Skip to main content

Advertisement

Log in

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

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aaris-Sørensen K (1998) Danmarks forhistoriske dyreverden. Gyldendal, Denmark

    Google Scholar 

  • Agapow P-M, Bininda-Emonds OR, Crandall KA, Gittleman JL, Mace GM, Marshall JC et al (2004) The impact of species concept on biodiversity studies. Q Rev Biol 79:161–179

    Article  PubMed  Google Scholar 

  • Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Wiley, New York

    Google Scholar 

  • Baker RJ, Bradley RD (2006) Speciation in mammals and the genetic species concept. J Mammal 87:643–662

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N et al (1996–2004) GENETIX 4.05, Logiciel Sous Windows TM Pour la Génétique des Populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier

  • Bradley RD, Baker RJ (2001) A test of the genetic species concept: cytochrome-b sequences and mammals. J Mammal 82:960–973

    Article  Google Scholar 

  • Casanovas-Vilar I, Moyà-Solà S, Agustí J, Köhler M (2005) The geography of a faunal turnover: tracking the Vallesian Crisis. In: Elewa AMT (ed) Migration of organisms. Springer, New York, pp 247–300

    Chapter  Google Scholar 

  • Casanovas-Vilar I, García-Paredes I, Alba DM, Van Den Hoek Ostende LW, Moyà-Solà S (2010) The European Far West: miocene mammal isolation, diversity and turnover in the Iberian Peninsula. J Biogeogr 37:1079–1093

    Article  Google Scholar 

  • Chang SW, Oshida T, Endo H, Nguyen ST, Dang CN, Nguyen DX, Jiang X, Li ZJ, Lin LK (2011) Ancient hybridization and underestimated species diversity in Asian striped squirrels (genus Tamiops): inference from paternal, maternal and biparental markers. J Zool 285:128–138

    Article  Google Scholar 

  • Colangelo P, Bannikova AA, Krystufek B, Lebedev VS, Annesi F, Capanna E et al (2010) Molecular systematics and evolutionary biogeography of the genus Talpa (Soricomorpha: Talpidae). Mol Phylogenet Evol 55:372–380

    Article  CAS  PubMed  Google Scholar 

  • Corbet GB (1978) The mammals of the Palearctic Region: a taxonomic review. British Museum (Natural History), London

    Google Scholar 

  • Costeur L, Legendre S, Aguilar J-P, Lécuyer C (2007a) Marine and continental synchronous climatic records: towards a revision of the European Mid-Miocene mammalian biochronological framework. Geobios 40:775–784

    Article  Google Scholar 

  • Costeur L, Montuire S, Legendre S, Maridet O (2007b) The Messinian event: what happened to the peri-Mediterranean mammalian communities and local climate? Geobios 40:423–431

    Article  Google Scholar 

  • Cracraft J (1983) Species concepts and speciation analysis. In: Johnston RF (ed) Current ornithology. Plenum Press, New York, pp 159–187

    Chapter  Google Scholar 

  • De Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56:879–886

    Article  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Earl DA, vonHoldt BM (2011) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Cons Gen Res 4:359–361

    Article  Google Scholar 

  • Estoup A, Jarne P, Cornuet JM (2002) Homoplasy and mutation model at microsatellite loci and their consequences for population- genetics analysis. Mol Ecol 11:1591–1604

    Article  CAS  PubMed  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 HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Res 10:564–567

    Article  Google Scholar 

  • Fortelius M, Eronen J, Liu L, Pushkina D, Tesakov A, Vislobokova I et al (2006) Late Miocene and Pliocene large land mammals and climatic changes in Eurasia. Palaeogeogr Palaeoclimatol Palaeoecol 238:219–227

    Article  Google Scholar 

  • Fortelius M, Werdelin L, Andrews P, Bernor RL, Gentry A, Humphrey L, Mittmann HW, Viranta S (1996) Provinciality, diversity, turnover and paleoecology in land mammal faunas of the later Miocene of western Eurasia. In: Bernor RL, Fahlbusch V, Mittmann HV (eds) The Evolution of Western Eurasian Neogene Mammal Faunas. Columbia University Press, New York, pp 414–448

