Biochemical Genetics

, 43:577 | Cite as

Biochemical Genetic Relationships Among Tunisian Hares (Lepus sp.), South African Cape Hares (L. capensis), and European Brown Hares (L. europaeus)

  • Hichem Ben Slimen
  • Franz Suchentrunk
  • Abdelmajid Memmi
  • Amel Ben Ammar Elgaaied


Tunisian hares (n = 45), currently assigned to Lepus capensis, were assayed for allelic variation at 40 allozyme loci, and allele frequencies at 32 loci were directly compared with earlier data of South African cape hares (L. capensis, n = 9) and European brown hares (L. europaeus, n = 244) to reveal genetic relationships among them. European mountain hares (L. timidus, n = 200) were used for outgroup comparison. In the Tunisian hares 27.5% of the loci were polymorphic with 2–4 alleles. Among all alleles at polymorphic loci, 15.1% occurred exclusively in Tunisian hares, 5.7% exclusively in cape hares, and 7.5% exclusively in brown hares at low frequencies. Not a single locus showed alternately fixed alleles between the samples of the L. capensis/L. europaeus complex. Levels of absolute and relative genetic differentiation among the samples of the L. capensis/ L. europaeus complex were low, relative to pairwise comparisons involving mountain hares. Diverse cluster analyses and multidimensional scaling of various pairwise genetic distance matrices concordantly grouped Tunisian hares with brown hares, and South African cape hares clustered only slightly farther apart, whereas mountain hares were distinctly separate. These results suggest regionally distinct phylogenetic units within an overall cohesive gene pool in the L. capensis/ L. europaeus complex, supporting Petter's view that all North African hares belong to L. capensis except for one local population of savanna hares, and that cape hares and brown hares are conspecific.


