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(Gyps Bengalensis, G. Africanus, G. Indicus and G. Fulvus) Based on Microsatellite Analysis

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(Gyps Bengalensis, G. Africanus, G. Indicus and G. Fulvus) Based on Microsatellite Analysis J. Raptor Res. 43(3):227–236 E 2009 The Raptor Research Foundation, Inc. GENETIC VARIATION OF FOUR GYPS SPECIES (GYPS BENGALENSIS, G. AFRICANUS, G. INDICUS AND G. FULVUS) BASED ON MICROSATELLITE ANALYSIS MUHAMMAD ARSHAD,1 INKEN PEDALL,JAVIER GONZALEZ, AND MICHAEL WINK Heidelberg University, Institute of Pharmacy and Molecular Biotechnology, INF 364, 69120 Heidelberg, Germany OHAD HATZOFE Science and Conservation, Israel Nature and Parks Authority, 3 Am Veolamo Street, Jerusalem 95463, Israel ALEEM AHMED KHAN Institute of Pure and Applied Biology (Zoology Division) University Multan, 60800 Pakistan TIM OSBORNE Tandala Ridge, P.O. Box 22 Okaukuejo, via Outjo, Namibia ABSTRACT.—Although several phylogenetic studies of Gyps species have been conducted, few studies have addressed the genetic diversity of these species on a finer scale such as microsatellite analyses. We collected samples of migratory adults and nestlings from four species of vultures in six different localities. We analyzed the samples using microsatellites in order to determine the genetic distance as well as the amount of variation within and among Gyps species populations. Low genetic diversity in Long-billed Vultures (G. indicus) was probably indicative of a single population with no immigration and low gene flow. As this species is critically endangered, future conservation programs should consider genetically suitable stock for a breeding and reintroduction program. High genetic diversity in African White-backed Vultures (G. africanus) was likely indicative of a number of populations, with immigration and gene flow. We confirmed previous findings of low genetic differentiation among Griffon Vulture (G. fulvus) populations, which indicated high mobility and gene flow among these populations. KEY WORDS: Gyps; genetic variation; microsatellite analysis; vultures. VARIACIO´ N GENE´ TICA CON BASE EN ANA´ LISIS DE MICROSATE´ LITES EN CUATRO ESPECIES DEL GE´ NERO GYPS (G. BENGALENSIS, G. AFRICANUS, G. INDICUS Y G. FULVUS) RESUMEN.—Aunque se han realizado varios estudios filogene´ticos en especies del ge´nero Gyps,so´lo unos pocos han abordado la estructura gene´tica de esas especies a una escala ma´s fina con un ana´lisis de microsate´lites. En el presente estudio fueron colectadas muestras de adultos migratorios y de polluelos de cuatro especies de buitres en seis localidades diferentes. Utilizamos un ana´lisis de microsate´lites para determinar la divergencia y variacio´n gene´tica dentro y entre poblaciones del ge´nero Gyps. La baja diversi- dad gene´tica en G. indicus se debe probablemente a la existencia de una sola poblacio´n sin inmigracio´n y bajo flujo ge´nico. Dado que esta especie se encuentra ‘‘En Peligro Crı´tico’’, los programas de conservacio´n futuros deberı´an considerar un stock gene´tico apropiado para programas de reintroduccio´n y crı´a. La alta diversidad gene´tica detectada en G. africanus se debe probablemente a una alta inmigracio´n y flujo ge´nico entre las numerosas poblaciones cercanas. Confirmamos los hallazgos previos con relacio´n a la baja va- riabilidad gene´tica en G. fulvus, lo que indico´ una alta movilidad y flujo ge´nico entre sus poblaciones. [Traduccio´n del equipo editorial] The vulture genus Gyps is widely distributed across Africa, Asia, and Europe and includes eight species: African White-backed Vulture (Gyps africa- 1 Email address: [email protected] nus), Oriental White-backed Vulture (G. bengalen- 227 228 ARSHAD ET AL.VOL. 43, NO.3 sis), Cape Vulture (G. coprotheres), Griffon Vulture (G. processes should be considered among the criteria fulvus), Himalayan Vulture (G. himalayensis), Long- for protecting habitats and species (Moritz 1999, billed Vulture (G. indicus), Rueppell’s Vulture (G. 2002). rueppellii), and Slender-billed Vulture (G. tenuirostris). Microsatellites are short tandem repeats (STR) Gyps species are efficient scavengers of the soft tissues that are probably the markers most frequently used of large mammals, usually ungulates (Houston 1983, to study population genetics. A number of recent Mundy et al. 1992). They tend to be colonial nesters studies used microsatellite markers in raptor species and communal feeders alongside conspecifics and and they have proved to be useful tools in the con- other vulture species. Gyps vultures reproduce slowly, servation and management of wild and captive pop- reaching maturity after 4–6 yr, and produce one egg ulations (Rudnick et al. 2005, Wink 2007, Banhos et during a breeding season (Mendelssohn and Leshem al. 2008). The evolution of simple repeats is far 1983, del Hoyo et al. 1994). In the phylogeographic from simple. One important