    Google Scholar 

  • Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927

    Article  Google Scholar 

  • Frankham R, Ballou JD, Dudash MR, Eldridge MDB, Fenster CB, Lacy RC et al (2012) Implications of different species concepts for conserving biodiversity. Biol Conserv 153:25–31

    Article  Google Scholar 

  • Fujisawa T, Barraclough TG (2013) Delimiting species using single-locus data and the Generalized Mixed Yule Coalescent approach: a revised method and evaluation on simulated data sets. Syst Biol 62:707–724

    Article  PubMed  PubMed Central  Google Scholar 

  • Galtier N, Enard D, Radondy Y et al (2006) Mutation hot spots in mammalian mitochondrial DNA. Genome Res 16:215–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3)

  • Guia APO, Saitoh T (2006) The gap between the concept and definitions in the Evolutionarily Significant Unit: the need to integrate neutral genetic variation and adaptive variation. Ecol Res 22:604–612

    Article  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acid Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hardy O, Vekemans X (2002) SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  Google Scholar 

  • Hardy OJ, Charbonnel N, Fréville H, Heuertz M (2003) Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 163:1467–1482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hare MP, Palumbi SR (1999) The accuracy of heterozygous base calling from diploid sequence and resolution of haplotypes using allele-specific sequencing. Mol Ecol 8:1750–1752

    Article  CAS  PubMed  Google Scholar 

  • Hausdorf B (2011) Progress toward a general species concept. Evolution 65:923–931

    Article  PubMed  Google Scholar 

  • Heller R, Frandsen P, Lorenzen ED, Siegismund HR (2013) Are there really twice asmany bovid species as we thought? Syst Biol 62:490–493

    Article  PubMed  Google Scholar 

  • Holden ME (2005) Family gliridae. In: Wilson DE, Reeder DM (eds) Mammal species of the world, 3rd edn. Smithsonian Institute Press, London, pp 819–841

    Google Scholar 

  • Isaac NJB, Mallet J, Mace GM (2004) Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19:464–469

    Article  PubMed  Google Scholar 

  • Juškaitis R, Büchner S (2013) The hazel dormouse. NBB English Edition

  • Kivanç E (1983) Die Haselmaus, Muscardinus avellanarius L., in der Türkei. Bonn zool Beitr 34:419–428

    Google Scholar 

  • Kopelman NM, Mayzel J, Jakobsson M, Rosenberg NA, Mayrose I (2015) Clumpak: a program for identifying clustering modes and packaging population structure inferences across K. Mol Ecol Res 15:1179–1191

    Article  CAS  Google Scholar 

  • Kotsakis T (2003) Fossil glirids of Italy: the state of the art Glíridos fósiles de Italia: situación actual. Coloquios Paleontol 1:335–343

    Google Scholar 

  • Lambeck K (1995) Late Devensian and Holocene shorelines of the British Isles and North Sea from models of glacio-hydro- isostatic rebound. J Geol Soc 152:437–448

    Article  Google Scholar 

  • Legendre S, Montuire S, Maridet O, Escarguel G (2005) Rodents and climate: a new model for estimating past temperatures. Earth Planet Sci Lett 235:408–420

    Article  CAS  Google Scholar 

  • Li S, He K, Yu F-H, Yang Q-S (2013) Molecular phylogeny and biogeography of Petaurista inferred from the Cytochrome b Gene, with implications for the taxonomic status of P. caniceps, P. marica and P. sybilla. PLoS One 8(7):e7046

    Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Luck GW, Daily GC, Ehrlich PR (2003) Population diversity and ecosystem services. Trends Ecol Evol 18:331–336

    Article  Google Scholar 

  • Ludt CJ, Schroeder W, Rottmann O, Kuehn R (2004) Mitochondrial DNA phylogeography of red deer (Cervus Elaphus). Mol Phylogenet Evol 31:1064–1083

    Article  CAS  PubMed  Google Scholar 

  • Masters PM, Flemming NC (1983) Quaternary coast- lines and marine archaeology: towards the prehistory of land bridges and continental shelves. Academic Press. MatLab, London