Tunisian hares allozymes Lepus capensis Lepus europaeus phylogeny 


  1. Alves, P. C., and Ferrand, N. (1999). Genetic variability in Portugese populations of the Iberian hare, Lepus granatensis. Folia Zool. 48 (Suppl. 1):3–10.Google Scholar
  2. Alves, P. C., Branco, M., Matias, O., and Ferrand, N. (2000). New genetic variation in the European hares, Lepus granatensis and L. europaeus. Biochem. Genet. 38:87–96.PubMedCrossRefGoogle Scholar
  3. Alves, P. C., Ferrand, N., and Suchentrunk, F. (2001). Developmental stability and protein heterozygosity in a local population of Iberian hares (Lepus granatensis). Mamm. Biol. 66: 238–250.Google Scholar
  4. Alves, P. C., Ferrand, N., Suchentrunk, F., and Harris, D. J. (2003). Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula. Mol. Phylogent. Evol. 27:70–80.Google Scholar
  5. Angermann, R. (1965). Revision der palaearktischen und äthiopischen Arten der Gattung Lepus (Leporidae, Lagomorpha). Diss. Thesis. Humboldt University of Berlin, pp. 200.Google Scholar
  6. Angermann, R. (1983). The taxononmy of Old World Lepus. Acta Zool. Fennica 174:17–21.Google Scholar
  7. Averianov, A. O., and Baryschnikov, G. F. (1992). Pleistocene hares (genus Lepus, Lagomorpha) of the Great Caucasus. Trudy Zool. Inst. RAN 246:4–28.Google Scholar
  8. Averianov, A., Niethammer, J., and Pegel, M. (2003). Lepus europaeus Pallas, 1778 –Feldhase. In Krapp, F. (ed.), Handbuch der Säugetiere Europas: Hasentiere, Aula-Verlag, Wiebelsheim, Germany, pp. 35–104.Google Scholar
  9. Avise, J. C. (1994). Molecular Markers, Natural History and Evolution, Chapman and Hall, New York, London, pp. 511.Google Scholar
  10. Belkhir, K. (1999). GENETIX, logiciel sous Windows pour la génétique des populations. Laboratoire Génome et Populations, CNRS UPR 9060, Université de Montpellier II, Montpellier (France).Google Scholar
  11. Bonhomme, F., Fernandez, J., Palacios, F., Catalan, J., and Machordon, A. (1986). Charactérisation biochimique du complex d'espèces du genre Lepus en Espagne. Mammalia 50:495–506.CrossRefGoogle Scholar
  12. Eggert, L. S., Rasner, C. A., and Woodruff, D. S. (2002). The evolution and phylogeography of the African elephant inferred from mitochondrial DNA sequence and nuclear microsatellite markers. Proc. R. Soc. Lond. B 269:1993–2006.CrossRefGoogle Scholar
  13. Ellerman, J. R., and Morrison Scott, T. C. S. (1951). Checklist of Palaearctic and Indian Mammals, British Museum of Natural History, London.Google Scholar
  14. Felsenstein, J. (1995). PHYLIP (Phylogeny Inference Package), Version 3.57c. Seattle: University of Washington.Google Scholar
  15. Flux, J. E. C., and Angermann, R. (1990). Hares ab Jackrabbits. In Chapman, J. A., and Flux, J. E. C. (eds.), Hares and Pikas: Status Survey and Conservation Action Plan, IUCN/SSC Lagomorph Specialist Group, Gland, Switzerland, pp. 61–94.Google Scholar
  16. Goudet, J. (1995). Fstat Version 1.2. A computer program to calculate F-statistics. J. Heredity 86:485–486.Google Scholar
  17. Goudet, J. (2001). Fstat, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Available from Updated from Goudet (1995).
  18. Grillitsch, M., Hartl, G. B., Suchentrunk, F., and Willing, R. (1992). Allozyme evolution and the molecular clock in the Lagomorpha. Acta Theriol. 37:1–13.Google Scholar
  19. Halanych, K. M., Demboski, J. R., van Vuuren, J. B., Klein, D. R., and Cook, J. A. (1999). Cytochrome b phylogeny of North American hares and jackrabbits (Lepus, Lagomorpha) and the effects of saturation in outgroup taxa. Mol. Phylogenet. Evol. 11:213–221.PubMedGoogle Scholar
  20. Harris, H., and Hopkinson, D. A. (1976). Handbook of Enzyme Electrophoresis in Human Genetics, North-Holland Publ. Co, Amsterdam.Google Scholar
  21. Hartl, G. B., and Höger, H. (1986). Biochemical variation in purebred and crossbred strains of domestic rabbit Oryctolagus cuniculus L. Genet. Res. (Camb.) 48:27–34.Google Scholar
  22. Hartl, G. B., Markowski, J., Kovacs, G., Grillitsch, M., and Willing, R. (1990). Biochemical variation and differentiation in the brown hare (Lepus europaeus) of Central Europe. Z. Säugetierkunde 55:186–193.Google Scholar
