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Influence of management regime and population history on genetic diversity and population structure of brown hares (Lepus europaeus) in an Italian province

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Abstract

In many areas, the management of overexploited populations of brown hare (Lepus europaeus) is based on annual restocking. While in some cases exotic hares are introduced, in some others hares are captured locally within protected areas and subsequently released into hunting grounds. We evaluated the genetic effects of this management regime in an Italian province where the brown hare population has recovered in the last few decades, by sequencing the hypervariable domain 1 of the mitochondrial control region and by genotyping eight autosomal microsatellites in hares sampled in both hunting and non-hunting areas. Both nuclear (H e = 0.68 and H o = 0.65) and mitochondrial variability (h = 0.853 and π = 0.012) were in line with other European populations. When comparing our data with mitochondrial sequences retrieved from GenBank, out of the 21 detected haplotypes, 14 were private to our study area. While 4.6 % of the individuals were found to carry haplotypes attributable to past introductions, 41.5 % grouped within a well-supported lineage, previously identified with a presumed native Italian taxon, L. e. meridiei. Despite the detectable geographic partitioning of mitochondrial haplotypes across the province, no genetic structure resulted from microsatellites analysis, indicating that no reproductive barriers exist among hares carrying different mitochondrial lineages. In conclusion, the local management seems to have contributed to the recovery of the species and to a full admixture of nuclear genes in the province. However, neither the extensive translocations nor the possible introductions of exotic heads seem to have completely undermined the local mitochondrial lineages.

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References

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Malden, pp 421–449

    Google Scholar 

  • Amori G, Angelici FM, Prigioni C, Vigna Taglianti A (1996) The mammal fauna of Italy: a review. Hystrix 8:3–7

    Google Scholar 

  • Andersen LW, Fredsted T, Wincentz T, Pertoldi C (2009) Brown hares on the edge: genetic population structure of the Danish brown hare. Acta Theriol 54:97–110

    Article  Google Scholar 

  • Andersson A-C, Thulin C-G, Tegelström H (1999) Applicability of rabbit microsatellite primers for studies of hybridisation between an introduced and a native hare species. Hereditas 130:309–315

    Article  CAS  PubMed  Google Scholar 

  • Angelici FM (1998) Lepre europea (autoctona) Lepus europaeus meridiei, Lepre appenninica Lepus corsicanus, Lepre sarda Lepus capensis mediterraneus. In: Bulgarini F, Calvario E, Fraticelli F, Petretti F, Sarrocco F (eds) Libro Rosso Degli Animali d’Italia. Vertebrati. WWF Italia, Roma, pp 116–117

    Google Scholar 

  • Arnason U, Adegoke JA, Bodin K, Born EW, Esa YB, Gullberg A, Nilsson M, Short RV, Xu X, Janke A (2002) Mammalian mitogenomic relationships and the root of the eutherian tree. Proc Natl Acad Sci U S A 99:8151–8156

    Article  CAS  PubMed  Google Scholar 

  • Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX 4.05, logiciel sous WindowsTM pour la génétique des populations, 4.05. Laboratoire Génome, Populations, Interactions CNRS UMR 5000. Universite´ de Montpellier II, Montpellier

    Google Scholar 

  • Ben Slimen H, Suchentrunk F, Ben Ammar Elgaaied A (2008) On shortcomings of using mtDNA sequence divergence for the systematics of hares (genus Lepus): an example from cape hares. Mamm Biol 73(1):25–32

    Google Scholar 

  • Bertorelle G, Papetti C, Hauffe H, Boitani L (2009) Monitoring and detecting translocations using genetic data. In: Bertorelle G, Bruford MW, Hauffe HC, Rizzoli A, Vernesi C (eds) Population genetics for animal conservation. Cambridge University Press, Cambridge, pp 148–166

    Google Scholar 

  • Bray Y, Devillard S, Marboutin E, Mauvy B, Peroux R (2007) Natal dispersal of European hare in France. J Zool 273:426–434

    Article  Google Scholar 

  • Canu A, Cossu A, Foddai R, Iacolina L, Ben Slimen H, Suchentrunk F, Apollonio M, Scandura M (2012) Differentiation under isolation and genetic structure of Sardinian hares as revealed by craniometric analysis, mitochondrial DNA and microsatellites. J Zool Syst Evol Res 50(4):328–337

    Article  Google Scholar 

  • Champagnon J, Elmberg J, Guillemain M, Gauthier-Clerc M, Lebreton J-D (2012) Conspecifics can be aliens too: a review of effects of restocking practices in vertebrates. J Nat Conserv 20(4):231–241

    Article  Google Scholar 

  • Corander J, Marttinen P, Sirén J, Tang J (2008) Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinforma 9:539

