Conservation Genetics

, Volume 14, Issue 1, pp 55–63

Genetic characterization of populations of the golden jackal and the red fox in Israel

  • Tali Magory Cohen
  • Roni King
  • Amit Dolev
  • Amitzur Boldo
  • Anat Lichter-Peled
  • Gila Kahila Bar-Gal
Research Article
  • 622 Downloads

Abstract

The golden jackal and red fox are among the wildlife species protected by Israeli law as enforced by the Israel Nature and Parks Authority. In 1964, as a part of a management program to control rabies in Israel, a poison eradication campaign was launched to exterminate golden jackals, considered to be the main reservoir of the disease. The program resulted in the near-complete extermination of jackals in Israel, while foxes were only mildly affected. Jackals have since regained their original numbers and have recolonized southern Israel. We here examined the population structure of the golden jackal and red fox in Israel, 48 years after the poison eradication campaign. DNA from 88 golden jackals and 89 red foxes representing five different geographic regions was extracted and amplified at 13 microsatellite loci in order to characterize the populations on a genetic level. High genetic diversity was found among the jackal and fox populations. A possible migration route through the Jordan Rift Valley was suggested for both species by the genetic similarity of populations in northern and southern Israel. However, in both species, the animals from the center of Israel were distinctive from those north or south, indicating the relative isolation of central populations, likely due to fragmentation or a high abundance of food resources. Genetic profiles obtained for the golden jackal and the red fox in Israel may aid in their conservation management and in the study of zoonotic diseases.

Keywords

Golden jackal Red fox Population genetics Microsatellites 

Supplementary material

10592_2012_423_MOESM1_ESM.doc (406 kb)
Supplementary material 1 (DOC 406 kb)

