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Molecular Relationships of the Israeli Shrews (Eulipotyphla: Soricidae

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Molecular Relationships of the Israeli Shrews (Eulipotyphla: Soricidae Mammalia 2021; 85(1): 79–89 Original study Erez Shpirer, Michal Haddas-Sasson, Maya Spivak-Glater, Tamar Feldstein, Shai Meiri* and Dorothée Huchon* Molecular relationships of the Israeli shrews (Eulipotyphla: Soricidae) based on cytochrome b sequences https://doi.org/10.1515/mammalia-2019-0143 1 Introduction Received November 28, 2019; accepted June 12, 2020; published online August 17, 2020 Shrews (family: Soricidae) are among the most diverse and abundant mammals (Burgin et al. 2018b; Wilson and Abstract: The number of shrew species in Israel has been Reeder 2005). Among them, the Old-World genus Croci- and still is the subject of debate. In this work we used for dura, contains 198 species, more than any other mamma- the first time a molecular marker, the cytochrome b gene, to lian genus (Burgin et al. 2018a). However, being mainly investigate the number and identity of shrew species in small, nocturnal, and rather unremarkable-looking, their Israel. Our molecular results confirmed the presence of four species: Crocidura leucodon, Crocidura suaveolens guel- diversity tends to have escaped the notice of the general denstaedtii, Crocidura ramona, and Suncus etruscus. The public, environmental decision-makers, conservation C. ramona sequences were found to differ from all other agencies, and even scientists. The number of shrew species Crocidura species sequenced to date, supporting its status thought to exist in Israel is under debate (Table 1). Tristram fi as a distinct species. Whether it is conspecific with Croci- (1884) recognized ve species in the Levant and assigned dura portali (described in 1920 from Israel and usually them to the genus Sorex: Sorex araneus, Sorex tetragonurus synonymized with C. suaveolens), will require additional (currently known as S. araneus), Sorex pygmaeus (currently study. The sequences of Israeli C. suaveolens were found to known as Suncus etruscus), Sorex crassicaudus (currently be very similar to those of Iran, Turkey, and Georgia known as Suncus murinus), and Sorex fodiens (currently (i.e., C. suaveolens gueldenstaedtii), in agreement with known as Neomys fodiens). N. fodiens is a water-shrew and, previous studies. The Israeli C. leucodon sequences, how- together with S. araneus and S. murinus, it has not been ’ ever, formed a distinct clade among C. leucodon. Finally, reported again in Israel since Tristram s original work the S. etruscus sequences clustered with sequences from (Bodenheimer 1935). Thomas (1919, 1920) assigned two France, Italy, and Iran. Israeli species to the genus Crocidura: Crocidura russula judaica (Thomas 1919) and a new species that he described: Keywords: barcoding; Crocidura; cyt b; levant; suncus. Crocidura portali (Thomas 1920). Bodenheimer (1935) con- tended that three species of Crocidura occur in Israel: C. russula, Crocidura judaica, and C. portali. Later, he Shai Meiri and Dorothée Huchon: These authors contributed equally to this work. considered C. portali as a subspecies of Crocidura suaveo- lens (Bodenheimer 1958); however, no explanation was *Corresponding authors: Shai Meiri and Dorothée Huchon, School of given for this decision. Regarding Suncus, Bodenheimer Zoology, Tel Aviv University, Ramat Aviv, 69978, Tel Aviv, Israel; and (1935) indicated that the presence of S. crassicaudus is a The Steinhardt Museum of Natural History and National Research consequence of misidentification and Bodenheimer (1958) Center, Tel-Aviv University, Tel Aviv, Israel, e-mail: [email protected] (Shai Meiri); reassigned the shrew described by Tristram (1884) as [email protected] (Dorothée Huchon). https://orcid.org/ S. pygmaeus, to S. etruscus. Harrison (1963), later con- 0000-0003-3839-6330 (S. Meiri). https://orcid.org/0000-0002- tended that Thomas’s C. russula judaica (1919) is in fact a 5047-244X (D. Huchon) local synonym of Crocidura leucodon, based on morpho- Erez Shpirer, Michal Haddas-Sasson and Maya Spivak-Glater: School logical traits. He further identified C. russula and C. sua- of Zoology, Tel Aviv University, Ramat Aviv, 69978, Tel Aviv, Israel as inhabiting Israel. Tamar Feldstein: School of Zoology, Tel Aviv University, Ramat Aviv, veolens portali 69978, Tel Aviv, Israel; The Steinhardt Museum of Natural History and Molecular studies of shrews started in the 1980s. Based National Research Center, Tel-Aviv University, Tel Aviv, Israel on karyotype and allozyme comparisons, Catzeflis et al. Open Access. © 2020 Erez Shpirer et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0 International License. 