Organisms Diversity & Evolution

, Volume 16, Issue 4, pp 791–808 | Cite as

Species radiation in the Alps: multiple range shifts caused diversification in Ringlet butterflies in the European high mountains

  • Thomas SchmittEmail author
  • Dirk Louy
  • Edineia Zimmermann
  • Jan Christian Habel
Original Article


The distributions of European high mountain species are often characterised by small and geographically isolated populations and, in many cases, have highly complex biogeographic histories. The butterfly genus Erebia represents one of the best examples for small-scale diversification in the European high mountain systems and therefore to understand speciation processes and associated range dynamics of high mountain species. In this study, we analysed 17 polymorphic allozyme loci of 1731 individuals from 49 populations representing four species, one of which has three subspecies: Erebia nivalis; Erebia tyndarus; Erebia ottomana; and Erebia cassioides cassioides, Erebia cassioides arvernensis, and Erebia cassioides neleus. Samples were collected in the high mountain systems of Europe (i.e. Pyrenees, Massif Central, Alps, Apennines, Carpathians, Balkan high mountains). Genetic analyses supported all previously accepted species. However, the genetic differentiation within E. cassioides sensu lato into three geographically delimited groups is justifying species rank: E. arvernensis distributed in the Pyrenees, Massif Central and western Alps; E. cassioides sensu stricto in the eastern Alps and Apennines; and E. neleus in the Balkan mountains and the south-western Carpathians. While the differentiation between western Alps and Massif Central as well as eastern Alps and Apennines was low, the Pyrenees as well as the south-western Carpathians were significantly differentiated from the other regions within the respective taxon. In general, the differentiation among the populations of E. neleus was stronger than between populations of the other taxa. Within E. cassioides, we found a west-east gradient of genetic similarity over the eastern Alps. Based on the obtained genetic structures, we are able to delineate glacial refugia and interglacial range modifications. Based on the genetic structures and genetic diversity patterns, we conclude that, triggered by the glacial-interglacial cycles, repeated range modifications have taken place with subsequent differentiation and speciation in the region of the Alps and Balkans. Colonisations to Pyrenees (E. arvernensis pseudomurina, E. arvernensis pseudocarmenta), Massif Central (E. ottomana tardenota, E. a. arvernensis) and Apennines (E. cassioides majellana) appear to be recent and most probably not older than the last interglacial period.


Allopatric differentiation Allozyme polymorphisms Erebia tyndarus group Glacial-interglacial cycles Ice ages Phylogeography Range shifts Speciation 



This study was supported by the Konrad Adenauer Foundation (PhD fellowship to DL). We acknowledge sampling permits to collect the samples, given from the respective institutions where necessary. We thank many colleagues for field assistance, especially László Rákosy (Cluj), Zoltán Varga (Debrecen) and Matthias Weitzel (Trier) as well as Leonardo Dapporto (Barcelona) and Zoltán Varga (Debrecen) for important constructive suggestions which helped improve the manuscript considerably.

Supplementary material

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© Gesellschaft für Biologische Systematik 2016

Authors and Affiliations

  • Thomas Schmitt
    • 1
    • 2
    • 3
    Email author
  • Dirk Louy
    • 3
  • Edineia Zimmermann
    • 3
    • 4
  • Jan Christian Habel
    • 5
  1. 1.Senckenberg Deutsches Entomologisches InstitutMünchebergGermany
  2. 2.Department of Zoology, Institute of Biology, Faculty of Natural Sciences IMartin Luther University Halle-WittenbergHalle (Saale)Germany
  3. 3.Department of BiogeographyTrier UniversityTrierGermany
  4. 4.Diagnose Genética Médica e Biologia Molecular LtdaCaxias do SulBrazil
  5. 5.Terrestrial Ecology Research Group, Department of Ecology and Ecosystem Management, School of Life Sciences WeihenstephanTechnische Universität MünchenFreisingGermany

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