Origin and Evolution of Western European Moles (Genus Talpa, Insectivora): a Multidisciplinary Approach

Mammal Study 30: S13–S17 (2005) © the Mammalogical Society of Japan

Origin and evolution of Western European moles (genus Talpa, Insectivora): a multidisciplinary approach

Anna Loy1,*, Paolo Colangelo2, Flavia Annesi2 and Ernesto Capanna2 1 Dipartimento STAT, Università del Molise, Via Mazzini 18, Isernia, I-86170, Italy 2 Dipartimento B.A.U., Università di Roma ‘La Sapienza’, Via Borelli 50, I-00161, Rome, Italy

Abstract. The European representatives of the subfamily Talpinae belong to the monophyletic genus Talpa. Five out of the nine species of Talpa occur in Western Europe. A wide central area is occupied by Talpa europaea, while the small sized Talpa caeca occurs in southern Europe. Three endemic species are restricted to the peripheral areas of the genus range and show a parapatric distribution with respect to T. europaea, i.e. the Iberian T. occidentalis, the southern Italian T. romana and the Balkan T. stankovici. The karyotypes of moles are very conservative, with the majority of the species showing 2n = 34. Allozyme data first allowed to assess the specific status of endemic taxa and the low levels of heterozygosity. Nei’s genetic distances suggest that T. occidentalis, T. romana and T. stankovici early diverged from an europaea–caeca line. Preliminary results from mtDNA analyses strongly support the monophyly of Western European moles, but are still not able to solve the relationships within this clade. Estimates of time of divergences indicate a basal split of an Eastern and a Western lineage during the Miocene-Pliocene transition, while the divergence among the Western European moles should have occurred in association to the Pliocene-Pleistocene climatic oscillations.

Key words: evolution, phylogeny, Talpa, Western Europe.

The systematic framework Talpa europaea inhabits a wide central area extending east to Russia as far as the Ob and Irtish rivers. Three The family Talpidae comprises about forty species in species characterize the three European peninsular blind three subfamilies, Talpinae, Desmaninae and Uropsilinae. alleys, the Iberian T. occidentalis, the southern Italian T. The subfamily Talpinae includes the strictly subterra- romana and the Balkan T. stankovici. These three spe- nean species, belonging to the genera Talpa, Scalopus, cies show a parapatric distribution with respect to T. Mogera, Scapanus, Scaptochirus, Parascalops and europaea. Finally, a small mole, T. caeca, was described Euroscaptor. All Old World moles belong to the mono- in southern mountainous areas of the Western Alps, phyletic genus Talpa (Mouchaty et al. 2000; Douady and Apennines and Tracia Mountains (Mitchell-Jones et al. Douzery 2003; Shinohara et al. 2003; Motokawa 2004). 1999). The most recent revision of the genus Talpa by Hutterer (1993) recognized nine species: four from the Cytogenetic and genetic variation Near East to Siberia and Altai, i.e. T. altaica Nikolasky 1883, T. levantis Thomas 1906, T. caucasica Satunin The karyotypes of western European species are very 1908 and T. streeti Lay 1965, and five from western conservative, showing an identical 2n = 34. Only T. Europe, T. europaea Linnaeus 1758, T. caeca Savi 1882, caeca has 2n = 36, due to one supplementary pair of T. romana Thomas 1902, T. occidentalis Cabrera 1907 small chromosomes (Meylan 1966; Todorovic and and T. stankovici Martino & Martino 1931. The distri- Soldatovic 1969). Slight morphological differences are bution of the western European moles is characteristic. observed in a pair of subtelocentrics (Meylan 1966;

*To whom correspondence should be addressed. E-mail: [email protected] S14 Mammal Study 30 (2005)

