Molecular Ecology (2008) 17, 21012106

NEWS AND VIEWS

Blackwell Publishing Ltd

PERSPECTIVE

Mountain coniferous forests, refugia and butterflies

Z O LT N VA R G A
Department Evolutionary Zoology, University of Debrecen, Egyetem tr 1, H-4010 Debrecen, Hungary

Abstract
The boreal coniferous forests form the most extended vegetation zone of the Northern Hemisphere. As opposed to North America, they are disconnected from the mountain coniferous forests in Europe, because of the dominant eastwest direction of the mountain chains. Consequently, the mountain forests show some unique characteristic features of glacial survival and postglacial history, as well. The mountain coniferous forests have numerous common floral and faunal elements with the boreal zone. However, the few unique faunal elements of the European mountain coniferous forests can be used to unravel the peculiar patterns and processes of this biome. In this issue of Molecular Ecology, Thomas Schmitt and Karola Haubrich (2008) use the relatively common and taxonomically well-studied butterfly, the large ringlet (Erebia euryale) to identify the last glacial refugia and postglacial expansion routes. Keywords: Carpathian biodiversity, extra-Mediterranean core areas, forest refugia, large ringlet (Erebia euryale), Weichsel glaciation

Received 12 January 2008; revision accepted 13 February 2008

A classic monoglacialistic view was that continental species arrived postglacially to Europe by a Siberian invasion. Two assumptions strongly shaped these ideas: (i) The climatic effects were generally milder in Siberia because of the huge unglaciated areas, and (ii) No arboreal refuges could exist north of the Mediterranean peninsulas. This picture was radically changed by findings of full-glacial forests in Europe north of the transversal mountain ranges, the phylogeography of cold-tolerant animal species and the biogeography and faunal history of European mountain butterflies (reviewed by Varga 2003; Schmitt 2007; Varga & Schmitt 2008). Full-glacial forests in Eastern Europe were often questioned, but also repeatedly confirmed by several macrofossil and palynological studies from the Carpathians which demonstrated that the most cold-resistant trees survived in refugial
Correspondence: Zoltn Varga, Fax: +36 52 512 941; E-mail: zvarga@tigris.unideb.hu

pockets in the hilly areas of the Carpathians during the last full glaciation (Fig. 1). Similarly, forest refugia were also proved for southern Moravia, the Eastern Alps, the Dinaric Mountains and in the eastern Balkans (e.g. Willis & Andel 2004; Magri et al. 2006). It was also predicted that the Mediterranean sanctuaria in general were not the core areas of postglacial expansion into deglaciated areas (Widmer & Lexer 2001). Thus, there was a need for new paradigms for the phylogeography of cold-resistant arboreal species, and their associated flora and fauna (Steward & Lister 2001). In this issue, Schmitt & Haubrich (2008) reveal the major patterns of recent glacial and postglacial history for the European mountain coniferous forests by studying the large ringlet, Erebia euryale, a well-known butterfly species. Most other species occurring in these forests have a large Eurasian or Euro-Siberian range and are thus hardly suitable for this sort of study. However, the large ringlet is a European endemic butterfly, is fairly widely dispersed in central and southern European mountains and is closely connected with the subalpine coniferous belt. It does not occur in northern Europe, Scandinavia or Asia. Therefore, survival of this species in European coniferous forest refugia during the last glaciation is the most plausible working hypothesis. These species can thus be used to answer questions about the allocation and extension of these refugia. Which core areas preserved a significant amount of genetic variation, and which refugial populations were involved in the postglacial re-population of suitable habitats? The authors have thoroughly reviewed and evaluated both the earlier and more recent references and suggested a plausible explanation for the glacial survival and postglacial re-population for an important component of the European mountain fauna. They used the established methods of allozyme electrophoresis, which reflect only a minor fraction of the actual genetic changes. However, these data clearly show patterns of genetic differentiation along a geographical gradient, allowing conclusions on the importance of the glacial coniferous mountain forest refugia in Europe. Neighbour-joining phenograms based on genetic distances distinguished four major genetic lineages: (i) the Pyrenees, (ii) the western Alps, (iii) the eastern Alps, and (iv) southeastern Europe. In particular, the three southeastern European samples were interesting, as they clustered very closely together and showed the highest diversity values (particularly in the Carpathians and Rila Mountains.). The genetic distances among the three western Alps samples were considerably higher than between the eastern Alps or southeastern European populations. Also of interest, the sample from the Pyrenees was highly differentiated from all other samples. Differences of this magnitude have been observed also in other species with strong intraspecific genetic structures evolved during long-lasting periods of allopatry in different refugial areas (Habel et al. 2005; Schmitt et al. 2006, 2007). Similar patterns of glacial survival and genetic differentiation were

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Fig. 1 Habitat of Erebia euryale in Romania, Mount Apuseni (West Transylvanian Carpathians). Mt. Apuseni was an important coniferous forest refugium during the last glacial maximum.

