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Evolutionary history and species delimitations: a case study of the hazel dormouse, Muscardinus avellanarius

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Abstract

Robust identification of species and significant evolutionary units (ESUs) is essential to implement appropriate conservation strategies for endangered species. However, definitions of species or ESUs are numerous and sometimes controversial, which might lead to biased conclusions, with serious consequences for the management of endangered species. The hazel dormouse, an arboreal rodent of conservation concern throughout Europe is an ideal model species to investigate the relevance of species identification for conservation purposes. This species is a member of the Gliridae family, which is protected in Europe and seriously threatened in the northern part of its range. We assessed the extent of genetic subdivision in the hazel dormouse by sequencing one mitochondrial gene (cytb) and two nuclear genes (BFIBR, APOB) and genotyping 10 autosomal microsatellites. These data were analysed using a combination of phylogenetic analyses and species delimitation methods. Multilocus analyses revealed the presence of two genetically distinct lineages (approximately 11 % cytb genetic divergence, no nuclear alleles shared) for the hazel dormouse in Europe, which presumably diverged during the Late Miocene. The phylogenetic patterns suggests that Muscardinus avellanarius populations could be split into two cryptic species respectively distributed in western and central-eastern Europe and Anatolia. However, the comparison of several species definitions and methods estimated the number of species between 1 and 10. Our results revealed the difficulty in choosing and applying an appropriate criterion and markers to identify species and highlight the fact that consensus guidelines are essential for species delimitation in the future. In addition, this study contributes to a better knowledge about the evolutionary history of the species.

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Acknowledgments

We thank everyone who provided tissue samples of M. avellanarius: Peter Vogel, Valdis Pilats, Luis Popa, Josef Bryja, Achim Schumacher, Helle Vilhelmsen, Nilson Goran (Goteborg Natural History Museum), Gabor Csorba (Hungarian Natural History Museum), Anita Gamauf (Wien Natural History Museum), Hans J Baagøe (Natural History Museum of Denmark). We thank Adrien Rieux, Jiajie Zhang for their kind help and advice for the phylogenetic analyses. This project was supported by the network “Bibliothèque du Vivant” funded by CNRS, the MNHN, INRA and CEA. A. Mouton is supported by a Belgian research fellowship from FRIA (Fonds pour la Formation et la Recherche dans l’Industrie et dans l’Agriculture) and a financial grant from the Belgian FNRS (crédits pour brefs séjours à l’étranger to A. Mouton) and from the University of Liège (Patrimoine) and J. R. Michaux (mandat Maitre de recherches) is supported by a Belgian research fellowship from FNRS (Fonds National pour la Recherche Scientifique) and financial grants from the Belgian FNRS (crédits aux chercheurs to J. R. Michaux). Part of this work was supported by the INTERREG-project “BioGrenzKorr” carried out by Naturstyrelsen, Stiftung Naturschutz Schleswig–Holstein and Schleswig-Holsteinische Landesforsten.

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Authors and Affiliations

  1. Institut de Botanique, Bâtiment 22, Université de Liège (Sart Tilman), Boulevard du Rectorat 27, 4000, Liège, Belgium

    A. Mouton, A. Latinne & J. R. Michaux

  2. Department of Wildlife Ecology, Fisheries and Conservation Biology, University of Maine, 5755 Nutting Hall, Orono, ME, 04469, USA

    A. Mortelliti

  3. Department for Botany and Biodiversity Research University of Vienna, Rennweg 14, 1030, Vienna, Austria

    A. Grill

  4. Dipartimento Biologia Ambientale e Biodiversità, Laboratorio di Zoogeografia ed Ecologia Animale, Via Archirafi 18, 90123, Palermo, Italy