    Google Scholar 

  • Mills C, Dawson DA, Horsburgh GJ, Godley BJ, Hodgson DJ (2013) Isolation and characterisation of hazel dormouse (Muscardinus avellanarius) microsatellite loci. Conserv Genet Resour 5:687–692

    Article  Google Scholar 

  • Montgelard C, Bentz S, Tirard C, Verneau O, Catzeflis FM (2002) Molecular systematics of sciurognathi (rodentia): the mitochondrial cytochrome b and 12S rRNA genes support the Anomaluroidea (Pedetidae and Anomaluridae). Mol Phylogenet Evol 22:220–233

    Article  CAS  PubMed  Google Scholar 

  • Montgelard C, Matthee CA, Robinson TJ (2003) Molecular systematics of dormice (Rodentia: Gliridae) and the radiation of Graphiurus in Africa. Proc Biol Sci 270:1947–1955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moritz C (1994) Defining ‘evolutionarily significants units’ for conservation. Trends Ecol Evol 9:373–375

    Article  CAS  PubMed  Google Scholar 

  • Mortelliti A, Santulli Sanzo G, Boitani L (2008) Species’ surrogacy for conservation planning: caveats from comparing the response of three arboreal rodents to habitat loss and fragmentation. Biodivers Conserv 18:1131–1145

    Article  Google Scholar 

  • Mortelliti A, Amori G, Capizzi D, Rondinini C, Boitani L (2010) Experimental design and taxonomic scope of fragmentation studies on European mammals: current status and future priorities. Mamm Rev 40:125–154

    Article  Google Scholar 

  • Mouton A, Grill A, Sara M, Kryštufek B, Randi E, Amori G et al (2012a) Using phylogeography to promote dormouse conservation: the case of Muscardinus avellanarius (Rodentia, Gliridae). Peckiana 8:255–264

    Google Scholar 

  • Mouton A, Grill A, Sara M, Kryštufek B, Randi E, Amori G, Juškaitis R, Aloise G, Mortelliti A, Panchetti F, Michaux J (2012b) Evidence of a complex phylogeographic structure in the common dormouse, Muscardinus avellanarius (Rodentia: Gliridae). Biol J Linn Soc 105:648–664

    Article  Google Scholar 

  • Nabholz B, Glemin S, Galtier N (2008) Strong variations of mitochondrial mutation rate across mammals—the longevity hypothesis. Mol Biol Evol 25(1):120–130

    Article  CAS  PubMed  Google Scholar 

  • Nadachoswki A, Daoud A (1995) Patterns of myoxid evolution in the Pliocene and Pleiostocene of Europe. Hystrix 6:141–149

    Google Scholar 

  • Naderi G, Kaboli M, Koren T, Karami M, Zupan S, Rezaei HR, Krystufek B (2014) Mitochondrial evidence uncovers a refugium for the fat dormouse (Glis glis Linnaeus, 1766) in Hyrcanian forests of northern Iran. Mamm Biol-Zeitschrift für Säugetierkd 79:202–207

    Article  Google Scholar 

  • Naim D, Kemp SJ, Telfer S, Watts PC (2009) Isolation and characterization of 10 microsatellite loci in the common dormouse Muscardinus avellanarius. Mol Ecol Res 9:1010–1012

    Article  Google Scholar 

  • Nunome M, Yasuda SP, Sato JJ, Vogel P, Suzuki H (2007) Phylogenetic relationships and divergence times among dormice (Rodentia, Gliridae) based on three nuclear genes. Zool Scr 36:537–546

    Article  Google Scholar 

  • Parnmen S, Rangsiruji A, Mongkolsuk P, Boonpragob K, Nutakki A, Lumbsch HT (2012) Using phylogenetic and coalescent methods to understand the species diversity in the Cladia aggregata complex (Ascomycota, Lecanorales). PLoS One 7:e52245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perez GCL, Libois R, Nieberding CM (2013) Phylogeography of the garden dormouse Eliomys quercinus in the western Palearctic region. J Mammal 94:202–217