Gropp et al. 1966; Kratochvil and Kràl 1972; Todorovic Pennsylvania) suggested a closer relationship between et al. 1972; Capanna 1981; Zima 1983; Jimenéz et al. T. romana and T. stankovici, and between M. latouchei, 1984), but the differences were not characterized by G T. europaea, T. caeca and T. occidentalis (Rohlf et al. or C band patterns. Only Zima (1983) and Jimenéz 1996). et al. (1984) provided the G and C band patterns of T. Geometric morphometrics also revealed specific dif- europaea and T. occidentalis, respectively, but there ferences in the shape of the skull of the mole species. was no apparent diversity between the two species. Specifically, the skull of the European mole T. europaea Nevertheless, Capanna (1981) was able to use the chro- was smaller and slender than that of T. stankovici and T. mosome morphology to predict an evolutionary scenario romana (Corti and Loy 1987; Loy et al. 1993; Rohlf et in which three lineages, T. romana, T. stankovici and T. al. 1996; Loy and Capanna 1998). Evidences of charac- caeca (plus T. caeca hergegovinensis), originated from ter displacement related to competitive interactions were an ancestral Talpa europaea stock. revealed in syntopic populations of T. europaea and T. Filippucci et al. (1987) examined the allozyme varia- romana in Italy. Competitive interactions were related tion of the five European taxa and confirmed the species to the way food is acquired and processed rather then to status of the three southern peninsular taxa, i.e. T. occi- a shift in the food niche (Loy and Capanna 1998; dentalis, T. romana and T. stankovici, which had been Beolchini and Loy 2004). considered synonyms of europaea or caeca (Ellerman Ecological and morphological data collected on the and Morrison-Scott 1951; Stein 1960). The allozyme Roman mole in the last twenty years suggested this spe- data allowed a first hypothesis about the pattern and cies might be favoured in the Mediterranean climate times of divergence of the western European moles. areas, being more able to survive the hot, dry summer Three taxa, T. occidentalis, T. romana and T. stankovici which severely limits food availability and digging appear to have diverged early from the europaea and activities (Loy 1992; Loy et al. 1994a, b). caeca lineages. Estimates of evolutionary time indicated that the five species diverged roughly 1–3 mya. The Fossil evidences and phylogenetic relationships authors also found that T. caeca shared the highest num- ber of alleles with all the other European mole species The oldest fossils assigned to the family Talpidae are (average 73%) and had the lowest values of genetic dis- from late Eocene sediments of Europe (McKenna and tance from each of them (D = 0.22–0.31). Therefore, Bell 1997). It has been suggested that the family origi- they suggested that T. caeca remained genetically more nated in Europe and spread by means of multiple dis- similar to the hypothetical ancestor of the group than the persal events to Asia and North America (Hutchison other species (Filippucci et al. 1987). 1974; Moore 1986; Whidden 2000). Explosive mole The extensive study of the parapatric contact between radiation occurred in the Miocene in Eurasia and North T. romana and T. europaea in Central Italy confirmed America (Yates and Moore 1990). The Miocene talpid the absence of gene flow between the two species (Loy fauna of Europe includes representatives of almost all et al. 2001). The study also revealed the existence of subfamilies (Hutchison 1968, 1974; Skoczeń 1980; introgressed alleles in both species. This introgression Storch and Qiu 1983). Ziegler (2003) described up to suggested that hybridization and backcrossing occurred fourteen species and six genera in the fauna of the when the two species first came into contact after a long Petersbuch fissure filling in southern Germany, and period of isolation. Dahlmann (2001) reported up to eleven species from one site at Wolfereheim, Germany, dated 12.5–13 mya. Morphometric variation and adaptation Therefore compared to the Neogene fossil record, the extant Talpid fauna is extremely impoverished, repre- Morphometric relationships among the five European sented only by the desmans and the monophyletic genus taxa have been investigated using both traditional and Talpa. The high Miocene diversification might have geometric approaches to skull morphology (Corti and been favoured by the peak of warm and humid climatic Loy 1987; Loy et al. 1993; Loy and Corti 1996; Rohlf et optimum in Central Europe at 18–16.5 mya (Böhme al. 1996). Phenograms derived from landmark analyses 2003). The Miocene warm period ended abruptly on the five European species and two outgroups (Mogera between 14.8 and 13.5 mya with a drop of the mean latouchei from China and Parascalops breweri from annual temperature of probably more than 7°C to Loy et al., Evolution of Western European moles S15 temperatures around 14.8–15.7°C (Böhme 2003). This in the Italian Apennine and Alpine belts during ice climatic transition was related to a massive extinction retreat, and might actually represent cold relic mole. crisis