References

  1. Bardeleben C, Moore RL, Wayne RK (2005) A molecular phylogeny of the Canidae based on six nuclear loci. Mol Phylogenet Evol 37:815–831PubMedCrossRefGoogle Scholar
  2. Berthier K, Charbonnel N, Galan M, Chaval Y, Cosson JF (2006) Migration and recovery of the genetic diversity during the increasing density phase in cyclic vole populations. Mol Ecol 15:2665–2676PubMedCrossRefGoogle Scholar
  3. Bino G, Dolev A, Yosha D, Guter A, King R, Saltz D, Kark S (2010) Abrupt spatial and numerical responses of overabundant foxes to a reduction in anthropogenic resources. J Appl Ecol 47:1262–1271CrossRefGoogle Scholar
  4. Boom R, Sol C, Salimans M, Jansen C, Van Wertheim Dillen P, Van der Noordaa J (1990) Rapid and simple method for purification of nucleic acids. J Clin Microbiol 28:495PubMedGoogle Scholar
  5. Central Bureau of Statistics (2010) Towns in Israel 2010. http://www1.cbs.gov.il/ishuvim/ishuvim_main.htm
  6. Chakraborty R, Nei M (1977) Bottleneck effects on average heterozygosity and genetic distance with the stepwise mutation model. Evolution 31:347–356CrossRefGoogle Scholar
  7. Chatterji S, Pachter L (2006) Reference based annotation with GeneMapper. Genome Biol 7:R29PubMedCrossRefGoogle Scholar
  8. Chevolot M, Ellis J, Rijnsdorp A, Stam W, Olsen J (2008) Temporal changes in allele frequencies but stable genetic diversity over the past 40 years in the Irish Sea population of thornback ray, Raja clavata. Heredity 101:120–126PubMedCrossRefGoogle Scholar
  9. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol–chloroform extraction. Anal Biochem 162:156–159PubMedCrossRefGoogle Scholar
  10. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  11. David D, Dveres N, Yakobson B, Davidson I (2009) Emergence of dog rabies in the northern region of Israel. Epidemiol Infect 137:544–548PubMedCrossRefGoogle Scholar
  12. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. PNAS 91:3166–3170PubMedCrossRefGoogle Scholar
  13. Dolev A (2006) Modelling the spatial dynamics of rabies in canid vectors using a realistic landscape: a tool for optimizing the spatial scattering of oral rabies vaccination. Ben-Gurion University of the Negev, Beer Sheba Google Scholar
  14. Dolev A, Perevolotsky A (2004) Vertebrates in Israel: the red book. Gefen, JerusalemGoogle Scholar
  15. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  16. Ellengren H, Hartman G, Johansson M, Andersson L (1993) Major histocompatibility complex monomorphism and low levers of DNA fingerprinting variability in a reintroduced and rapidly expanding population of beavers. Proc Nat Acad Sic USA 90:8150–8153CrossRefGoogle Scholar
  17. Ellstrand NC, Elam (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242CrossRefGoogle Scholar
  18. England PR, Osler GHR, Woodworth LM, Montgomery ME, Briscoe DA, Frankham R (2003) Effects of intense versus diffuse population bottlenecks on microsatellite genetic diversity and evolutionary potential. Conserv Genet 4:595–604CrossRefGoogle Scholar
  19. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  20. Excoffier L, Laval G, Schneider S (2005) Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol Bioinform 1:47Google Scholar
  21. Frankham R (1995) Conserv Genet. Annu Rev Genet 29:305–327CrossRefGoogle Scholar
  22. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  23. Frankham R, Ralls K (1998) Conservation biology: inbreeding leads to extinction. Nature 392:441–442CrossRefGoogle Scholar
  24. Frankham R, Briscoe DA, Ballou JD (2002) Introduction to Conservation Genetics. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. Gabbay S (1997) Conservation of biological diversity in Israel. Isr Environ Bull 20:2–10Google Scholar
  26. Gutman R, Sinai Y, Sadot E, Shkedi Y (2002) The effect of traffic on Israeli roads on animal mortality, and evaluation of the efficiency of existing animal passages. Nature and Parks Authority. [In Hebrew]Google Scholar
  27. Hoelzel AR, Halley J, O’Brien SJ, Campagna C, Arnborm T, Le Boeuf B, Ralls K, Dover GA (1993) J Hered 84:443–449PubMedGoogle Scholar
  28. Hoss M, Paabo S (1993) DNA extraction from Pleistocene bones by a silica-based purification method. Nucleic Acids Res 21:3913PubMedCrossRefGoogle Scholar
  29. Jhala Y, Moehlman P (2004) Golden jackal (Canis aureus). Canids: foxes, wolves, jackals and dogs. Status survey and conservation action plan. IUCN/SSC Canid Specialist Group, Gland, Switzerland, and Cambridge, UKGoogle Scholar
  30. Lacy RC (1997) Importance of genetic variation to the viability of mammalian populations. J Mammal 78:320–335CrossRefGoogle Scholar
  31. Lanszki J, Heltai M (2002) Feeding habits of golden jackal and red fox in south-western Hungary during winter and spring. Mamm Biol-Z Saugetierkd 67:129–136Google Scholar
  32. Leberg PL (1992) Effects of population bottlenecks on genetic diversity as measured by allozyme electrophoresis. Evolution 46:477–494CrossRefGoogle Scholar
  33. Luikart G (1997) Usefulness of molecular markers for detecting population bottlenecks and monitoring genetic change. University of Montana, MissoulaGoogle Scholar
