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Species Radiation in the Alps: Multiple Range Shifts Caused Diversification in Ringlet Butterflies in the European High Mountains

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Species Radiation in the Alps: Multiple Range Shifts Caused Diversification in Ringlet Butterflies in the European High Mountains Org Divers Evol (2016) 16:791–808 DOI 10.1007/s13127-016-0282-6 ORIGINAL ARTICLE Species radiation in the Alps: multiple range shifts caused diversification in Ringlet butterflies in the European high mountains Thomas Schmitt1,2,3 & Dirk Louy3 & Edineia Zimmermann3,4 & Jan Christian Habel5 Received: 28 December 2015 /Accepted: 11 April 2016 /Published online: 22 April 2016 # Gesellschaft für Biologische Systematik 2016 Abstract The distributions of European high mountain spe- However, the genetic differentiation within E. cassioides cies are often characterised by small and geographically iso- sensu lato into three geographically delimited groups is justi- lated populations and, in many cases, have highly complex fying species rank: E. arvernensis distributed in the Pyrenees, biogeographic histories. The butterfly genus Erebia represents Massif Central and western Alps; E. cassioides sensu stricto in one of the best examples for small-scale diversification in the the eastern Alps and Apennines; and E. neleus in the Balkan European high mountain systems and therefore to understand mountains and the south-western Carpathians. While the dif- speciation processes and associated range dynamics of high ferentiation between western Alps and Massif Central as well mountain species. In this study, we analysed 17 polymorphic as eastern Alps and Apennines was low, the Pyrenees as well allozyme loci of 1731 individuals from 49 populations as the south-western Carpathians were significantly differen- representing four species, one of which has three subspecies: tiated from the other regions within the respective taxon. In Erebia nivalis; Erebia tyndarus; Erebia ottomana;andErebia general, the differentiation among the populations of E. neleus cassioides cassioides, Erebia cassioides arvernensis,and was stronger than between populations of the other taxa. Erebia cassioides neleus. Samples were collected in the high Within E. cassioides, we found a west-east gradient of genetic mountain systems of Europe (i.e. Pyrenees, Massif Central, similarity over the eastern Alps. Based on the obtained genetic Alps, Apennines, Carpathians, Balkan high mountains). structures, we are able to delineate glacial refugia and inter- Genetic analyses supported all previously accepted species. glacial range modifications. Based on the genetic structures and genetic diversity patterns, we conclude that, triggered by the glacial-interglacial cycles, repeated range modifications Electronic supplementary material The online version of this article have taken place with subsequent differentiation and specia- (doi:10.1007/s13127-016-0282-6) contains supplementary material, tion in the region of the Alps and Balkans. Colonisations to which is available to authorized users. Pyrenees (E. arvernensis pseudomurina, E. arvernensis * Thomas Schmitt pseudocarmenta), Massif Central (E. ottomana tardenota, [email protected] E. a. arvernensis) and Apennines (E. cassioides majellana) appear to be recent and most probably not older than the last interglacial period. 1 Senckenberg Deutsches Entomologisches Institut, Eberswalder Straße 90, 15374 Müncheberg, Germany . 2 Keywords Allopatric differentiation Allozyme Department of Zoology, Institute of Biology, Faculty of Natural polymorphisms . Erebia tyndarus group . Glacial-interglacial Sciences I, Martin Luther University Halle-Wittenberg, 06099, Halle (Saale), Germany cycles . Ice ages . Phylogeography . Range shifts . Speciation 3 Department of Biogeography, Trier University, 54296 Trier, Germany 4 Diagnose Genética Médica e Biologia Molecular Ltda, Caxias do Introduction Sul, Rio Grande do Sul, Brazil 5 Terrestrial Ecology Research Group, Department of Ecology and The number of phylogeographic studies increased since the Ecosystem Management, School of Life Sciences Weihenstephan, foundation of this scientific discipline, almost 30 years ago Technische Universität München, 85354 Freising, Germany (Avise et al. 1987). Although phylogeographic projects have 792 T.Schmittetal. been performed all around the world (Hewitt 2004), Europe generalised phylogeographic scenario across the European (Hewitt 1999;Schmitt2007) and North America (Soltis et al. high mountain systems. In particular, the European high 2006;Shaferetal.2010;Woodetal.2013) are by far the best mountain massifs with a small proportion of high mountain studied regions. In particular, Europe and the Mediterranean habitats (i.e. the alpine zone), such as the French Massif region have been addressed in many studies (reviewed in Central, the Apennines and the high mountain ranges of the Taberlet et