80 E. Shpirer et al.: Molecular relationships of Israeli shrews Table : Number and identities of Israeli shrew species. Source Shrew species inhabiting Israel Tristram () Sorex araneus, S. tetragonurusa, S. pygmaeusb, S. crassicaudusc, S. fodiensd Thomas (, )h C. russula judaica, C. portali e Bodenheimer (; ) Sorex araneus, Sorex minutus (=pygmaeus), Neomys fodiens, C. russula, C. r. judaica, C. portali e, S. tristrami f Bodenheimer () C. russula, C. judaica, C. suaveolens portali, S. etruscus Harrison ()i C. russula, C. leucodon judaica, C. suaveolens portali Mendelssohn and Yom-Tov () C. russula, C. leucodon, C. suaveolens, S. etruscus Mendelssohn and Yom-Tov (); C. leucodon judaica, C. suaveolens monacha, S. etruscus etruscus Harrison and Bates () Dolev and Perevolotsky (); C. ramona, C. leucodon, C. suaveolens, S. etruscus Meiri et al. (), this work Wilson and Reeder () C. gmelini g, C. katinka, C. ramona, C. leucodon, C. suaveolens, S. etruscus IUCN red list () C. katinka, C. ramona, C. leucodon, C. suaveolens, S. etruscus, perhaps C. gmelini Burgin et al. (b) C. ramona, C. leucodon judaica, C. gueldenstaedtii gueldenstaedtii, S. etruscus etruscus aSorex tetragonurus has been synonymized with Sorex araneus (Wilson and Reeder ). bSorex pygmaeus has been synonymized with Suncus etruscus (Wilson and Reeder ). cSorex crassicaudus has been synonymized with Suncus murinus (Wilson and Reeder ). Its presence in Israel was considered to be the result of a misidentification by Bodenheimer () and later sources. dSorex fodiens has been synonymized with Neomys fodiens (Wilson and Reeder ). eCrocidura portali has been synonymized either with C. suaveolens (Bodenheimer ) or under C. gmelinig (Wilson and Reeder ), or kept at the species rank (Kryštufek and Vohralík ). fSuncus tristrami has been synonymized with C. suaveolens (Wilson and Reeder ). gCrocidura gmelini has been synonymized with C. suaveolens (Bannikova et al. ; Burgin et al. b; Saeedzadeh et al. ). hDescription of specific specimens. iHarrison () focused on the genus Crocidura. (1985) demonstrated that the individuals called C. russula in which presents different morphological characteristics and theMiddleEastwereinfactmembersofC. suaveolens,and karyotype to those of C. leucodon and C. suaveolens. further placed the subspecies gueldenstaedtii and monacha It is thus currently considered that there are at least four within suaveolens. Harrison and Bates (1991) treated C. sua- shrew species in Israel: C. leucodon, C. suaveolens/C. guel- veolens specimens from Israel as C. suaveolens monacha. denstaedtii, C. ramona,andS. etruscus (Dolev and Per- They also noted that a smaller form is present in southern evolotsky 2004; Meiri et al. 2019; while there is debate Israel, Sinai, and Arabia, and that, consequently, a second regarding two additional species, C. portali and Crocidura subspecies may be present “If this proves to be the case the katinka Table 1, Gerrie and Kennerley 2017; Wilson and name portali is available”. Relationships among members of Reeder 2005). C. katinka was originally described in 1937 the suaveolens species complex have been found to be from a Pleistocene skull discovered in the Tabun Cave near intricate and obscured by introgression events (Bannikova Mount Carmel (Bate 1937). The species was thought to be et al. 2006; Castiglia et al. 2017; Dubey et al. 2006, 2007a; extinct until the recent discovery of skulls similar to Bate’s Ohdachi et al. 2004). C. suaveolens specimens from the C. katinka in owl pellets from Syria (Hutterer and Kock 2002). Caucasus, the Balkans, and the Levant have been either While there has not been recent evidence of C. katinka’s treated as a distinct species within the suaveolens group, presence in Israel, it is often listed as a member of the Israeli Crocidura gueldenstaedtii (Bannikova et al. 2006; Burgin fauna (Gerrie and Kennerley 2017; Wilson and Reeder 2005). et al. 2018b), or as a subspecies: C. suaveolens gueldenstaedtii Similarly, the exact status of C. portali Thomas 1920 remains (Burgin et al. 2018a; Dubey et al. 2008; Palomo et al. 2016). Of unresolved. It has been treated variously as a distinct species note, the subspecies assignment of Israeli specimens is (Kryštufek and Vohralík 2001) or suggested as a senior syn- further complicated by the use of the subspecies monacha onym of C. ramona (Burgin et al. 2018b; Kryštufek and (Harrison and Bates 1991; Mendelssohn and Yom-Tov 1999). Vohralík 2001), synonymized with C. suaveolens (Bod- In the absence of a formal revision of the C. suaveolens group, enheimer 1958) or with Crocidura gmelini (Hoffmann 1996; we refer throughout the text to such specimens as C. sua- Wilson and Reeder 2005).C.gmeliniis found in arid envi- veolens gueldenstaedtii. Ivanitskaya et al. (1996) described a ronments from Iran to Kazakhstan (Hutterer 2017) and new species of Israeli endemic shrew: Crocidura ramona, has sometimes been synonymized with C. suaveolens E. Shpirer et al.: Molecular
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