  34. Luikart G, Cornuet JM (1997) Empirical evaluation of a test for identifying recently bottlenecked populations from allele frequency data. Conserv Biol 12:228–237Google Scholar
  35. Macdonald D, Reynolds J (2004) Red fox Vulpes vulpes Linnaeus, 1758, least concern (2004). Canids: foxes, wolves, jackals and dogs: status survey and conservation action plan. Gland (Switzerland): International Union for conservation of Nature Specialist Group: 129–36Google Scholar
  36. Macdonald D, Voigt D (1985) The biological basis of rabies models. Population dynamics of rabies in wildlife. Academic, LondonGoogle Scholar
  37. Mendelssohn H (1972) Ecological effects of chemical control of rodents and jackals in Israel. In: Favar TM, Milton JP (eds) The careless technology: ecology and International development. Natural History, New York, pp 527–544Google Scholar
  38. Mendelssohn H, Yom-Tov Y (1999) Mammalia of Israel. Israel Academy of Science and Humanities, JerusalemGoogle Scholar
  39. Moran S, Keidar H (1993) Checklist of vertebrate damage to agriculture in Israel. Crop Prot 12:173–182CrossRefGoogle Scholar
  40. Nei M (1977) F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet 41:225–233PubMedCrossRefGoogle Scholar
  41. Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10CrossRefGoogle Scholar
  42. Nemtzov SC (2002) Management of wildlife–human conflicts in Israel: a wide variety of vertebrate pest problems in a difficult and compact environment. In: Timm RM, Schmidt RH (eds) Proceedings of the 20th vertebrate pest conference. University of California, Davis, pp 348–353Google Scholar
  43. Nemtzov S, King R (1998) Wildlife and rabies in Israel. Unpublished report of the Israel Nature and Parks Authority. [In Hebrew]Google Scholar
  44. Nemtzov S, King R (2002) Management of wild canids (fox, jackal and wolf) in Israel, with respect to their damage to agriculture and to the spread of rabies. Advances in vertebrate pest management II. Filander, FurthGoogle Scholar
  45. Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  46. Piry S, Luikart G, Cornuet JM (1999) Bottleneck: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503CrossRefGoogle Scholar
  47. Primmer CR, Saino N, Møller AP, Ellegren H (1998) Unravelling the processes of microsatellite evolution through analysis of germ line mutations in barn swallows Hirundo rustica. Mol Biol Evol 15:1047–1058CrossRefGoogle Scholar
  48. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  49. Roca A, Georgiadis N, O’Brien SJ (2005) Cytonuclear genomic dissociation in African elephant species. Nature 37:96–100Google Scholar
  50. Shalmon B (1999) La-Teva Nolad report 1999-on the status of wild animals in Israel. The Society for the Protection of Nature in Israel, Tel-AvivGoogle Scholar
  51. Shmida A, Polak G (2008) The red plant book: endangered plants of Israel. Israel Nature and Parks Authority, JerusalemGoogle Scholar
  52. Sillero-Zubiri C, Hoffman M, Macdonald DW (2004) Canids: Foxes, Wolves, Jackals and Dogs— 2004 Status Survey and Conservation Action Plan. IUCN/SSC Canid Specialist Group ISBN 2831707862Google Scholar
  53. Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  54. Wayne RK, Geffen E, Girman DJ, Koepfli KP, Lau LM, Marchall CR (1997) Molecular systematics of the Canidae. Syst Biol 46:622–653PubMedCrossRefGoogle Scholar
  55. White PCL, Harris S, Smith GC (1995) Fox contact behaviour and rabies spread: a model for the estimation of contact probabilities between urban foxes at different population densities and its implications for rabies control in Britain. J Appl Ecol 32:693–706CrossRefGoogle Scholar
  56. Wictum E, Kun T, Lindquist C, Malvick J, Vankan D, Sacks B (2012) Developmental validation of DogFiler, a novel multiplex for canine DNA profiling in forensic casework. Forensic Sci Int Gen (in press)Google Scholar
  57. Yakobson B, Manalo D, Bader K, Perl S, Haber A, Shahimov B, Shechat N, Orgad U (1998) An epidemiological retrospective study of Rabies diagnosis and control in Israel, 1948–1997. Isr J Vet Med 53:114–127Google Scholar
  58. Yom-Tov Y, Mendelssohn H (1988) Changes in the distribution and abundance of vertebrates in Israel during the 20th century. Monogr Biol 62:515–547Google Scholar
  59. Zachos FE, Cirovic D, Kirschning J, Otto M, Hartl GB, Petersen B, Honnen AC (2009) Genetic variability, differentiation, and Founder effect in golden jackals (Canis aureus) from Serbia as revealed by mitochondrial DNA and nuclear microsatellite loci. Biochem Genet 47:241–250PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  • Tali Magory Cohen
    • 1
  • Roni King
    • 2
  • Amit Dolev
    • 3
  • Amitzur Boldo
    • 2
  • Anat Lichter-Peled
    • 1
  • Gila Kahila Bar-Gal
    • 1
  1. 1.The Koret School of Veterinary Medicine, The Robert H. Smith Faculty of Agriculture, Food and EnvironmentThe Hebrew University of JerusalemRehovotIsrael
  2. 2.Nature and Parks AuthorityJerusalemIsrael
  3. 3.Israel Mammal Research CentreThe Society for the Protection of Nature in IsraelTel-AvivIsrael

Personalised recommendations