    M. Sara

  5. Slovenian Museum of Natural History, Prešernova 20, 1000, Ljubljana, Slovenia

    B. Kryštufek

  6. Institute of Ecology of Nature Research Centre, Akademijos 2, 08412, Vilnius, Lithuania

    R. Juškaitis

  7. EcoHealth Alliance, 460 West 34th Street, New York, NY, 10001, USA

    A. Latinne

  8. CNR, Institute of Ecosystem Studies, Viale dell’Università 32, 00185, Rome, Italy

    G. Amori

  9. Laboratorio di Genetica, Istituto Superiore per la Protezione e la Ricerca Ambientale (ISPRA), Via Cà Fornacetta 9, 40064, Ozzano Emilia, BO, Italy

    E. Randi

  10. Ortsstr.174, Friedersdorf, 02829, Markersdorf, Germany

    S. Büchner

  11. Stiftung Naturschutz Schleswig-Holstein, Eschenbrook 4, 24113, Molfsee, Germany

    B. Schulz

  12. Gutenbergstr, 8, 24118, Kiel, Germany

    S. Ehlers

  13. Working Group for Wildlife Biology, Justus Liebig University Giessen, Leihgesterner Weg 217, 35392, Giessen, Germany

    J. Lang

  14. Department of Zoology, Palacky University, 17, listopadu 50, 771 76, Olomouc, Czech Republic

    P. Adamik

  15. Natuurpunt Studie/Mammal Working Group, Coxiestraat 11, 2800, Mechelen, Belgium

    G. Verbeylen

  16. Natuurbalans, Radboud Universiteit, Toernooiveld 1, Postbus 6508, 6503 GA, Nijmegen, Netherlands

    M. Dorenbosch

  17. Holtside Bungalow, Batts Corner, Dockenfield, Farnham, Surrey, GU10 4EX, UK

    R. Trout

  18. Department of Bioscience-Wildlife Ecology and Biodiversity, Aarhus University, 8410, Rønde, Denmark

    M. Elmeros

  19. Museo di Storia Naturale della Calabria e Orto Botanico, Via P. Bucci s.n., Rende, CS, Italy

    G. Aloise

  20. Museo di Storia Naturale, Via Filippo de Pisis, 24, 44100, Ferrara, Italy

    S. Mazzoti

  21. Department of Biology, Science and Art Faculty, Bülent Ecevit University, 67100, Zonguldak, Turkey

    F. Matur

  22. CEFE UMR 5175, CNRS-Université de Montpellier-Université Paul-Valéry Montpellier-EPHE – Laboratory Biogeography and Vertebrate Ecology, 1919 route de Mende, 34293, Montpellier, France

    F. Poitevin

  23. Department of Biotechnology, Chemistry and Environmental Engineering, Aalborg University, Sohngaardsholmsvej 57, 9000, Aalborg, Denmark

    E. Randi

  24. CIRAD Animal et Gestion Intégrée des Risques (AGIRs), Campus de Baillarguet, 34093, Montpellier Cedex 5, France

    J. R. Michaux

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  1. A. Mouton
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  2. A. Mortelliti
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  3. A. Grill
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  4. M. Sara
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  5. B. Kryštufek
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  6. R. Juškaitis
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  7. A. Latinne
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  8. G. Amori
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  9. E. Randi
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  10. S. Büchner
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  11. B. Schulz
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  12. S. Ehlers
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  13. J. Lang
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  14. P. Adamik
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  15. G. Verbeylen
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  16. M. Dorenbosch
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  17. R. Trout
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  18. M. Elmeros
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  19. G. Aloise
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  20. S. Mazzoti
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  21. F. Matur
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  22. F. Poitevin
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  23. J. R. Michaux
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Corresponding author

Correspondence to A. Mouton.

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The authors declare there are no conflicts of interest.

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Accession numbers are available at the “European Nucleotide Archive” browser at the address http://www.ebi.ac.uk/ena/data/view/LT614830-LT614893 and in Supplementary Table 6.

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Mouton, A., Mortelliti, A., Grill, A. et al. Evolutionary history and species delimitations: a case study of the hazel dormouse, Muscardinus avellanarius . Conserv Genet 18, 181–196 (2017). https://doi.org/10.1007/s10592-016-0892-8

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