Fig. 2 Underside of Erebia euryale isarica female (left side) from the Lower Tatra Mountains (Slovakia) combined with Erebia euryale syrmia female (right side) from the Pirin Mountains (Bulgaria). Erebia euryale isarica is the most widely distributed northern subspecies of E. euryale distributed from northern and eastern Alps to the northern and northeastern Carpathians. Erebia euryale syrmia has shown in the Balkanic mountains a high genetic diversity. The Pirin Mountains was also a coniferous forest refugium during the last glacial maximum and is very rich in endemic alpine plant species.

Fig. 3 Underside of Erebia euryale isarica male (left side) from the Lower Tatra Mountians (Slovakia) combined with Erebia euryale syrmia male (right side) from the Pirin Mountains (Bulgaria).

already shown in several recent papers published in Molecular Ecology (e.g. Schnswetter et al. 2003a, b; Deffontaine et al. 2005; Pinceel et al. 2005; Muster & Berendonk 2006; Hofman et al. 2007). Schmitt and Haubrich have concluded that the mountains of southeastern Europe were the most important reservoirs of the coniferous forests in Europe. The other important aspect of glacial survival and postglacial expansion was shown by the wide distribution of the northern racial group of E. euryale

(E. euryale isarica) from the Carpathians to the Pyrenees, as opposed to the more fragmented pattern of southern races (Figs 2, 3). These results essentially coincide with the conclusions drawn from the molecular biogeography of other extraMediterranean faunal elements of Europe. Extra-Mediterranean core areas have been found for the widely dispersed, cold-tolerant frogs and reptiles Rana arvalis, Zootoca vivipara, Vipera berus (Surget-Groba et al. 2001; Babik et al. 2004; Ursenbacher et al. 2006). Carpathian populations proved to be the sources of colonization into more northern areas for these animals, as well as others such as bank voles and brown bears (Kotlk et al. 2006; Saarma et al. 2007). The identification of Carpathian centres of genetic diversity for so many species shows the importance of habitat conservation in this region.
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Additionally, these results show the power of this type of study, and draw the attention to some unresolved problems of European phylogeography. It would be very interesting to further explore, for example, the pattern of extended but genetically more uniform distributions north of the Alps (as observed in E. euryale isarica and other species), and more southern refugial populations which regularly show more scattered pattern of distribution but higher levels of genetic diversity.
glacier buttercup Ranunculus glacialis (Ranunculaceae). Molecular Ecology, 12, 33733381. Schnswetter P, Tribsch A, Barfuss M, Nikfeld H (2003b) Several Pleistocene refugia detected in the high alpine plant Phyteuma globulariifolium Sternb. & Hoppe (Campanulaceae) in the European Alps. Molecular Ecology, 11, 26372647. Steward JR, Lister AM (2001) Cryptic northern refugia and the origins of the modern biota. Trends in Ecology & Evolution, 16, 608613. Surget-Groba Y, Heulin B, Guillaume C-P et al. (2001) Intraspecific phylogeography of Lacerta vivipara and the evolution of viviparity. Molecular Phylogenetics and Evolution, 18, 449459. Ursenbacher S, Carlsson M, Helfer V et al. (2006) Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data. Molecular Ecology, 15, 3425 3437. Varga Z (2003) The geographical distribution of high mountain macrolepidoptera in Europe. In: Alpine Biodiversity in Europe (eds Nagy L, Grabherr G, Krner C, Thompson DBA), pp. 239257. Springer, Berlin & Heidelberg, Germany. Varga Z, Schmitt T (2008) Types of oreal and oreotundral disjunctions in the western Palearctic. Biological Journal of the Linnean Society, 93, in press. Widmer A, Lexer Ch (2001) Glacial refugia: sanctuaries for allelic richness, but not for gene diversity. Trends in Ecology & Evolution, 16, 267269. Willis KJ, van Andel TH (2004) Trees or no trees? The environments of central and eastern Europe during the Last Glaciation. Quaternary Science Reviews, 23, 23692387.

