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(Apodemus Mystacinus) in the Eastern Mediterranean Area Based on Mitochondrial and Nuclear Genes

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(Apodemus Mystacinus) in the Eastern Mediterranean Area Based on Mitochondrial and Nuclear Genes Blackwell Science, LtdOxford, UKBIJBiological Journal of the Linnean Society0024-4066The Linnean Society of London, 2005*** 2005 85•• M.5363 JOHAN ETOriginal AL Article . BIOGEOGRAPHY OF THE BROAD-TOOTHED FIELD MOUSE Biological Journal of the Linnean Society, 2005, 85, 53–63. With 3 figures Taxonomy, evolutionary history and biogeography of the broad-toothed field mouse (Apodemus mystacinus) in the eastern Mediterranean area based on mitochondrial and nuclear genes JOHAN MICHAUX1,2*, ERICA BELLINVIA3 and PETROS LYMBERAKIS4 1Unité de Recherches Zoogéographiques, Institut de Zoologie, Quai Van Beneden 22, 4020 Liège, Belgium 2Centre de Biologie et de Gestion des Populations (CBGP) UMR 1062, Campus International de Baillarguet, CS 30016, 34988, Montferrier/Lez (Montpellier) Cedex, France 3Department of Zoology, Charles University, Vinièna 7, Praha 2, CZ 128 44, Czech Republic 4Natural History Museum of Crete, University of Crete, Knosou Avenue, Irakleio, Greece Received 16 January 2004; accepted for publication 1 August 2004 The broad-toothed field mouse (Apodemus mystacinus) is distributed throughout the Balkan Peninsula, Asia Minor and the Middle East. It is generally split into two different specific entities: Apodemus epimelas occurs on the Balkan Peninsula and A. mystacinus inhabits Asia Minor and the Middle East. This analysis, based on two mitochondrial regions (cytochrome b and the D-loop) and the interstitial retinol binding protein (IRBP) nuclear gene, confirms an important level of genetic divergence between the animals from these regions and their separation from each other at least 4.2–5.1 Mya, which is in favour of a distinct specific status. Finally, the broad-toothed field mice from south- western Turkey appear to be closely related to the animals from Crete but highly distinct from the populations of the other Oriental regions. This supports a distinct subspecific level (A. m. rhodius) for the insular animals and also for those from south-western Turkey. From a biogeographical point of view, it can be assumed that either late Pliocene or early Pleistocene cooling led to the isolation of two main groups of A. mystacinus, one in the Balkan region and the other one in Turkey and the Near East (Syria and Israel). In this region, it is suggested that a more recent event appeared during the Quaternary period, isolating broad-toothed field mice in Crete and leading to the appearance of two well-differentiated genetic groups: one in Crete and south-western Turkey, and the other widespread in north- ern and eastern Turkey as well as in the Near East. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 53–63. ADDITIONAL KEYWORDS: eastern Mediterranean region – IRBP nuclear gene – mitochondrial control region – mitochondrial cytochrome b gene. INTRODUCTION size and a dark-grey coloration of the fur. Its range extends from the Balkan region (Albania, the former The broad-toothed field mouse, Apodemus mystacinus Yugoslavia, Bulgaria and Greece) (Mitchell-Jones (Danford & Alston, 1877), is a small rodent of the et al., 1999) to the Near East (Turkey, Georgia, Jor- Murinae subfamily distributed throughout the east- dan, Lebanon, Israel and Iraq) (Kock, Malec & Storch, ern Mediterranean region. It lives in rocky and stony 1972). It is also present in Corfu, Rhodes, Karphatos habitats in various environments such as cultivated and Crete, as well as in several Aegean islands areas, woodlands or ruins. It is clearly distinguishable (Niethammer, 1978). from the other European Apodemus species by differ- The taxonomic status of this species is still unclear. ent morphological characters such as a greater body Two subspecies were firstly described within A. mystacinus: A. m. epimelas (Nehring, 1902) occur- *Corresponding author. E-mail: [email protected] ring on the Balkan peninsula (Terra typica: Parnas © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 53–63 53 54 M. JOHAN ET AL. Mountains, Greece) and A. m. mystacinus (Danford & Alston, 1877) inhabiting Asia Minor and the Middle east (Terra typica: Bolkar Daglari Mountains, Asia Minor). This classification is supported by Spitzen- Bu berger (1973) on the basis of morphological studies. 