of thermophilic vertebrates in Europe, which Most recent effects of glacial expansion and retreats occurred between 14.0 and 13.5 mya (Böhme 2003). can also be envisaged in the step cline variation revealed This climatic change could have also forced most of in T. europaea by Corti and Loy (1987). Step clines talpids to migrate eastward, with the only exception of were detected across the Alps and the Apennines, and desmans and Talpa spp. have been interpreted as the result of secondary contacts The preliminary results from the analyses of cyto- after postglacial expansions from western, southern and chrome b sequences of T. romana, T. caeca, T. europaea, eastern refugia following the last Pleistocene glaciation and T. occidentalis supported a basal split between T. (Corti and Loy 1987). altaica and the other western European species, which Despite more data are needed to assess the relation- form a strongly supported monophyletic assemblage ships and the pattern and time of divergence among the (Colangelo et al. in prep.). A preliminary estimates of western European moles, it is worth noting that T. divergence between the Western and the Eastern clade minor–T. caeca fossil remains are found together with dates this event at about 6 mya, at the Miocene-Pliocene the fossil T. romana and T. fossilis–T. europaea during transition, and more specifically at MN13 (6.8–5 mya, the middle Pleistocene in northern Italy (Bartolomei et Agustì et al. 2001). Other western and eastern European al. 1976; Bartolomei and Tozzi 1978; Cattani et al. 1991; mammalian taxa are known to have diverged at about the Fanfani 2000; Kotsakis et al. 2003). This evidence both same time, such as Erinaceus europaeus and E. concolor indicate that 0.7–0.5 mya three Talpa species were (Santucci et al. 1998), or the eastern and western clade of already established in Europe and that, similarly to T. Cervus elaphus (Ludt et al. 2004). europaea, also the Italian range of T. romana shrank and Molecular and allozyme analyses suggest that the expanded following the Pleistocene climatic oscillations divergence among the western European lineage (Kotsakis et al. 2003). occurred at the end of the Pliocene to the beginning of the Pleistocene. During the Plio-pleistocene, most part Acknowledgments: Our gratitute goes to Tassos Kotsakis of Europe was covered with ice and permafrost, with and to Pasquale Raia for their unvaluable advices on extensive unsuitable habitats for moles, such as the European mole fossil records and for their critical tundra belts, covering most of Central and Eastern revision of the manuscript. The research was supported Europe (Hewitt 2000). by the Ministry of University and Research (M.I.U.R.– The present distributions of T. romana and T. stankovici Project of relevant interest no. 2003057545). suggest speciation events related to isolation in warm refugia during one of the oldest cold phases in the Italian, References the Iberian and the Balkan peninsulas. Agustì, J., Cabrera, L., Garcés, M., Krijgsman, W., Oms, O. and Parés, A different scenario is invoked for the blind mole T. J. M. 2001. A calibrated mammal scale for the Neogene of West- caeca. This taxon is endemic to southern Europe, were it ern Europe. State of the art. Earth-Science Review 52: 247–260. currently survives with scattered and fragmented popu- Bartolomei, G., Peretto, C. and Sala, B. 1976. Depositi a loess con lations found in cold and rocky soils in the Western Ochotona e rinoceronte nel Carso di Trieste. Rendiconti dell’Accademia Nazionale dei Lincei 61: 280–284. Alps, the Apennines, the Balkans, and in the Romanian Bartolomei, G. and Tozzi, C. 1978. Nuovi dati stratigrafi ci sui Carpathians (Krystufek 1999). In Italy, T. caeca is the depositi del Pleistocene medio a Ochotona del Riparo di species most adapted to cold habitats. In fact, it is cur- Visogliano nel Carso di Trieste. Rendiconti dell’Accademia Nazionale dei Lincei 64: 490–497. rently found at the highest altitudes among all European Beolchini, F. and Loy, A. 2004. Diet of syntopic moles T. romana and mole species, occurring in the Alps and Apennines above T. europaea in central Italy. Mammalian Biology (Zeitschrift fur the tree line, up to 2500 m asl, where it replaces both Saugetierkunde) 69: 1–5. T. europaea and T. romana (Toschi 1959). The auto- Böhme, M. 2003. The Miocene Climatic Optimum: evidence from ectothermic vertebrates of Central Europe. Palaeogeography, ecology and distribution of T. caeca suggest that it’s Palaeoclimatology and Palaeoecology 195: 389–401. origin is related to the expanding alpine prairies during Capanna, E. 1981. Caryotype et morphologie crânienne de Talpa one of the latest Pleistocene ice phase. In fact, Jullien romana Thomas de terra typica. Mammalia 45: 71–82. Cattani, L., Cremaschi, M., Ferraris, M. R., Mallegni, F., Masini, F., (1972) refers to a ‘small’ mole in Würm II deposits, Scola, V. and Tozzi, C. 1991. Le gisement du Pléistocène moyen coinciding with a cold climate. This taxon likely refuged de Visogliano (Trieste): restes humains, industries, environne- S16 Mammal Study 30 (2005)