al. 1998; Hewitt 1999;Schönswetteretal.2005; Balkan Peninsula, are poorly studied, and their importance as Schmitt 2007, 2009; Schmitt and Varga 2012;Husemannetal. stepping stones and refugial differentiation centres is far from 2014). This plenitude of studies clearly demonstrated a rather being understood comprehensively (cf. Schmitt et al. 2014). high phylogeographic complexity of the western Palaearctic For these reasons, phylogeographic studies including entire in comparison to other regions of the world, e.g. eastern North groups of closely related high mountain species are a suitable America (reviewed in Soltis et al. 2006), the African savan- study system to enhance our knowledge of the complex bio- nahs (reviewed in Lorenzen et al., 2012) or southern Australia geographic patterns within and among the different high (reviewed in Byrne 2008). However, in contrast to an earlier mountain systems of Europe. One suitable species group with theory (e.g. Reinig 1937, 1950; de Lattin 1949, 1964, 1967), it high potential to enhance our understanding in this context is is not only the warm-adapted species showing complex pat- the Erebia tyndarus species group. This group is composed of terns. Also cold-adapted species with wide distributions at least seven species in Europe (Erebia tyndarus, Erebia (reviewed in Schmitt and Varga 2012) and high mountain taxa cassioides, Erebia nivalis, Erebia calcaria, Erebia rondoui, (reviewed in Schönswetter et al. 2005;Schmitt2009)contrib- Erebia hispania, Erebia ottomana), three species in western ute considerably to the great biogeographic complexity of this Asia (Erebia graucasica, Erebia transcaucasica, Erebia region. iranica) and the Holarctic Erebia callias with its most western With respect to the phylogeographic patterns of high old world populations in the northern Urals (Albre et al. mountain taxa, a highly repetitive pattern has been shown 2008). Many of these species are endemics with small distri- for the Alps. Here, many species have several, often bution ranges; in Europe, only E. cassioides and E. ottomana four, different genetic lineages along this mountain chain are relatively widespread. E. cassioides is found from the (Schönswetter et al. 2005). These genetic lineages have been Cantabrian Mountains in northern Spain to Rila, Pirin and suggested to have evolved in perialpine refugia at the southern Stara Planina in Bulgaria; this species is split into numerous and eastern foothills of the Alps and retreated to the high regional subspecies and some authors argue that this taxon altitudes along the postglacial warming and the melting of might be a complex of closely related allopatric species. the glaciers (Schönswetter et al. 2005). This phylogeographic E. ottomana is widely distributed in most high mountain sys- pattern is now considered the differentiation paradigm for the tems of the Balkan Peninsula, but is also found in north- Alps. Other studies, yet less in number, have suggested sur- western Anatolia, the Monte Baldo and the south-eastern vival at nunataks, i.e. mountain tops above the glaciers Massif Central. E. tyndarus, E. nivalis and E. calcaria are (Stehlik et al. 2001, 2002; Holderegger et al. 2002; Stehlik endemic to different regions of the Alps, while E. rondoui is 2002), or even north of the mountain chain of the Alps restricted to the Pyrenees and E. hispana to the Sierra Nevada (Schmitt et al. 2006). Bringing together such genetic data with in southern Spain (Albre et al. 2008 ; Tshikolovets 2011). recent distribution patterns of species, palaeoecological stud- This species group has already attracted some attention but ies, niche models, etc. allows the reconstruction of glacial mostly regarding systematics (e.g. Lorković 1953, 1957, refugia for species today distributed in the high altitudes of 1958; Popescu-Gorj 1962;Lattesetal.1994; Jutzeler et al. the Alps relatively robustly. Furthermore, the combination of 2002;Martinetal.2002; Albre et al. 2008) or the biogeogra- all these methods and data helps to understand the processes phy of single species at the regional scale (Louy et al. 2014a). involved in range dynamics triggering the observed genetic However, a comprehensive study analysing the genetic struc- differentiations. tures of all more widespread species of this group in Europe is However, much less in known about the phylogeographic missing. For this reason, we sampled 1731 individuals at 49 structures of other mountain systems of Europe. So far, bio- localities across all major European high mountain systems, geographic links between adjoining high mountain systems i.e. Pyrenees, French Massif Central, Alps, Apennines, based on morphological and distribution data (Varga and Carpathians and several high mountain systems of the Schmitt 2008) were demonstrated (reviewed in Schmitt Balkan Peninsula. These samples were analysed by allozyme 2009 ), and suitable phylogeographic data
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