1-2 GEO Tur2 Tur3 Another subspecies has also been described in the Tur4 Gr2 islands of Crete, Karpathos and Rhodes, namely Gr1 Tur1 Cr 1-5 Sy2 A. m. rhodius (Ondrias, 1966). Sy1 On the basis of palaeontological data, however, Sy3 Storch (1977) considers that A. epimelas and A. mystacinus are two distinct species, an opinion also Figure 1. Geographic distribution of the Apodemus myst- shared by Mezhzherin (1997), in his systematic revi- acinus samples. The shaded zones correspond to the distri- sion of the Apodemus species of northern Eurasia. bution area of this species (as described by Mitchell-Jones To date only a single genetic study based on allozyme et al., 1999 and Kock et al., 1972). White circles, black data (Filippucci, Macholán & Michaux, 2002) has been circles and triangles correspond to clades A, B1 and B2, performed on this species and tends to confirm a respectively. See Table 1 for sample symbols. specific status for A. epimelas and A. mystacinus. Nevertheless, a new molecular study based on DNA sequences and carried out on different specimens from MATERIAL AND METHODS European and oriental regions would be extremely useful to highlight the taxonomic debate. BIOLOGICAL MATERIAL From a biogeographical point of view, the existence A total of 21 Apodemus mystacinus from 15 localities of these various taxa raises many interesting widespread throughout a large part of the species dis- questions: tribution area were analysed (Table 1, Fig. 1). One Apodemus agrarius and one Apodemus peninsulae 1. How old are the morphologic differences between were also analysed to sequence their D-loop region. the European and oriental populations? Are they resulting from an ancient allopatric isolation asso- ciated to a previous geological phenomenon or cli- LABORATORY METHODS mate change (e.g. the Quaternary ice ages)? DNA was extracted from ethanol-preserved tissue fol- 2. As the Marmara Sea was frequently replaced by lowing Sambrook, Fritsch & Maniatis (1989) or Bahl dry lands during the Quaternary ice ages, why is & Pfenninger (1996). Tissues were taken from the the European form absent from Turkey and Apodemus tissue collection of J. R. Michaux (JRM vice-versa? numbers) and those of E. Bellinvia (EB numbers). 3. As suggested by the description of several subspe- A large portion of the cytochrome b gene (972 bp) cies within the oriental group (Spitzenberger, was amplified using the universal PCR primers L7 1973), is it possible to distinguish different genetic (5¢-ACCAATGACATGAAAAATCATCGTT-3¢) and H16 lineages in this region. How and when did they (5¢-ACATGAATYGGAGGYCAACCWG-3¢) (Kocher eventually appear? et al., 1989). Moreover, 782 bp of the IRBP gene were 4. What is the origin of the A. mystacinus populations amplified using the PCR primers I1 and J2 (Stanhope in Crete? As Apodemus sylvaticus (J. Michaux, et al., 1992). Finally, the whole D-loop and flanking unpubl. data), did it invade this island from Greece, tRNA genes (about 1000 bp) were amplified in two or did it come from oriental regions, similar to overlapping segments of about 600 bp each. Primers another rodent, Acomys minous (Barome et al., 1 (5¢-ATAAACATTACTCTGGTCTTGTAAAC-3¢) and 2001)? 2 bi (5¢-CACAGTTATGGAAGTCTTGG-3¢) were used 5. When did it invade the oriental Mediterranean to obtain a PCR product including the whole tRNAThr islands? Is it, like A. sylvaticus (J. Michaux, and tRNAPro genes and about 460 bp of the D-loop up unpubl. data) and Acomys minous (Barome et al., to about half of the central domain. The second 2001), a recent colonist associated with anthropo- segment, extending from about one half of the D-loop genic introductions? central domain to the beginning of the 12S tRNA The aims of this study are to address these ques- region, including the tRNAPhe gene, was produced tions and to better determine the taxonomic status of with primers 3 (5¢-CGTTCCCCTAAATAAGACA-3¢) A. mystacinus. Several well-distributed populations and 4 (5¢-TAATTATAAGGCCAGGACCA-3¢). are analysed using sequences of the nuclear IRBP Amplification reactions were carried out in gene and two mitochondrial regions, the cytochrome b 2 ¥ 50 mL volumes including 25 mL of each 2 mM gene and the D-loop region. primer, 20 mL of 1 mM dNTP, 10 mL of 10¥ reaction © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 85, 53–63 © 2005TheLinneanSocietyof London, Table 1. Geographic distribution and references of Apodemus and other rodent tissues used for the experiments Sample Accession numbers symbols Geographic origin Tissue (see Fig. 1) (IRBP gene) (cytochrome b gene) (D-loop) Apodemus mystacinus Greece, Peloponissos, Taygetos JRM-480 Gr 1 AJ48222 AJ48228 AY623070 Biological JournaloftheLinnean Society, Greece, Peloponissos, Delphes JRM-281, JRM-282 Gr 2 AJ48222, AJ48224 AJ48229, AJ48230 AY623069, AY623064 Crete EB-1816 Cr 1 AJ48211 AJ48232 AY623071 Crete, Anogia JRM-458 Cr 2 AJ48213 AJ48235 AY623073 BIOGEOGRAPHY OFTHEBROAD-TOOTHEDFIELDMOUSE Crete, Mamas JRM-464 Cr 3 AJ48214 AJ48234 AY623072 Crete, Nida plateau JRM-477, JRM-478 Cr 4 AJ48212, AJ48215 AJ48231, AJ48233 AY623074, AY623075 Bulgaria, Ploski, Blagoevogard JRM-535 Bu 1 AJ48223 AJ48227 AY623063 Bulgaria, Breznica EB-177 Bu 2 – – AY623068 Syria, Bloudan JRM-542 Sy 1 AJ48220 AJ48236 AY623065 Syria, Bloudan JRM-543 Sy 1 – – AY623078 Syria, Slinfeh JRM-544 Sy 2 AJ48219 AJ48237 AY623080 Syria, Quanawat JRM-261 Sy 3 AJ48216 AJ48238 AY623077 Syria, Quanawat JRM-536 Sy 3 – – AY623081 Georgia JRM-545 Geo AJ48218 AJ48240 AY623083 Turkey, Antalya EB-1169, EB 1170 Tur 1 AJ48210, AJ48209 AJ48226, AJ48225 AY623076, AY623067 Turkey, Safran Bolou EB-178 Tur 2 AJ48208 – AY623079 2005, Turkey, Damar JRM-262 Tur 3 AJ48217 AJ48239 AY623066 Turkey, Damar EB-98 Tur 4 – – AY623082 85 Apodemus agrarius , 53–63 GenBank/CZ- Krásná Lipa Suzuki et al., 2003 Suzuki et al., 2003 AY588250 Apodemus peninsulae GenBank/Bajkal, Russia Suzuki et al., 2003 Suzuki et al., 2003 AY588251 Mus musculus GenBank Suzuki et al., 2000 Bibb et al.
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