Molecular Biogeography of Red Deer Cervus Elaphus from Eastern Europe: Insights from Mitochondrial DNA Sequences
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Acta Theriol (2011) 56:1–12 DOI 10.1007/s13364-010-0002-0 ORIGINAL PAPER Molecular biogeography of red deer Cervus elaphus from eastern Europe: insights from mitochondrial DNA sequences Magdalena Niedziałkowska & BogumiłaJędrzejewska & Ann-Christin Honnen & Thurid Otto & Vadim E. Sidorovich & Kajetan Perzanowski & Anna Skog & Günther B. Hartl & Tomasz Borowik & Aleksei N. Bunevich & Johannes Lang & Frank E. Zachos Received: 30 June 2010 /Accepted: 8 October 2010 /Published online: 16 November 2010 # The Author(s) 2010. This article is published with open access at Springerlink.com Abstract European red deer are known to show a analyses. To close this gap, we produced mtDNA control conspicuous phylogeographic pattern with three distinct region sequences from more than 500 red deer from mtDNA lineages (western, eastern and North-African/ Denmark, Germany, Poland, Lithuania, Belarus, Ukraine Sardinian). The western lineage, believed to be indicative and western Russia and combined our data with sequences of a southwestern glacial refuge in Iberia and southern available from earlier studies to an overall sample size of France, nowadays covers large areas of the continent almost 1,100. Our results show that the western lineage including the British Isles, Scandinavia and parts of central extends far into the European east and is prominent in all Europe, while the eastern lineage is primarily found in eastern countries except for the Polish Carpathians, Ukraine southeast-central Europe, the Carpathians and the Balkans. and Russia where only eastern haplotypes occurred. While However, large parts of central Europe and the whole the latter may actually reflect the natural northward northeast of the continent were not covered by previous expansion of the eastern lineage after the last ice age, the Communicated by: Jan M. Wójcik M. Niedziałkowska : B. Jędrzejewska : T. Borowik : K. Perzanowski F. E. Zachos (*) Catholic University of Lublin, Mammal Research Institute, Polish Academy of Sciences, ul. Konstantynów 1H, ul. Waszkiewicza 1, 20-708 Lublin, Poland 17-230 Białowieża, Poland e-mail: [email protected] A. Skog A.-C. Honnen : T. Otto : G. B. Hartl : F. E. Zachos Centre for Ecological and Evolutionary Synthesis (CEES), Zoological Institute, Christian-Albrechts-University, Department of Biology, University of Oslo, Olshausenstrasse 40, Oslo, Norway 24118 Kiel, Germany A. N. Bunevich V. E. Sidorovich State National Park Belovezhskaya Pushcha, Institute of Zoology, National Academy of Sciences of Belarus, Kamenec Raion, Akademicheskaya str. 27, 225063 Kamenyuki, Republic of Belarus Minsk 220072, Republic of Belarus K. Perzanowski J. Lang Carpathian Wildlife Research Station in Ustrzyki Dolne, Institut für Tierökologie und Naturbildung, ul. Ogrodowa 10, Hauptstraße 30, 38-700 Ustrzyki Dolne, Poland 35321 Laubach, Germany 2 Acta Theriol (2011) 56:1–12 present distribution of the western lineage in eastern Europe species where human translocations and restocking modi- may in large parts be artificial and a result of translocations fied genetic structure, e.g. the brown hare Lepus europaeus and reintroduction of red deer into areas where the species (Andersen et al. 2009) and the wild boar Sus scrofa became extinct in historical times. (Nikolov et al. 2009). Red deer have also been studied in detail with respect to Keywords Red deer . Phylogeography. mtDNA . Eastern their phylogeography, both addressing more specific ques- Europe . Translocations . Human management tions like the origin of the Sardinian/Corsican subspecies (Hmwe et al. 2006a; Hajji et al. 2008) and continent-wide patterns (Ludt et al. 2004; Skog et al. 2009, for an inclusion Introduction of the fossil record see Sommer et al. 2008). Skog et al. (2009), in by far the most comprehensive study to date, The cyclic climatic changes during the Quaternary have had a have found three distinct genetic lineages in European red profound impact on the genetic structure of European deer based on mitochondrial DNA (cytochrome b and the temperate species in that these have been undergoing repeated control region): one confined to Sardinia and the north- range contractions and expansions in the wake of glacial and African Barbary red deer; a western lineage spreading from interglacial pulses (e.g. Hewitt 2000). During glacials, most Iberia through the British Isles to Scandinavia, Germany temperate European species retreated to refuge areas in the and western Poland; and an eastern lineage covering the south of the continent, viz. the Iberian Peninsula and Balkans, the Romanian Carpathians and reaching north to southern France, Italy and the Balkan and Carpathian Austria, Hungary and the