orba gave us permission to capture define it. animals in protected areas. Daniele Pariselli and Francesco Goggi helped us to capture individuals from the Fondi and San Genuario populations respectively. Giuliano Milana and Germana Spuznar provided tissues from individuals from Popoli. Thanks are extended to two anonymous reviewers and to the associate editor. R. Castiglia received grants from Università di Roma “La Sapienza” and PRIN (2012). Introduction a profound change in the taxonomy of Arvicola, which cannot be sum- Water voles (genus Arvicola Lacépede, 1799) are characterized by an marized better than the title of the work itself: “Fossorial morphotype extraordinary morphological and ecological plasticity. Two ecological does not make a species in water voles”. Briefly, the mtDNA phylo- types (ecotypes) can be distinguished, the aquatic and the fossorial, genetic reconstructions of the extended sample failed to identify two each with different living habits (Meylan, 1977). These ecotypes are reciprocally monophyletic groups matching A. amphibius and A. scher- often morphologically distinct (Meylan, 1977) and this variability has man. Instead they revealed a major clade, hereafter called A. amphibius caused a long-standing dispute concerning the species limits within the sensu lato (s.l.) subdivided into two lineages. One lineage is distrib- genus. The two extreme positions were exemplified by the clumping of uted from Europe to western Siberia (herein called Euroasiatic clade) the different forms under one nominal species A. terrestris (Linnaeus, and includes both aquatic and fossorial water voles. The second lin- 1758) (Ellerman and Morrison-Scott, 1951) versus the recognition of eage includes a few populations of strictly fossorial Swiss voles (herein seven species (for western Europe alone) by Miller (1912) . called Western European clade) (Fig. 1). This pattern renders A. scher- The more recent revision by Musser and Carleton (2005) divided the man sensu Musser and Carleton (2005) undeserving of species status. genus into three species. Two of them are aquatic: A. sapidus (2n=40) In this context, the taxonomic position of Italian Arvicola popula- (Miller, 1908), endemic to the Iberian Peninsula and France, and A. am- tions was neglected. Aquatic voles are distributed with scattered pop- phibius (2n=36), stretching from western Europe to the River Lena in ulations throughout the Italian Peninsula. A previous genetic analysis eastern Siberia (Shenbrot and Krasnov, 2005; Batsaikhan et al., 2008). based on cytochrome b (Cytb) mtDNA genes indicated the presence of The third species, the fossorial A. scherman (2n=36) (Shaw, 1801), is divergent haplotypes in the peninsula (Taberlet et al., 1998). However mainly distributed in the upland regions of northern Spain, the Pyren- the exact location of the sampled population was not indicated and the ees, the Alps, the mountains of central Europe and the Carpathians, but relative sequences were not deposited in public databases. is also recorded in plains and hilly areas (Cagnin , 2008). The need of more precise genetic information on Italian voles is A recent morphological and molecular phylogenetic study includ- shown by the current taxonomy, which considers the aquatic voles liv- ing fossorial and aquatic water voles from various regions of their ing in Italy as belonging to two endemic taxa (Gippoliti, 2012) deemed European and Asiatic range (Kryštufek et al., 2015) lay the basis for to be subspecies (Cagnin , 2008): “A. amphibius italicus” Savi, 1839, restricted to the central-northern part of Italy, and “A. amphibius musig- nani” de Sélys Longchamps, 1839, thought to be distributed in central- ∗Corresponding author southern Italy. Strictly fossorial voles (“A. scherman”) are known only Email address: [email protected] (Riccardo Castiglia) from a few localities in north-eastern Italy (Lapini and Paolucci, 1994) Hystrix, the Italian Journal of Mammalogy ISSN 1825-5272 30th May 2016 ©cbe2016 Associazione Teriologica Italiana doi:10.4404/hystrix–11588 Hystrix, It. J. Mamm. (2016) 27(2): 99–103 Table 1 – Details of the specimens used for the analysis: localities, morphotypes and length of the sequenced Cytb fragment. Locality – n° on map N Morphotype Karyotype Cytb Verzuolo (Piedmont) – 1 8 Fossorial – 1081bp San Genuario (Piedmont) – 2 2 Aquatic – 647bp Fondi (Latium) – 3 4 Aquatic yes 647bp Popoli (Abruzzo) – 4 2 Aquatic – 1081bp Sila Grande M.ts (Calabria) – 5 2 Aquatic – 1081bp The Cytb sequences were isolated with universal primers L14723 and H15915 (Irwin et al., 1991). A shorter fragment was amplified from more problematic samples with a new designed reverse primer Figure 1 – The distribution of Arvicola amphibius s.l. in Europe (light grey). Triangles and H15408M arv (5’ – TGA AAG GG ATT TTA TCT GC – 3’) used to- crosses indicated the distribution of the Western European clade and of the Euroasiatic clade respectively. White square and dots indicated the Italian respectively fossorial and gether with 14727-SP (5’ – GAC AGG AAA AAT CAT CGT TG – acquatic samples analysed in this study. 3’) (Jaarola and Searle, 2002) for amplification. Amplifications were performed by polymerase chain reaction (PCR) in a Biometra Thermo- cycler machine. The resulting sequences ranged from 647 to 1081 bp (see Tab. 1, accession numbers LT546145-62, European Nucleotide and recently in Piedmont, north-western Italy (Capizzi and Santini, Archive - ENA) 2007; Bertolino S., unpublished data). In this study we characterized populations of Arvicola amphibius Phylogenetic analyses s.l. along the Italian peninsula through molecular (mtDNA Cytb) and cytogenetic markers. The samples included aquatic voles and the newly In order to build a comprehensive phylogenetic tree, we downloaded A. amphibius s.l. found fossorial vole population from Piedmont. The aim was to assess 68 Cytb sequences of from GenBank: KM004997- the phylogenetic position and the genetic and karyotypic divergence of KM005047 (Kryštufek et al., 2015), HQ728467-78 (Schlegel et al., Italian voles with respect to the other European lineages. Moreover, we 2012), JX457750-51 (Barbosa et al., 2013), AY332708-9 (Pfunder et analyzed the morphology of the Italian fossorial population to deepen al., 2004), GU954310 (Fink et al., 2010). Three sequences belong- Arvicola sapidus Myodes rutilus the phenetic diversity of ecotypes taking into account their genetic re- ing to (FJ539342), (KJ789562) and Chionomys nivalis lationships. (AY513848) were also downloaded and used as the outgroup. The alignment of 1081bp includes 90 sequences (with 19 Cytb se- Methods quences new to Italy). The aligned sequences were used to build max- Specimens and morphometry imum likelihood (ML) and Bayesian phylogenetic trees under the as- sumption of a HKY model of sequence evolution considering gamma Eighteen voles were trapped in five populations along the Italian Pen- rate of substitutions and the proportion of invariable sites. This model insula (Fig. 1, Tab. 1), namely four aquatic (localities 2-5) and one was chosen among 54 evolutionary models using the software Mod- fossorial population
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