    Article  CAS  Google Scholar 

  • Estonba A, Solís A, Iriondo M, Sanz-Martin MJ, Pérez-Suárez G, Markov G, Palacios F (2006) The genetic distinctiveness of the three Iberian hare species: Lepus europaeus, L. granatensis and L. castroviejoi. Mamm Biol 71:52–59

    Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer H (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fickel J, Schmidt A, Putze M, Pitra C (2005) Genetic structure of populations of European brown hare: implications for management. J Wildlife Manage 69:760–770

    Article  Google Scholar 

  • Fickel J, Hauffe HC, Pecchioli E, Soriguer R, Vapa L, Pitra C (2008) Cladogenesis of the European brown hare (Lepus europaeus Pallas, 1778). Eur J Wildl Res 54:495–510

    Article  Google Scholar 

  • Frantz A, Cellina S, Krier A, Schley L, Burke T (2009) Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance? J Appl Ecol 46:493–505

    Article  Google Scholar 

  • Fredsted T, Wincentz T, Villesen P (2006) Introgression of mountain hare (Lepus timidus) mitochondrial DNA into wild brown hares (Lepus europaeus) in Denmark. BMC Ecol 6:17

    Article  PubMed  CAS  Google Scholar 

  • Hamill RM, Doyle D, Duke EJ (2007) Microsatellite analysis of mountain hares (Lepus timidus hibernicus): low genetic differentiation and possible sex-bias in dispersal. J Mammal 88(3):784–792

    Article  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • 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 34:55–66

    Article  CAS  PubMed  Google Scholar 

  • Koutsogiannouli EA, Moutou KA, Stamatis C, Mamuris Z (2012) Analysis of MC1R genetic variation in Lepus species in Mediterranean refugia. Mamm Biol 77(6):428–433

    Google Scholar 

  • Laikre L, Schwartz MK, Waples RS, Ryman N, The GeM working group (2010) Compromising genetic diversity in the wild: unmonitored large-scale release of plants and animals. Trends Ecol Evol 25:520–529

    Article  PubMed  Google Scholar 

  • Mamuris Z, Sfougaris AI, Stamatis C (2001) Genetic structure of Greek brown hare (L. europaeus) populations as revealed by mtDNA RFLP-PCR analysis: implications for conserving genetic diversity. Biol Conserv 101:187–196

    Article  Google Scholar 

  • Mamuris Z, Moutou KA, Stamatis C, Sarafidou T, Suchentrunk F (2010) Y DNA and mitochondrial lineages in European and Asian populations of the brown hare (Lepus europaeus). Mamm Biol 75(3):233–242

    Google Scholar 

  • Melo-Ferreira J, Alves PC, Rocha J, Ferrand N, Boursot P (2011) Interspecific X-chromosome and mitochondrial DNA introgression in the Iberian hare: selection or allele surfing? Evolution 65:1956–1968

    Article  PubMed  Google Scholar 

  • Melo-Ferreira J, Boursot P, Carneiro M, Esteves PJ, Farelo L, Alves PC (2012) Recurrent introgression of mitochondrial DNA among hares (Lepus spp.) revealed by species-tree inference and coalescent simulations. Syst Biol 61(3):367–381

    Article  CAS  PubMed  Google Scholar 

  • Modesto P, Cava PL, Peletto S, Colussi S, Vidus Rosin A, Meriggi A, Acutis PL (2011) Evaluation of genetic variability in brown hare populations from two protected areas in northern Italy. Hystrix, It J Mamm 22(2):257–268

    Google Scholar 

  • Mougel F, Mounolou JC, Monnerot M (1997) Nine polymorphic microsatellite loci in the rabbit, Oryctolagus cuniculus. Anim Genet 28:58–71

    Article  CAS  PubMed  Google Scholar 

  • Olden JD, Poff NL, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24

    Article  PubMed  Google Scholar 

  • Pamilo P, Nei M (1988) Relationships between gene trees and species trees. Mol Biol Evol 5:568–583

    CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2006) Genalex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • 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 8:1805–1817

    Article  CAS  PubMed  Google Scholar 

  • Pierpaoli M, Riga F, Trocchi V, Randi E (2003) Hare populations in Europe: intra and interspecific analysis of mtDNA variation. C R Biol 326:80–84

    Article  CAS  Google Scholar 

  • Pietri C, Alves PC, Melo-Ferreira J (2011) Hares in Corsica: high prevalence of Lepus corsicanus and hybridization with introduced L. europaeus and L. granatensis. Eur J Wildl Res 52:313–321

    Article  Google Scholar 

  • Posada D (2004) Collapse 1.2. Online. Available at http://Darwin.Uvigo.es. Accessed 15 September 2011