Acknowledgements
I would like to thank Nolan Kane for his helpful comments on the earlier draft of this manuscript.

References
Babik W, Branicki W, Sandera M et al. (2004) Mitochondrial phylogeography of the moor frog, Rana arvalis. Molecular Ecology, 13, 14691480. Deffontaine V, Libois R, Kotlk P et al. (2005) Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Molecular Ecology, 14, 17271739. Habel JC, Schmitt T, Mller P (2005) The fourth paradigm pattern of postglacial range expansion of European terrestrial species: the phylogeography of the Marbled White butterfly (Satyrinae, Lepidoptera). Journal of Biogeography, 32, 14891497. Hofman S, Spolsky C, Uzzel T et al. (2007) Phylogeography of the fire-bellied toads Bombina: independent Pleistocene histories inferred from mitochondrial genomes. Molecular Ecology, 16, 23012316. Kotlk P, Deffontaine V, Mascheretti S et al. (2006) A northern glacial refugium for bank voles (Clethrionomys glareolus). Proceedings of the National Academy of Sciences, USA, 102 (40), 1486014864. Magri D, Vendramin GG, Comps B et al. (2006) A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist, 171, 199221. Muster C, Berendonk TU (2006) Divergence and diversity: lessons from an arcticalpine distribution (Pardosa saltuaria group, Lycosidae). Molecular Ecology, 15, 29212933. Pinceel J, Jordaens K, Pfenninger M, Backeljau T (2005) Rangewide phylogeography of a terrestrial slug in Europe: evidence for Alpine refugia and rapid colonization after the Pleistocene glaciations. Molecular Ecology, 14, 11331150. Saarma U, Ho SYW, Pybus OG et al. (2007) Mitogenetic structure of brown bears (Ursus arctos L.) in northeastern Europe and a new time frame for the formation of European brown bear lineages. Molecular Ecology, 16, 401413. Schmitt T (2007) Molecular biogeography of Europe: pleistocene cycles and postglacial trends. Frontiers in Zoology, 4, 11 doi: 10.1186/1742-9994-4-11. Schmitt T, Haubrich K (2008) The genetic structure of the mountain forest butterfly Erebia euryale unravels the late Pleistocene and Postglacial history of the mountain coniferous forest biome in Europe. Molecular Ecology, 17, 21942207. Schmitt T, Hewitt GM, Mller P (2006) Disjunct distributions during glacial and interglacial periods in mountain butterflies: Erebia epiphron as an example. Journal of Evolutionary Biology, 19, 108113. Schmitt T, Rkosy L, Abadjiev S, Mller P (2007) Multiple differentiation centres of a non-Mediterranean butterfly species in south-eastern Europe. Journal of Biogeography, 34, 939950. Schnswetter P, Paun O, Tribsch A, Nikfeld H (2003a) Out of the Alps: colonization of northern Europe by east Alpine populations of the

The author is professor of Zoology and Evolutionary Biology at the University of Debrechen, Hungary. His research focuses mostly on taxonomy, evolutionary biology, biogeography and phylogeography of Lepidoptera, but he is also involved in biodiversity research and conservation, scientific illustrations, etc.

doi: 10.1111/j.1365-294X.2008.03744.x
2103???AND VIEWS NEWS 2 0101??? February 2008 3715 10.1111/j.1365-294X.2008.03715.x

PERSPECTIVE

Speciation with gene flow could be common

PAT R I K N O S I L
Zoology Department and Centre for Biodiversity Research, University of British Columbia, 6270 University Boulevard, Vancouver, British Columbia, Canada V6T 1Z4

Abstract
The likelihood of speciation in the face of homogenizing gene flow (i.e. without complete geographical isolation) is one of the most debated topics in evolutionary biology. Demonstrating this phenonemon is hampered by the difficulty of isolating the effects of time since population divergence vs. gene flow on levels of molecular genetic differentiation. For example, weak genetic differentiation between taxa could be due to recent divergence, gene flow, or a combination of these factors. Nonetheless, a number of convincing examples of speciation with gene flow have recently

2008 The Author Journal compilation 2008 Blackwell Publishing Ltd