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European Journal of Wildlife Research

, Volume 57, Issue 2, pp 313–321 | Cite as

Hares in Corsica: high prevalence of Lepus corsicanus and hybridization with introduced L. europaeus and L. granatensis

  • Christian Pietri
  • Paulo Célio Alves
  • José Melo-Ferreira
Original Paper

Abstract

The Italian hare, Lepus corsicanus, was first described in Corsica more than 100 years ago, but the knowledge on the status of the species in this island remains scarce. Moreover, frequent introductions of thousands of individuals from other hare species, namely Lepus europaeus and Lepus granatensis, into Corsica are known to have occurred and an updated assessment of the prevalence of L. corsicanus in Corsica is therefore of utmost importance. Here, to estimate the relative prevalence of the hare species present in Corsica, we conducted a molecular analysis on 67 samples collected by hunters between 2002 and 2007 in 36 Corsican communes. Sequencing of portions of the nuclear gene transferrin and of the control region of the mitochondrial DNA allowed classifying most of the collected samples as belonging to L. corsicanus (70.1%). Of the sampled Corsican communes, 86.1% contained this species, while only in 11.1%, L. europaeus was present. Three of the analyzed specimens showed an inconsistent molecular assignment between markers suggesting a hybrid origin: L. corsicanus × L. europaeus, L. corsicanus × L. granatensis, and L. europaeus × L. granatensis. The first two cases of hybridization had never been described in nature, even in studies focusing on hares from Italy where L. corsicanus and L. europaeus are often sympatric. These results stress the real risk of corrosion of the native gene pool of L. corsicanus via hybridization with introduced species. We highlight the need of urgently rethinking the management plan of hare populations in Corsica.

Keywords

Conservation Corsica Italian hare Hybridization Lepus Introduced species 

Notes

Acknowledgements

Funding for this research was provided by Centro de Investigação em Biodiversidade e Recursos Genéticos (CIBIO), Fundação para a Ciência e a Tecnologia (PPCDT/BIA-BDE/58817/2004, PTDC/BIA-EVF/111931/2009, and PTDC/BIA-EVF/115069/2009 research projects, and SFRH/BPD/43264/2008 post-doc grant to José Melo-Ferreira), the Fédération des Chasseurs de Haute-Corse, and the Fédération des Chasseurs de Corse-du-Sud. DNA sequencing was performed on the platform of Centro de Testagem Molecular (CTM) of CIBIO. We thank Nuno Ferrand for his comments and suggestions on this work. We are indebted to the people who were directly involved in collecting the biological material used, particularly all hare hunters and Roger Maupertuis, Paul Ettori, Christian Olivesi, and Victor Acquaviva. We also thank Nils Meunier and two anonymous reviewers for their helpful comments on the manuscript.