implication is that context, almost no geographic partition was observed the mutational rate for microsatellite DNA is not within three Gyps species, G. bengalensis, G. indicus, uniform; the rate differs among loci and perhaps and G. fulvus, with respect to the analysed mtDNA also among species (Ellegren 2004). Consequently, sequences (Arshad et al. 2009a). the use of microsatellite data to address interspecific In the 1980s, G. bengalensis was regarded as ‘‘pos- relationships should be done only with caution. sibly the most abundant large bird of prey in the Although a number of phylogenetic studies of Gyps world’’ (Houston 1985). On the Indian subconti- species have been conducted based on nucleotide nent, populations of three Gyps species (G. bengalen- sequences of marker genes (Seibold and Helbig sis, G. indicus and G. tenuirostris) have dramatically 1995, Wink 1995, Lerner and Mindell 2005, Johnson declined within the past 10 yr and have recently et al. 2006), only a few studies have addressed Gyps’ been listed as critically endangered by the World genetic structure on a finer scale, by using methods Conservation Union (IUCN 2007). Because G. ben- of high resolution such as microsatellite analyses. In galensis and G. indicus are currently very rare or ex- the present study, we analysed samples using micro- tinct in many parts of their historic range (IUCN satellite DNA analysis, to determine the genetic dis- 2007), their biology is of considerable conservation tance as well as diversity within and among Gyps spe- interest. Griffon Vultures were widespread around cies populations from different locations. the Mediterranean Sea, but underwent a severe pop- ulation decline at the end of the nineteenth century METHODS and beginning of the twentieth century, mainly due Sample Collection. To determine the genetic to direct and indirect human persecution (Gouar et structure among four species of the genus Gyps a al. 2007). In France, they went extinct in the Alps at total of 186 samples were studied from six native the end of nineteenth century and in the Massif colonies in Pakistan (Toawala and Nagar Parkar), Central in 1945. However, successful reintroduc- Namibia (Ethosa National Park), Spain, Israel and tions have occurred since the 1980s. In contrast to Cyprus. These colonies are scattered throughout other Old World vulture species, G. africanus appar- the geographical ranges of the species (Fig. 1). ently receives little attention from researchers, and For three species (G. bengalensis, G. indicus and G. there seems to be limited conservation concern re- africanus), we collected 3–5 drops of blood from garding this species (van Wyk et al. 2001). nestlings ca. 6 wk old using brachial puncture (Ta- Conservation should not only be directed toward ble 1). In three populations of G. fulvus, we collect- endangered species but should also encompass the ed blood and muscle samples from marked adults management of existing biodiversity. To ensure the and nestlings (Table 1). long-term persistence of a species, a conservation DNA Extraction. Blood was stored in EDTA buff- strategy should therefore include the assessment er (Arctander 1988) or in 70% ethanol. Total DNA and the preservation of the amount and pattern of was isolated from blood or muscle using standard genetic variation within current populations (May phenol-chloroform protocols (Sambrook and Rus- and Henry 1995, Helbig 1996); ecological data sell 2001). may also be relevant for defining population distinc- Microsatellite and Genotyping System. Several tiveness as evolutionarily significant units (Crandall known microsatellite primers were tested for their et al. 2000). Moreover, the maintenance and resto- degree of polymorphism. The following eight mi- ration of both ecological and microevolutionary crosatellite loci were selected to analyse the genetic SEPTEMBER 2009 GENETIC VARIATION OF GYPS SPECIES 229 Figure 1. Approximate location of sample sites (filled circles) across the range of Gyps species The shaded area is the distribution range of the species (after del Hoyo et al. 1994, Ferguson-Lees and Christie 2001 and Rasmussen and Anderton 2005). distance and diversity of a total of 186 individuals dCTP, dTTP, and dATP), 2.5 ml103 buffer with from six populations of the genus Gyps: Gf3F3, 15 mM MgCl2, 0.15 ml Taq-Polymerase (0.6 Units; Gf3H3, Gf11A4 (Mira et al. 2002), BV5, BV12, Bioron, Ludwigshafen, Germany), 0.1 ml 33P a–dATP BV13, BV14, and BV20 (Gautschi et al. 2000). (1 mCi). Thermal cycling was performed under the The PCR was performed with 60 ng of total DNA following conditions: 2 min at 94uC, followed by 35 in 25 ml of reaction volume containing 10 pmol of cycles of 30 sec at 94uC, 1 min at 50–58uC, 1 min at each primer, 1 ml nucleotide-mix (100 mM of dGTP, 72uC, with a final extension at 72uC for 10 min and then lowered to 4uC for further storage. PCR products
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