Czech Republic. There were only regions, while in the following interglacials with their milder very few exceptions to this geographic pattern, indicating climate these species recolonised their previously abandoned that most of the extensive translocations in red deer—at territories (Hewitt 1996, 2000; Sommer and Nadachowski least as far as females are concerned—were carried out 2006). However, the refugial populations that expanded from within these lineages rather than among them. However, the south carried distinct genetic lineages as a legacy of their large parts of central Europe (particularly where the western long isolation from each other. The identification of these and eastern lineages might meet north of the Czech lineages in present populations throughout Europe and their Republic) and the whole northern parts of eastern Europe geographic distribution (“phylogeography”) allows for the were not covered by the study of Skog et al. (2009). It is reconstruction of glacial refugia and postglacial recolonisa- hence unknown how far to the east the western lineage tion routes. It is important to note that for present phylogeo- extends and how far north the eastern lineage reaches. graphic patterns, it is the last glacial maximum (LGM) In the present study we aim at closing this gap by 25,000–18,000 BP that is decisive because in this time analysing mtDNA control region sequences from more than distribution ranges were more contracted than ever before in 500 red deer from seven countries in central and eastern the history of extant species (Sommer and Zachos 2009). Europe (Denmark, Germany, Poland, Lithuania, Ukraine, Therefore, it is only the refugia during the LGM that served Belarus and Russia). We combine our data set with that of as reservoirs for the recolonisation of central and northern Skog et al. (2009, n=587) and base our conclusions on data Europe in the Late Pleistocene and Holocene (Sommer and from nearly 1,100 animals, making this study one of the Zachos 2009). In Europe, most species have been found to most comprehensive analyses ever of European phylogeog- follow a number of recolonisation patterns, the most raphy. In addition, by means of an extensive literature common of which are the so-called “grasshopper pattern” search focusing on sources from eastern Europe and Russia, (recolonisation from a primarily Balkan refuge), “bear we try to estimate in how far the patterns observed today pattern” (main recolonisation from a western/Iberian refuge) may be attributed to natural colonisation and to which and the “hedgehog pattern” (recolonisation from Iberia, Italy extent translocations might have blurred the natural genetic and the Balkans) (Hewitt 1999). structure in east-European red deer. The European red deer Cervus elaphus has been in the focus of evolutionary and conservation biologists alike in the recent past. As one of the most widespread and most Material and methods important game species it has undergone a variety of human influences such as selective hunting, translocations and Sampling information habitat fragmentation which have locally and regionally resulted in high levels of genetic drift, inbreeding and the Muscle or skin samples from 507 legally culled red deer were blurring of natural patterns of genetic structure (e.g. Hartl et collected in Denmark, Germany, Poland, Belarus, Ukraine, al. 2003; Zachos et al. 2007). Human impact on genetic Lithuania and Russia (see Fig. 1 and Table 1 for details). It diversity is not specific to red deer: there are many other is important in the context of this study to consider Acta Theriol (2011) 56:1–12 3 Fig. 1 Map showing red deer distribution in Europe and sample sites Susz, Zaporowo Forest Districts, Poland; 11 Spała and Poddębice of the present study and Skog et al.’s(2009). Sample sites: 1 Forest Districts, Poland; 12 Brynek, Milicz, Olesno, Prószków, Smolensk Region, Russia; 2 Bransk oblast, Russia; 3 Vitebsk Region, Świerklaniec Forest Districts (Silesia) Poland; 13 Bieszczady Mts., Belarus; 4 Mogilev Region, Belarus; 5 Gomel Region, Belarus; 6 Poland; 14 Tismenickii Raion, Ivano-Frankivskaya oblast, Ukraine; 15 Grodno Region, Belarus and Joniškis and Širvintos Districts, Dolinskii Raion, Ivano-Frankivskaya oblast, Ukraine; 16 Saxony, Lithuania; 7 Augustów, Borki and Rominta Forests, Poland; 8 Biało- Germany; 17 Rostock, Germany; 18 Mecklenburg, Germany; 19 wieża Forest (both Polish and Belarusian parts), Knyszyn and Mielnik Lauenburg, Germany; 20 southern Denmark; 21 Hils region, Forests, Łomża and Sokołów Forest Districts, Poland, Brest Region, Germany; 22 Spessart and Vogelsberg, Germany; 23 Kyllwald and Belarus; 9 Napiwoda and Pisz Forests, Poland; 10 Bytów, Młynary, Gerolstein, Germany human influences on red deer distribution. In the seventeenth to Niedziałkowska 2008). Red deer migrated from Latvia