References

  1. Alves PC, Ferrand N, Suchentrunk F, Harris DJ (2003) Ancient introgression of Lepus timidus mtDNA into L. granatensis and L. europaeus in the Iberian Peninsula. Mol Phylogenet Evol 27:70–80PubMedCrossRefGoogle Scholar
  2. Alves PC, Melo-Ferreira J, Branco M, Suchentrunk F, Ferrand N, Harris DJ (2008a) Evidence for genetic similarity of two allopatric European hares (Lepus corsicanus and L. castroviejoi) inferred from nuclear DNA sequences. Mol Phylogenet Evol 46:1191–1197PubMedCrossRefGoogle Scholar
  3. Alves PC, Melo-Ferreira J, Freitas H, Boursot P (2008b) The ubiquitous mountain hare mitochondria: multiple introgressive hybridization in hares, genus Lepus. Philos Trans R Soc Lond B Biol Sci 363:2831–2839PubMedCrossRefGoogle Scholar
  4. Angelici FM, Luiselli L (2001) Distribution and status of the Apennine hare Lepus corsicanus in continental Italy and Sicily. Oryx 35:245–249Google Scholar
  5. Aragon T (2008) Epitools: epidemiology tools. R package version 0.5–7. http://www.medepi.com
  6. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  7. Dubray D, Roux D, Gardes ONC (1984) Répartition des lagomorphes (lièvre commun et lapin de garenne) en Corse. Bull Mens Off Natl Chasse 85:36–38Google Scholar
  8. Ellerman JR, Morrison-Scott TCS (1951) Checklist of palaearctic and indian mammals 1758 to 1946. Trustees of the British Museum (Natural History), LondonGoogle Scholar
  9. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50PubMedGoogle Scholar
  10. Freitas H (2006) Natural hybridization between the Iberian hare (Lepus granatensis) and the brown hare (L. europaeus) in northern Iberian Peninsula. MSc thesis, Faculdade de Ciências do Porto, PortoGoogle Scholar
  11. Freitas H, Melo-Ferreira J, Alves PC (2006) Hibridação natural entre lebre-europeia e lebre-ibérica na província de Álava: evidência de novos marcadores genéticos. Accazadores 11:46–48Google Scholar
  12. Gissi C, Gullberg A, Arnason U (1998) The complete mitochondrial DNA sequence of the rabbit, Oryctolagus cuniculus. Genomics 50:161–169PubMedCrossRefGoogle Scholar
  13. Kasapidis P, Suchentrunk F, Magoulas A, 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 34:55–66PubMedCrossRefGoogle Scholar
  14. Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC (2005) Invasion from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14:2459–2464PubMedCrossRefGoogle Scholar
  15. Melo-Ferreira J, Boursot P, Randi E, Kryukov A, Suchentrunk F, Ferrand N, Alves PC (2007) The rise and fall of the mountain hare (Lepus timidus) during Pleistocene glaciations: expansion and retreat with hybridization in the Iberian Peninsula. Mol Ecol 16:605–618PubMedCrossRefGoogle Scholar
  16. Melo-Ferreira J, Alves PC, Freitas H, Ferrand N, Boursot P (2009) The genomic legacy from the extinct Lepus timidus to the three hare species of Iberia: contrast between mtDNA, sex chromosomes and autosomes. Mol Ecol 18:2643–2658PubMedCrossRefGoogle Scholar
  17. Miller GS (1912) Catalogue of the mammals of Western Europe (Europe exclusive of Russia) in the collection of the British Museum. British Museum (Natural History), LondonGoogle Scholar
  18. Palacios F (1996) Systematics of the indigenous hares of Italy traditionally identified as Lepus europaeus Pallas, 1778 (Mammalia: Leporidae). Bonn Zool Beitr 5:59–91Google Scholar
  19. Pierpaoli M, Randi E (2005) Evoluzione del genere Lepus in Europa. In: Trocchi V, Riga F (eds) I Lagomorfi in Italia. Linee guida per la conservazione e gestione. Min. Politiche Agricole e Forestali - INFS, Documenti Tecnici 25, pp 8–11Google Scholar
  20. Pierpaoli M, Riga F, Trocchi V, Randi E (1999) Species distinction and evolutionary relationships of the Italian hare (Lepus corsicanus) as described by mitochondrial DNA sequencing. Mol Ecol 8:1805–1817PubMedCrossRefGoogle Scholar
  21. Pietri C (2007) Caccia e protezione delle popolazioni di lepre (Lepus sp.) in Corsica. In: De Filippo G, De Riso L, Riga F, Trocchi V, Troisi SR (eds) Conservazione di Lepus corsicanus De Winton, 1898 e stato delle conoscenze. IGF Publication, Napoli, pp 52–62Google Scholar
  22. Randi E, Mengoni C, Mucci N (2007a) Genetic distinction and assessment of interspecific hybridisation among three of hares (Lepus) in Italy. V European Congress of Mammalogy, Siena, Italy, 21–26 September 2007. Hystrix (N.S.) II, Supp., 362Google Scholar
