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Population Structure, Diversity, and Phylogeography in the Near bij_1099 Biological Journal of the Linnean Society, 2008, ••, ••–••. With 3 figures 1 Population structure, diversity, and phylogeography in 2 the near-threatened Eurasian black vultures Aegypius 3 monachus (Falconiformes; Accipitridae) in Europe: 4 insights from microsatellite and mitochondrial 5 DNA variation 22 6 1,2 3 1 1 4 7 N. POULAKAKIS *†, A. ANTONIOU †, G. MANTZIOU , A. PARMAKELIS , T. SKARTSI , 33 8 D. VASILAKIS4, J. ELORRIAGA4, J. DE LA PUENTE5, A. GAVASHELISHVILI6, 9 M. GHASABYAN7, T. KATZNER8, M. MCGRADY8,N.BATBAYAR9, M. FULLER10 and 10 T. NATSAGDORJ9 11 1 12 Natural History Museum of Crete, University of Crete, Heraklion, Greece 44 13 2Yale Institute for Biospheric Studies, Yale University, Newhaven, CT, USA 14 3Department of Genetics and Molecular Biotechnology, Hellenic Centre for Marine Research, 15 Heraklion, Crete, Greece 16 4WWF Greece-Dadia Project, Daia, Soufli, Greece 17 5Área de Estudio y Seguimiento de Aves, SEO/BirdLife Melquiades Biencinto, Madrid, Spain 18 6Georgian Center for the Conservation of Wildlife, Tbilisi, The Republic of Georgia 19 7Armenian Society for the Protection of Birds, Yerevan, Armenia 20 8Natural Research, Ltd, Krems, Austria 21 9The Peregrine Fund, World Center for Birds of Prey, Boise, ID, USA 22 10USGS, Forest and Rangeland Ecosystem Science Center, Snake River Field Station, and Boise 23 State University, Boise, ID, USA 24 25 Received 18 February 2008; accepted for publication 21 April 2008 26 27 The Eurasian black vulture (Aegypius monachus) has experienced a severe decline during the last two centuries 28 and is globally classified as near-threatened. This has led to the extinction of many traditional breeding areas in 29 Europe and resulted in the present patchy distribution (Iberian and Balkan peninsulas) in the Western Palearctic. 30 In the present study, we describe the current genetic status of the European populations using both mitochondrial 31 cytochrome b sequences and nuclear microsatellite markers, comparing with those found in Asia (Mongolia and 32 Caucasus region). Although, mitochondrial (mt)DNA revealed a relatively low genetic variability (haplotype 33 diversity), no evidence of genome-wide genetic erosion exists because nuclear diversity exhibits normal levels and 34 strong differentiation. A highly philopatric dispersal behaviour must be invoked to explain the existence of a clear 35 pattern that revealed by the phylogeographic analysis, which indicates a sharp East–West clinal distribution and 36 an allopatric differentiation. The distribution of mtDNA haplotypes one in the Iberian population and two in 37 Balkan population and the significance divergence at nuclear loci fulfill the definitions of those populations as 38 evolutionary significant units. We discuss how management strategies should aim at the maintenance (or increase) 39 of current genetic variability levels, suggesting that independent conservation plans are urgently required to 40 protect these two breeding European populations from extinction. © 2008 The Linnean Society of London, 41 Biological Journal of the Linnean Society, 2008, ••, ••–••. 42 ADDITIONAL KEYWORDS: conservation genetics – nuclear DNA. 55 43 44 45 *Corresponding author. E-mail: 46 [email protected] 47 †These authors contributed equally to this work. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, ••, ••–•• 1 bij_1099 2 N. POULAKAKIS ET AL. 1 Figure 1. A map of Eurasia showing the location of the sampling areas, the number of samples from each locality, and 2 the present distribution of the species Aegypius monachus. 3 4 INTRODUCTION ing in the present patchy distribution of breeding 39 5 nuclei in Europe (Fig. 1). Extant European popula- 40 6 The Eurasian black vulture (Aegypius monachus)is tions are confined to Spain, the Balkans (Rhodope 41 7 the largest bird of prey (Falconiformes) in the world Mountain), and the Caucasus mountains (Russia, 42 8 (i.e. the unrelated, slightly larger Andean Condor Georgia, Armenia, and Azerbaijan). It is worth noting 43 9 is now affiliated with the Ciconiiformes). By being that there is no evidence (field observations) of 44 10 mainly a scavenger or carrion eater bird with a long contact between Balkan and Iberian populations sub- 45 11 life-span and an extended home-range, vast areas of sequent to the extinction of the intermediate popula- 46 12 suitable habitats are considered indispensable for the tion(s) in 19th Century. Much less information is 47 13 species’ well being (Cramp & Simmons, 1980; Carrete available regarding the status and population trends 48 14 & Donazar, 2005). Its global range extends from of the species in Asia, where the bulk of the global 49 15 the Iberian Peninsula across southern Europe and population resides. It appears that breeding popula- 50 16 through the central Asian plateau to Mongolia and tions are more or less stable in Mongolia (where the 51 17 China. species is described as common) and Pakistan (where 52 18 Listed in Appendix I of the CITES (Convention on it is described as scarce), although fluctuations in 53 19 International Trade of Endangered Species of Wild distribution and breeding success occur. In Kazakh- 54 20 Fauna and Flora) and considered near-threatened stan, however, populations of all vulture species are 55 21 by the IUCN (2006 IUCN Red List of Threatened in severe decline. This trend may be mirrored in 56 22 Species) the Eurasian black vulture has attracted a number of other central Asian countries where 57 23 some conservation attention. It is classified as vulner- populations of both domesticated livestock and wild 58 24 able at European level (BirdLife International, 2006) ungulates have declined greatly in recent years 59 25 and endangered in Greece (Handrinos, 1992). Despite (BirdLife International, 2006). 60 26 the fact that in some regions (e.g. Spain) its popula- Faced with the growing challenge of deriving strat- 61 27 tions are now recovering (Sánchez, 2004), the species egies for salvaging diminishing flora and fauna, con- 62 28 has suffered a serious demographic decline during the servation biologists and ecologists continue to search 63 29 last century, mainly as a result of human pressure for methods that can distinguish unambiguous units 64 30 (i.e. the degradation and destruction of its breeding for conservation purposes (Fraser & Bernatchez, 65 31 habitats, direct persecution and poisoning, the aban- 2001). An understanding of the genetic diversity and 66 32 doning of extensive livestock economy, and the rar- the spatial structure of populations is important for 67 33 efaction of wild ungulate populations) (Hiraldo, 1974; establishing the appropriate scale and subunits for 68 34 Donazar et al., 2002). Many traditional breeding conservation management and minimizing genetic 69 35 areas were lost and the species is now extinct in erosion (Moritz, 1999). Current genetic patterns in a 70 36 France, Italy, Poland, Slovakia, Austria, Croatia, species are shaped both by historical and contempo- 71 37 Yugoslavia, Romania, Moldova, and Cyprus (Cramp & rary factors that affect its biogeography and its 72 38 Simmons, 1980; Meyburg & Meyburg, 1984), result- demography. The relative contributions of historic 73 © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, ••, ••–•• bij_1099 THE GENETIC STRUCTURE OF EURASIAN BLANK VULTURES 3 1 and contemporary factors in shaping the genetic vultures. Although hair and scat (the most common 57 2 makeup of the species are not easy to unravel, and a non-invasive material) have been used extensively 58 3 combination of several analyses at different temporal for genetic tagging (Taberlet et al., 1997), large-scale 59 4 scales (i.e. haplotype relatedness, demographic his- studies utilizing feathers for individual identification 60 5 tory, and population genetics) might be necessary to remain rare (Rudnick et al., 2005). 61 6 describe the geographical structure and investigate 62 7 the historic or contemporary processes that determine MATERIAL AND METHODS 63 8 its origin (Bernatchez, 2001; Godoy et al., 2004). 9 However, there has been no attempt to describe the SAMPLING AND DNA EXTRACTION, AMPLIFICATION, 64 10 geographical distribution of genetic diversity or the AND SEQUENCING 65 11 evolutionary history of A. monachus. Like many In total, 173 samples of A. monachus were collected 66 12 large-sized raptors, A. monachus is difficult to study from wild-caught individuals captured during field 67 13 because: (1) it is an endangered species with large ecology projects (Fig. 1). DNA from blood or muscle 68 14 home ranges; (2) it keeps small or limited popula- tissue (N = 135) was extracted with DNeasy Tissue 69 15 tions, whereas some of them are not well monitored Kit (Qiagen) following the manufacturer’s instruction. 70 16 and the available information are limited; (3) its nests DNA from dry skins/bones (N = 12) and naturally 71 17 are located in inaccessible places; and (4) males and molted adult feathers (N = 26) was isolated using 72 18 females are indistinguishable visually, and adults are DNA techniques for museum specimens. The feathers 73 19 sometimes difficult to capture and mark. and skins were washed three times in 1 mL of 10 mM 74 20 To date, few genetic studies have been carried out Tris-HCl (pH 8.0) on a rotary mixer for 24 h per wash 75 21 for large-sized vultures, including bearded vultures to re-hydrate (Austin & Melville, 2006), whereas 76 22 (Gypaetus barbatus) (Negro & Torres, 1999; Gautschi 40 mg of powder bones were incubated in 1 mL of 77 23 et al., 2003; Godoy et al., 2004), griffon vultures proteinase K digestion buffer composed of 10 mM Tris 78 24 (Gyps fulvus) (Le Gouar et al., 2006), Egyptian (pH 8.0), 10 mM NaCl, 50 mM ethylenediaminetet- 79 25 vulture (Neophron percnopterus) (Kretzmann et al., raacetic acid (pH 8.0), 0.5% sodium dodecyl sulphate 80 26 2003), Andean condors (Vultur gryphus) (Hendrickson and1mgmL-1 proteinase K for 1 h at 56 °C under 81 27 et al., 2003), and Old World vultures (Lerner & agitation (Rohland & Hofreiter, 2007).
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