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  Google Scholar 

  • Provincial Administration of Arezzo (1991) Wildlife management plan update, vol 2. Provincial Administration of Arezzo, Arezzo

    Google Scholar 

  • Provincial Administration of Arezzo (2006) Wildlife management plan 2006–2010. Provincial Administration of Arezzo, Arezzo

    Google Scholar 

  • Provincial Administration of Arezzo (2012) Wildlife management plan 2012–2015. Provincial Administration of Arezzo, Arezzo

    Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  Google Scholar 

  • Rico C, Rico I, Webb N, Smith S, Bell D, Hewitt G (1994) Four polymorphic loci for the European wild rabbit, Oryctolagus cuniculus. Anim Genet 25:397

    Google Scholar 

  • Rousset F (2008) GENEPOP’007: a complete re-implementation of the GENEPOP software for Windows and Linux. Mol Ecol Res 8:103–106

    Article  Google Scholar 

  • Scandura M, Iacolina L, Ben Slimen H, Suchentrunk F, Apollonio M (2007) Mitochondrial CR-1 variation in Sardinian hares and its relationships with other old world hares (genus Lepus). Biochem Genet 45:305–323

    Article  CAS  PubMed  Google Scholar 

  • Schwartz MK, McKelvey KS (2009) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452

    Article  Google Scholar 

  • Stamatis C, Suchentrunk F, Moutou K, 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 36:515–528

    Article  Google Scholar 

  • Stroh G (1931) Zwei sichrer Altermerkmale beim Hasen. Berliner Tierärztliche Wochenschrift 47(12):180–181 (In German)

    Google Scholar 

  • Suchentrunk F, Mamuris Z, Sfougaris AI, Stamatis C (2003) Biochemical genetic variability in brown hares (Lepus europaeus) from Greece. Biochem Genet 41(5–6):127–140

    Article  CAS  PubMed  Google Scholar 

  • 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 21:151–165

    Article  Google Scholar 

  • Surridge AK, Bell DJ, Rico C, Hewitt GM (1997) Polymorphic microsatellite loci in the European rabbit (Oryctolagus cuniculus) are also amplified in other lagomorphs species. Anim Genet 28:302–305

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface; flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Thulin CG, Malmsten J, Laurila A (2012) Differences in body mass, health status and genetic variation between insular and mainland brown hares (Lepus europaeus) in Sweden. Eur J Wildl Res 58(6):897–907

    Article  Google Scholar 

  • Trocchi V, Riga F (2005) I Lagomorfi in Italia. Linee guida per la conservazione e la gestione. Min. Politiche Agricole e Forestali. Ist. Naz. Fauna Selvatica. Documenti Tecnici 25:1–128

    Google Scholar 

  • 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 4:535–538

    Article  CAS  Google Scholar 

  • Waltari E, Demboski JR, Klein DR, Cook JA (2004) A molecular perspective on the historical biogeography of the northern high latitudes. J Mammal 85(4):591–600

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analyses of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Williams ES, Yuill T, Artois M, Fischer J, Haigh SA (2002) Emerging infectious diseases in wildlife. Rev Sci Tech 21(1):139–57

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the Provincial Administration of Arezzo and the hunting districts AR 1, AR 2, and AR 3 for financial and logistic support to the study. We are particularly grateful to G. Kwiatowski for the coordination of sampling activities, to the AGRIFOREST staff and many hunters for their collaboration to sampling, and to L. Mattioli for his help in collecting information on hare management. We also thank E. Bassi for geographical analysis and G. Falceri for linguistic revision. We finally thank the associate editor and two anonymous reviewers for their valuable comments on the manuscript.

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Authors and Affiliations

  1. Department of Science for Nature and Environmental Resources, University of Sassari, Via Muroni 25, 07100, Sassari, Italy

    Antonio Canu, Massimo Scandura, Antonio Cossu, Laura Iacolina & Marco Apollonio

  2. Piazza della Meridiana 2, 07100, Sassari, Italy

    Sara Luchetti

  3. Provincial Administration of Arezzo, Piazza della Libertà 3, 52100, Arezzo, Italy

    Marco Bazzanti

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  1. Antonio Canu
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  2. Massimo Scandura
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  3. Sara Luchetti
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Correspondence to Massimo Scandura.

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Communicated by C. Gortázar

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Canu, A., Scandura, M., Luchetti, S. et al. Influence of management regime and population history on genetic diversity and population structure of brown hares (Lepus europaeus) in an Italian province. Eur J Wildl Res 59, 783–793 (2013). https://doi.org/10.1007/s10344-013-0731-x

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  • DOI: https://doi.org/10.1007/s10344-013-0731-x

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