  23. Randi E, Mengoni C, Mucci N (2007b) Genetica di Lepus corsicanus: evoluzione, speciazione ed assenza di ibridazione interspecifica. In: De Filippo G, De Riso L, Riga F, Trocchi V, Troisi SR (eds) Conservazione di Lepus corsicanus De Winton, 1898 e stato delle conoscenze. IGF Publication, Napoli, pp 37–43Google Scholar
  24. R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna, Austria. http://www.R-project.org
  25. Riga F, Trocchi V, Toso S (2001) Morphometric differentiation between the Italian hare (Lepus corsicanus De Winton, 1898) and European brown hare (Lepus europaeus Pallas, 1778). J Zool 253:241–252CrossRefGoogle Scholar
  26. Riga F, Trocchi V, Angelici FM, Randi E, Pierpaoli M (2003) Lepus corsicanus De Winton, 1898—Apenninenhase. In: Krapp F (ed) Handbuch der Säugetiere Europas Hasentiere. Aula-Verlag, Wiebelsheim, pp 117–135Google Scholar
  27. Romi R (1988) La chasse en Corse. In: Couret A, Ogé F (eds) Droit et Animal. IEP, Toulouse, pp 185–208Google Scholar
  28. Sambrook E, Fritsch F, Maniatis T (1989) Molecular cloning. Cold Spring Harbour Press, Cold SpringGoogle Scholar
  29. Scalera R, Angelici FM (2003) Rediscovery of the Appenine Hare Lepus corsicanus in Corsica. Bolletino del Museo Regionale Scienze Naturali Torino 20:161–166Google Scholar
  30. Scherrer B (1984) Biostatistique. Gaëtan Morin, BouchervilleGoogle Scholar
  31. Stamatis C, Suchentrunk F, Moutou KA, Giacometti M, Haerer G, Djan M, Vapa L, Vukovic M, Tvrtkovic N, Sert H, Alves PC, Mamuris Z (2009) Phylogeography of the brown hare (Lepus europaeus) in Europe: a legacy of south-eastern Mediterranean refugia? J Biogeogr 36:515–528CrossRefGoogle Scholar
  32. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Am J Hum Genet 76:449–462PubMedCrossRefGoogle Scholar
  33. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989PubMedCrossRefGoogle Scholar
  34. Suchentrunk F, Mamuris Z, Stamatis C, Ben Slimen H, Hackländer K, Haerer G, Giacometti M (2005) Introgressive hybridization in wild living mountain hares (L. timidus varronis) and brown hares (L. europaeus) and morphological consequences. Mamm Biol 70(suppl):39–40Google Scholar
  35. Suchentrunk F, Ben Slimen H, Stamatis C, Sert H, Scandura M, Apollonio M, Mamuris Z (2006) Molecular approaches revealing prehistoric, historic, or recent translocations and introductions of hares (genus Lepus) by humans. Hum Evol 21:151–165CrossRefGoogle Scholar
  36. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  37. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  38. Temple HJ, Terry A (2007) The status and distribution of European mammals. Office for Official Publications of the European Communities, LuxembourgGoogle Scholar
  39. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedCrossRefGoogle Scholar
  40. Thulin CG, Jaarola M, Tegelstrom H (1997) The occurrence of mountain hare mitochondrial DNA in wild brown hares. Mol Ecol 6:463–467PubMedCrossRefGoogle Scholar
  41. Thulin CG, Fang M, Averianov AO (2006) Introgression from Lepus europaeus to L. timidus in Russia revealed by mitochondrial single nucleotide polymorphisms and nuclear microsatellites. Hereditas 143:68–76PubMedCrossRefGoogle Scholar
  42. Toschi A (1965) Fauna D'italia: Mammalia. Lagomorpha–Rodentia–Carnivora–Artiodactyla–Cetacea. Calderini, BolognaGoogle Scholar
  43. Trocchi V, Riga F (2005) I Lagomorfi in Italia. Linee guida per la conservazione e gestione. Ist. Naz. Fauna. Selvatica, Documenti Tecnici 25:1–128Google Scholar
  44. Vigne JD (1999) The large “true” Mediterranean islands as a model for the Holocene human impact on the European vertebrate fauna? Recent data and new reflections. In: Benecke N (ed) The Holocene history of European vertebrate fauna. Modern aspects of research. Deutsches Archäologisches Institut Eurasien-Abteilung, Verlag Marie Leidorf GmbH Rahden/Westf, pp 295–322Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Christian Pietri
    • 1
  • Paulo Célio Alves
    • 2
    • 3
  • José Melo-Ferreira
    • 2
  1. 1.Fédération Départementale des Chasseurs de Haute-Corse (FDCHC)BastiaFrance
  2. 2.CIBIO, Centro de Investigação em Biodiversidade de Recursos GenéticosUniversidade do PortoVairãoPortugal
  3. 3.Departamento de Biologia da Faculdade de CiênciasUniversidade do PortoPortoPortugal

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