ment. L’Antropologie 95: 9–36. Talpa romana, a fossorial insectivore from south central Italy. Corti, M. and Loy, A. 1987. Morphometric divergence in southern Journal of Mammalogy 64: 365–370. European moles (Insectivora, Talpidae). Bollettino di Zoologia Loy, A., Beolchini, F., Martullo, S. and Capanna, E. 1994b. Territo- 54: 187–191. rial behaviour of Talpa romana (Mammalia, Insectivora, Talpi- Dahlmann, T. 2001. Die Kleinsäuger der unter-pliozänen Fundstelle dae) in an olive grove environment in Central Italy. Bollettino di Wölfers-heim in der Wetterau (Mammalia: Lipotyphla, Chirop- Zoologia 61: 207–211. tera, Rodentia). Courier Forschungsinstitut Senckenberg 227: 1– Loy, A. and Corti, M. 1996. Distribution of Talpa europaea 129. (Mammalia, Insectivora, Talpidae) in European biogeographic Douady, C. J. and Douzery, E. J. P. 2003. Molecular estimation of hypothesis based on morphometric data. Italian Journal of Zool- Eulipotyphla divergence times and the evolution of “Insectivora”. ogy 63: 277–284. Molecular Phylogenetics and Evolution 28: 285–296. Loy, A. and Capanna, E. 1998. A parapatric contact area between two Ellerman, J. R. and Morrison-Scott, T. C. S. 1951. Checklist of Palae- species of moles (genus Talpa): character displacement investi- arctic and Indian Mammals. British Museum of Natural History, gated through the geometric morphometric of skull. Acta Zoo- London, 810 pp. logica Academiae Scientiarum Hungaricae 44: 151–164. Fanfani, F. 2000. Revisione degli insettivori (Mammalia) tardo neo- Loy, A., Capula, M., Palombi, A. and Capanna, E. 2001. Genetic and genici e quaternari dell’Italia peninsulare. PhD Thesis, Università morphometric evidence of past introgression between Talpa di Bologna-Firenze-Modena-Roma ‘La Sapienza’, 282 pp. europaea and Talpa romana along a parapatric contact zone. Filippucci, M. G., Nascetti, G., Capanna, E. and Bullini, L. 1987. Journal of Zoology, London 254: 229–238. Allozyme variation and systematics of european moles of the Ludt, C. J., Schroeder, W., Rottmann, O. and Kuehn, R. 2004. Mito- genus Talpa (Mammalia, Insectivora). Journal of Mammalogy chondrial DNA phylogeography of red deer (Cervus elaphus). 68: 487–499. Molecular Phylogenetics and Evolution 31: 1064–1083. Gropp, A., Geisler, M. and Cytoler, P. 1966. The chromosomes of the McKenna, M. and Bell, S. K. 1997. Classification of Mammals above hedgehog (Erinaceus europaeus) and the mole (Talpa europaea). the Species Level. Columbia University Press, New York, 631 Mammalian Chromosomes Newsletter 22: 181–182. pp. Hewitt, G. M. 2000. The genetic legacy of the Quaternary ice ages. Meylan, A. 1966. Données nouvelles sur les chromosomes des insec- Nature 405: 907–913. tivores européens (Mamm.). Revue Suisse de Zoologie 73: 548– Hutchison, J. H. 1968. Fossil Talpidae (Insectivora, Mammalia) from 558. the Late Tertiary of Oregon. Bulletin of the Museum of Natural Mitchell-Jones, A. J., Amori, G., Bogdanowicz, W., Krystufek, B., History University of Oregon 11: 1–117. Reijinders, P. J. H., Spitzenberger, F., Stubbe, M., Thissen, J. B. Hutchison, J. H. 1974. Notes on the type species of European M., Vorhalik, V. and Zima, J. (eds.) 1999. The Atlas of European Miocene Talpidae and tentative classification of Old World Mammals. Academic Press, London, 484 pp. Tertiary Talpidae. Geobios 7: 211–256. Moore, D. W. 1986. Systematic and Biogeographic Relationships Hutterer, R. 1993. Order Insectivora. In (D. E. Wilson and D. M. among the Talpinae (Insectivora: Talpidae). Ph.D. dissertation, Reeder, eds.) Mammal Species of the World: A Taxonomic and University of New Mexico, Albuquerque, 255 pp. Geographic Reference. 2nd ed. Pp. 69–130. Smithsonian Institu- Motokawa, M. 2004. Phylogenetic relationships within the family tion, Washington. Talpidae (Mammalia: Insectivora). Journal of Zoolology, Lon- Jimenéz, R., Burgos, M. and Diaz de la Guardia, R. 1984. Karyotype don 263: 147–157. and chromosome banding in the mole (Talpa occidentalis) from Mouchaty, S. K., Gullberg, A., Janke, A. and Arnason, U. 2000. The the South-East of the Iberian peninsula. Implications on its taxo- phylogenetic position of the Talpidae within eutheria based on nomic position. Caryologia 37: 253–258. analysis of complete mitochondrial sequences. Molecular Biol- Jullien, R. 1972. Les insectivores du Wurmien II de la grotte de ogy and Evolution 17: 60–67. l’Hortus (Valflaunès, Hérault). Etudes Quaternaires Mémoire 1: Rohlf, F. J., Loy, A. and Corti, M. 1996. Morphometric analysis of 243–244. Old World Talpidae (Mammalia, Insectivora) using partial warp Kotsakis, T., Abbazzi, L., Angelone, C., Argenti, P., Barisone, G., scores. Systematic Biology 45: 344–362. Fanfani, F., Marcolini, F. and Masini, F. 2003. Plio-Pleistocene Santucci, F., Emerson, B. C. and Hewitt, G. M. 1998. Mitochondrial biogeography of Italian mainland micromammals. DEINSEA DNA phylogeography of European hedgehogs. Molecular Ecol- Annual of the Natural History Museum Rotterdam 10: 313–342. ology 7: 1163–1172. Kratochvil, J. and Kràl, B. 1972. Karyotypes of phylogenetic relation- Shinohara, A., Campbell, K. L. and Hitoshi, S. 2003. Molecular hips of certain species of the genus Talpa (Talpidae, Insectivora). phylogenetic relationships of moles, shrew moles, and desmans Zoological Listy 21: 199–208. from the new and old worlds. Molecular Phylogenetics and Evo- Krystufek, B. 1999. Talpa caeca. In (A. J. Mitchell-Jones, G. Amori, lution 27: 247–258. W. Bogdanowicz, B. Kristufek, P. J. H. Reijinders, F. Spitzen- Skoczeń, S. 1980. Scaptonychini Van Valen, 1967, Urotrichini and berger, M. Stubbe, J. B. M. Thissen, V. Vorhalik and J. Zima, Scalopini Dobson, 1883 (Insectivora, Mammalia) in the Pliocene eds.) The Atlas of European Mammals. Pp. 80–81. Academic and Pleistocene of Poland. Acta Zoologica Cracoviensia 24: Press, London. 411–448. Loy, A. 1992. Biologia evolutiva delle talpe europee. PhD disserta- Stein, G. H. W. 1960. Schädelallometrien und Systematik bei tion thesis, Università di Roma ‘La Sapienza’ 148 pp. altweltlichen Maulwürfen (Talpinae). Mitteilungen aus dem Loy, A., Corti, M. and Marcus, L. F. 1993. Landmark data: size and Zoologischen Museum in Berlin 36: 1–49. shape analysis in systematics. A case study on Old World Talpi- Storch, G. and Qiu, Z. 1983. The Neogene mammalian faunas of dae (Mammalia, Insectivora). In (L. F. Marcus, E. Bello and A. Ertemte and Harr Obo in Inner Mongolia (Nei Mongol), China. 2. Valdecasas, eds.) Contribution to Morphometrics. Monographias Moles-Insectivora: Talpidae. Senckenbergiana Lethaea 64: 89– 8. Pp. 215–240. Museo Nacional de Ciencias Naturales, Madrid. 127. Loy, A., Duprè, E. and Capanna, E. 1994a. Territorial behaviour in Todorovic, M. and Soldatovic, B. 1969. The karyotype of the sub- Loy et al., Evolution of Western European moles S17