  23. Hartl, G. B., Markowski, J., Swiatecki, A., Janiszewski, T., and Willing, R. (1992). Genetic diversity in the Polish brown hare Lepus europaeus Pallas, 1778: Implications for conservation and management. Acta Theriol. 37:15–25.Google Scholar
  24. Hartl, G. B., Suchentrunk, F., Nadlinger, K., and Willing, R. (1993). An integrative analysis of genetic differentiation in the brown hare Lepus europaeus based on morphology, allozymes, and mitochondrial DNA. Acta Theriol. 38 (suppl. 2):33–57.Google Scholar
  25. Hartl, G. B., Willing, R., and Nadlinger, K. (1994). Allozymes in mammalian population genetics and systematics: Indicative function of a marker system reconsidered. In Schierwater, B., Streit, B., Wagner, G. P., and DeSalle, R. (eds), Molecular Ecology and Evolution: Approaches and Applications, Birkhäuser Verlag, Basel, Switzerland, pp. 299–310.Google Scholar
  26. Kasapidis, P., Suchentrunk, F., Magoulas, A., and Kotoulas, G. (2005). The shaping of mitochondrial DNA phylogeographic patterns of the brown hare (Lepus europaeus) under the combined influence of Late Pleistocene climatic fluctuations and anthropogenic translocations. Mol. Phylogenet. Evol. 34:55–66.PubMedCrossRefGoogle Scholar
  27. Kretzoi, M. (1941). Die unterpleistozäne Säugetierfauna von Betfia bei Nagyvárad. Földt. Közl. 71:308–335.Google Scholar
  28. Kryger, U., Robinson, T. J., and Bloomer, P. (2002). Isolation and characterization of six polymorphic microsatellite loci in South African hares (Lepus saxatilis F. Cuvier, 1823, and Lepus capensis Linnaeus, 1758). Mol. Ecol. Notes 2:422–424.CrossRefGoogle Scholar
  29. Li, W. H. (1997). Molecular Evolution. Sinauer Assoc., Sunderland, Mass., pp. 487.Google Scholar
  30. Lu, X. (2000). Body weights of the cape hare Lepus capensis in northern China. Acta Theriol. 45:271–280.Google Scholar
  31. Mamuris, Z., Sfougaris, A. I., and Stamatis, C. (2001). Genetic structure of Greek brown hares (Lepus europaeus) as revealed by mtDBNA RFLP-PCR analysis: Implications for conserving genetic diversity. Biol. Conserv. 101:187–196.CrossRefGoogle Scholar
  32. Mamuris, Z., Sfougaris, A. I., Stamatis, C., and Suchentrunk, F. (2002). Assessment of genetic structure of Greek brown hare (Lepus europaeus) populations based on variation in random amplified polymorphic DNA (RAPD). Biochem. Genet. 40:323–338.PubMedCrossRefGoogle Scholar
  33. Mils, G., and Hes, L. (1999). Säugetiere des südlichen Afrika: Eine illustrierte Enzyklopädie, Könemann Publisher, Köln, Germany, pp. 356.Google Scholar
  34. Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590.PubMedGoogle Scholar
  35. Petter, F. (1959). Eléments d'une révision des lièvres africains du sous-genre Lepus. Mammalia 23:41–67.Google Scholar
  36. Petter, F. (1961). Eléments d'une révision des lièvres européens et asiatiques du sous-genre Lepus. Z. Säugetierkunde 26:1–11.Google Scholar
  37. Pielowski, Z. (1969). Sex ratio and weight of hares from Poland. Acta Theriol. 14:119–131.Google Scholar
  38. Pierpaoli, M., Riga, F., Trocchi, V., and Randi, E. (1999). Species distinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing. Mol. Ecol. 8:1805–1817.PubMedCrossRefGoogle Scholar
  39. Rekovets, L. I. (1985). Mikrotheriofauna desnyansko-podneprovskogo posdnego paleolita. Naukova Dumka, Kiev, Belarus, pp. 168.Google Scholar
  40. Rice, W. S. (1989). Analyzing tables of statistical tests. Evolution 43:223–225.Google Scholar
  41. Richardson, B. J., Baverstock, P. R., and Adams, M. (1986). Allozyme electrophoresis. A Handbook for animal systematics and populaiton studies. Academic Press, San Diego, pp. 410.Google Scholar
  42. Rothe, G. M. (1994). Electrophoresis of Enzymes: Laboratory Methods, Springer Lab Manual. Springer Verlag, Berlin, pp. 307.Google Scholar
  43. Sert, H., Suchentrunk, F., and Erdogan, A. (2005). Genetic diversity in brown hares (Lepus europaeus Pallas, 1778) from Anatolia and differentiation among Anatolian and European populations. Mamm. Biol. 70:171–186.Google Scholar