    Article  Google Scholar 

  • Pons J, Barraclough T, Gomez-Zurita J, Cardoso A, Duran D, Hazell S et al (2006) Sequence- based species delimitation for the DNA taxonomy of undescribed insects. Syst Biol 55:595–609

    Article  PubMed  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  CAS  PubMed  Google Scholar 

  • Pritchard JK, Wen W (2004) Documentation for STRUCTURE Software Version 2. Available from http://pritch.bsd.uchicago.edu

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut A, Drummond AJ (2009) Tracer v1.5. Available: http://beast.bio.ed.ac.uk/Tracer

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S et al (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–554

    Article  PubMed  PubMed Central  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 

  • Ryder OA (1986) Species conservation and systematics: the dilemma of subspecies. Trends Ecol Evol 1:9–10

    Article  Google Scholar 

  • Santucci F, Emerson BC, Hewitt GM (1998) Mitochondrial DNA phylogeography of European hedgehogs. Mol Ecol 7:1163–1172

    Article  CAS  PubMed  Google Scholar 

  • Sauer J, Hausdorf B (2012) A comparison of DNA-based methods for delimiting species in a Cretan land snail radiation reveals shortcomings of exclusively. Cladistics 28:300–316

    Article  Google Scholar 

  • Searle JB, Kotlίk P, Rambau RV, Marková S, Herman JS, McDevitt AD (2009) The Celtic fringe of Britain: insights from small mammal phylogeography. Proc R Soc B Biol Sci 276:201–207

    Article  CAS  Google Scholar 

  • Simson S, Ferrucci L, Kurtonur C, Ozkan B, Filippucci MG (1994) Phalli and bacula of european dormice: description and comparison. Hystrix 6:231–244

    Google Scholar 

  • Snell C, Tetteh J, Evans IH (2005) Phylogeography of the pool frog (Rana lessonae Camerano) in Europe: evidence for native status in Great Britain and for an unusual postglacial colonization route. Biol J Linn Soc 85:41–51

    Article  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 57:758–771

    Article  PubMed  Google Scholar 

  • Storch G (1978) Gliridae-Schlafer. In: Niethammer J, Krapp F (eds) Handbuch der saugetiere Europas. Akad, Wiesbaden, pp 201–280

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei N, 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  PubMed Central  Google Scholar 

  • Tobien H (1967) Subdivision of Pontian mammal faunas. Giorn Geol 35:1–5

    Google Scholar 

  • Vilhelmsen H (2003) Status of dormice (Muscardinus avellanarius) in Denmark. Acta Zool Acad Sci Hungaricae 49:139–145

    Google Scholar 

  • Wilting A, Courtiol A, Christiansen P, Niedballa J, Scharf AK, Orlando L, Balkenhol N, Hofer H, Kramer-Schadt S, Fickel J, Kitchener AC (2015) Planning tiger recovery: understanding intraspecific variation for effective conservation. Sci Adv 1:e1400175

    Article  PubMed  PubMed Central  Google Scholar 

  • Zachos FE, Lovari S (2013) Taxonomic inflation and the poverty of the Phylogenetic Species Concept – a reply to Gippoliti and Groves. Hystrix 24(2):142–144

    Google Scholar 

  • Zachos JC, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    Article  CAS  PubMed  Google Scholar 

  • Zachos FE, Apollonio M, Bärmann EV, Festa-bianchet M, Göhlich U, Christian J et al (2013) Species inflation and taxonomic artefacts—a critical comment on recent trends in mammalian classification. Mamm Biol-Zeitschrift für Säugetierkd 78:1–6

    Article  Google Scholar 

  • Zhang D-X, Hewitt GM (2003) Nuclear DNA analyses in genetic studies of populations: practice, problems and prospects. Mol Ecol 12:563–584

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Kapli P, Pavlidis P, Stamatakis A (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics 29(22):1–8

    Article  Google Scholar 

  • Zink RM, Barrowclough GF (2008) Mitochondrial DNA under siege in avian phylogeography. Mol Ecol 17:2107–2121

    Article  CAS  PubMed  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Mouton.

Ethics declarations

Conflict of interest

The authors declare there are no conflicts of interest.

Additional information

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.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 41 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-016-0892-8

Keywords

Navigation