species Talpa mizura hercegovinensis. Arhiv Bioloskih Nauka Yates, T. L. and Moore, D. W. 1990. Speciation and evolution in the 21: 5–6. family Talpidae (Mammalia: Insectivora). In (E. R. Nevo and O. Todorovic, M., Soldatovic, B. and Dunderski, Z. 1972. Characteris- A. Reig, eds.) Evolution of Subterranean Mammals at the Organ- tics of the karyotype of the populations of the genus Talpa from ismal and Molecular Levels. Pp. 1–22. Alan R. Liss, New York. Macedonia and Montenegro. Arhiv Bioloskih Nauka 24: 131– Ziegler, R. 2003. Moles (Talpidae) from the Middle Miocene in South 139. Germany. Acta Palaeontologica Polonica 48: 617–648. Toschi, A. 1959. Mammalia — Generalità, Insectivora, Chiroptera. Zima, J. 1983. The karyotype of the Talpa europaea kratochvili Fauna d’Italia, Volume IV. Edizioni Calderini, Bologna, 485 pp. (Talpidae, Insectivora). Folia Zoologica 32: 131–136. Whidden, H. P. 2000. Comparative myology of moles and the phylog- eny of the Talpidae (Mammalia, Lipotyphla). American Museum Received 29 November 2005. Accepted 27 January 2006. Novitates 294: 1–53.