  44. Suchentrunk, F., Hartl, G. B., Flux, J. E. C., Parkes, J., Haiden, A., and Tapper, S. (1998). Allozyme heterozygosity and fluctuating asymmetry in brown hares Lepus europaeus introduced to New Zealand: Developmental homeostasis in populations with a bottleneck history. Acta Theriol., Suppl. 5:35–52.Google Scholar
  45. Suchentrunk, F., Polster, K., Giacometti, M., Ratti, P., Thulin, C.-G., Ruhlé, C., Vasil'ev, A. G., and Slotta-Bachmayr, L. (1999). Spatial partitioning of allozyme variability in European mountain hares (Lepus timidus): Gene pool divergence across a disjunct distributional range? Z. Säugetierkunde 64:1–11.Google Scholar
  46. Suchentrunk, F., Michailov, C., Markov, G., and Haiden, A. (2000a). Population genetics of Bulgarian brown hares Lepus europaeus: Allozymic diversity at zoogeographical crossroads. Acta Theriol. 45:1–12.Google Scholar
  47. Suchentrunk, F., Alkon, P. U., Willing, R., and Yom-Tov, Y. (2000b). Epigenetic dental variability of Israeli hares (Lepus sp.): Ecogenetic or phylogenetic causation? J. Zool. (London) 252:503–515.Google Scholar
  48. Suchentrunk, F., Jaschke, C., and Haiden, A. (2001). Little allozyme and mtDNA variability in brown hares (Lepus europaeus) from New Zealand and Britain: A legacy of bottlenecks? Mamm. Biol. 66:48–59.Google Scholar
  49. Suchentrunk, F., Mamuris, Z., Sfougaris, A. I., and Stamatis, C. (2003). Biochemical genetic variability in brown hares (Lepus europaeus) from Greece. Biochem. Genet. 41:127–140.PubMedCrossRefGoogle Scholar
  50. Suchentrunk, F., Mamuris, Z., Stamatis, C., Kryger, U., and Alkon, P. U. (in press): Skull shape and molecular differentiation among brown hares (L. europaeus), cape hares (Lepus capensis) and hares from Israel, a presumed contact zone of these two species. Biol. J. Linn. Soc.Google Scholar
  51. Swofford, D. L.; and Selander, R. B. (1989). BIOSYS-1: A computer program for the analysis of allelic variation in population genetics and biochemical systematics. Release 1.7. Users manual. Illinois Natural History Survey, Champaign.Google Scholar
  52. Sych, L. (1965). Fossil Leporidae from the Pliocene and Pleistocene of Poland. Acta Zool. Cracov. 10:1–83.Google Scholar
  53. Thulin, C.-G., Jaarola, M., and Tegelström, H. (1997). The occurrence of mountain hare mitochondrial DNA in wild brown hares. Mol. Ecol. 6:463–467.PubMedCrossRefGoogle Scholar
  54. Vapa, L., Obreht, D., Vapa, M., and Selmic, V. (2002). Genetic variability in brown hare (Lepus europaeus) populations in Yugoslavia. Z. Jagdwiss. 48 (Suppl.):261–266.Google Scholar
  55. Vapa, L., Davidovic, M., Obreht, D., Hammer, S., and Suchentrunk, F. (in press). Allozyme variability of brown hares (Lepus europaeus) from the Vojvodina region (Serbia and Montenegro), compared to central and southeastern European populations. Acta Zool. Acad. Sci. Hung.Google Scholar
  56. Vigne, J. D. (1992). Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia since the last ice age. Mammal Rev. 2:87–89.Google Scholar
  57. Weir, B. S., and Cockerham, C. C. (1984). Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370.Google Scholar
  58. Wilson, D. E., and Reeder, D. A. M. (eds.) (1993). Mammal Species of the World: A Taxonomic and Geographic Reference, 2nd edn., Smithsonian Institution Press, Washington, DC, 1207 pp.Google Scholar
  59. Wright, S. (1978). Evolution and Genetics of Populations, 4: Variability within and among natural populations. University of Chicago Press, Chicago, 580 pp.Google Scholar

Copyright information

© Springer Science + Business Media, Inc. 2005

Authors and Affiliations

  • Hichem Ben Slimen
    • 1
  • Franz Suchentrunk
    • 2
  • Abdelmajid Memmi
    • 3
  • Amel Ben Ammar Elgaaied
    • 1
  1. 1.Laboratoire de Génétique Moléculaire, Immunologie et Biotechnologie, Faculté des Sciences de TunisTunisTunisia
  2. 2.Research Institute of Wildlife EcologyUniversity of Veterinary Medicine ViennaViennaAustria
  3. 3.Faculté de Pharmacie de MonastirMonastirTunisia

Personalised recommendations