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Keywords:

  • allozyme electrophoresis;
  • alpine species;
  • ice age;
  • Lepidoptera;
  • phylogeography;
  • Satyrinae

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Over several decades, the distribution patterns and evolution of alpine disjunct species has become an increasingly discussed subject. Large scale genetic analysis has allowed the resolution of the past range changes and intraspecific evolution of many species, in Europe especially of Mediterranean origin. However, the phylogeographic structures of species with arctic–alpine disjunct distribution patterns are relatively poorly studied. The existing phylogeographic analysis (mostly of alpine plant species) supports disjunct distributions during glacial as well as post-glacial periods for a number of species. However, several questions still remain unresolved and we therefore analysed the Mountain Ringlet Erebia epiphron as a model for such alpine disjunct species. We found strong differentiation into five different lineages supporting five differentiation centres: (i) the eastern Pyrenees, (ii) the mountain ranges between the central Pyrenees and south-western Alps, (iii, iv) two areas along the southern Alps margin and (v) the northern Alps margin. We propose that these patterns evolved due to the humidity requirements of this species, which did not allow survival in the dry glacial steppes, but along the margins of the wetter glaciated high mountain ranges.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Climate and its changes are of enormous importance for the distribution of animal and plant species (Parmesan et al., 1999; Thomas & Lennon, 1999). In this context, the major climatic oscillations of the Pleistocene, with switching between shorter warm and more humid periods and longer cold and dry climates, are of great significance (Williams et al., 1998). The biological consequences of these climatic cycles have been discussed for several decades (Reinig, 1938; Holdhaus, 1954; de Lattin, 1967; Müller, 1980). Based on fossil records and chorological evidence, it was argued that temperate species were isolated in southern refugia (e.g. the Mediterranean peninsulas of Europe) and pole-ward expansions during the warm interglacials were proposed that were often combined with loss of diversity during the process (Reinig, 1938; de Lattin, 1967). Recent work applying molecular methods have substantiated and extended these hypotheses (Hewitt, 1996, 1999, 2000, 2001, 2004; Comes & Kadereit, 1998; Taberlet et al., 1998).

It was thought that cold resistant species were probably widely distributed during the last ice age with its cold and dry climatic conditions and only became disjunct after the climate warmed and their habitats shifted pole-wards and to higher elevations in mountains (Reinig, 1938; Holdhaus, 1954; de Lattin, 1967). Recent work on arctic species has revealed that this pattern was an oversimplification. In fact, there is evidence that some arctic animal and plant species survived the last glaciation at high latitudes or north of the extensive ice shields; the evidence is strong for Beringia and north-eastern Asia, weaker for the High Nearctic and doubtful for northern Europe (Abbott et al., 2000; Abbott & Brochmann, 2003; Hewitt, 2004). Much less data is available for alpine species, particularly that including populations from several high mountain systems. Recent work on alpine plant species suggests that many of these did not have continuous distributions during the glacial periods (Despres et al., 2002; Kropf et al., 2002, 2003; Schönswetter et al., 2002, 2003, 2004; Stehlik et al., 2002; Comes & Kadereit, 2003; Stehlik, 2003). However, plants are immobile and even their pollen and seeds often have restricted dispersal (e.g. Despres et al., 2002), so that they tend to show more local genetic patterns, which may not always reflect broader phylogeographic structures.

The hypothesis of disjunct distribution patterns of high mountain species during glacial periods needs further testing, particularly in animals. To test this specific question, one should select as a model an animal species fulfilling the following criteria: (i) the species must have a sufficiently high dispersal ability to spread rapidly into newly emerging suitable habitats ensuring that the species occupies the available space, (ii) once established, populations must be large and stable to reflect large scale structures (i.e. phylogeographic signals) and not recent local population structures and (iii) although having a high dispersal ability, the single individual has to be mostly sedentary so that the phylogeographic patterns are not swamped as for example in migratory species.

The biology of the Mountain Ringlet Erebia epiphron is well known and it matches all these criteria very well. As is the case for most lepidopterans, E. epiphron is able to fly and adopt its distribution to the habitats available. Therefore, the species is widely distributed in the European high mountain systems (Kudrna, 2002). Furthermore, the species’ populations are mostly composed of many individuals (SBN, 1987; Cizek et al., 2003; Kuras et al., 2003) and its populations are quite stable (SBN, 1987; Asher et al., 2001; Kuras et al., 2003). Thus, local population structures are relatively weak (Schmitt et al., in press). Finally, although individuals disperse within their habitats (Konvicka et al., 2002; Kuras et al., 2003), the species has to be considered as sedentary with respect to their habitat patches (Schmitt et al., 2005a).

Using genetic measures we seek to examine the following propositions: (i) the distribution of this species has not been continuous during the glaciations and this glacial disjunct pattern has strongly influenced the present genetic pattern; (ii) parts of different high mountain systems may be colonized post-glacially from the same source region, so that they show major genetic similarities (e.g. the Alps and Pyrenees); (iii) the actual patterns of distribution, which were shaped during the post-glacial period, have had no major impact on the genetic structure due to their relatively recent origins.

Material and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

We analysed a total of 575 individuals of E. epiphron from 16 populations from the Pyrenees, Alps and the Hruby Jesenik Mts (NE Czechia) (Fig. 1). Three populations had less than 35 individuals analysed (Col de Vars: 11; Camporeilles: 13, La Glèbe: 23). Sampling was performed at alpine and subalpine meadows between 1200 and 2400 m.a.s.l. from late June to early August of the years 1997 and 2001–2003. The butterflies were netted in the field, frozen alive in liquid nitrogen and stored under these conditions till analysis.

image

Figure 1. Sampling sites of the 16 analysed populations of E. epiphron. The five genetic groups are given in parentheses – see text and Fig. 2.

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For allozyme electrophoresis, we used cellulose acetate plates applying standard protocols (Richardson et al., 1986; Hebert & Beaton, 1993). We analysed a total of 18 allozyme loci (for loci studied and electrophoretic conditions see Schmitt & Seitz, 2001a; note: Me1 was not analysed for E. epiphron). Allele frequencies and F-statistics were calculated by means of G-Stat (Siegismund, 1993). Hardy–Weinberg equilibrium, genetic disequilibrium, amova and hierarchical F-statistics were performed using Arlequin 2.000 (Schneider et al., 2000). Nei's (1972) standard genetic distances and phylogenetic trees using the neighbour joining and the UPGMA algorithms were constructed with the package PHYLIP Version 3.5.c (Felsenstein, 1993). Bootstraps based on 1000 iterations were calculated with the same software.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

All 18 loci analysed were polymorphic and had banding patterns consistent with known quaternary protein structures (Richardson et al., 1986). Apart from 6Pgdh, Mpi and Me, no further locus exhibited a significant deviation from Hardy–Weinberg equilibrium (all P > 0.05). All female individuals appeared ‘homozygous’ at the three former loci whereas the males were not. Therefore, these three genes most probably are located on the Z chromosome, as already known for the related Erebia medusa (Schmitt & Seitz, 2001a). As female butterflies only have one copy of the Z chromosome, this can explain the deviation from Hardy–Weinberg equilibrium, especially as significant deviation only occurred in populations with a considerable number of females analysed. Excluding all females for this analysis, significant deviation from Hardy–Weinberg equilibrium was only found in the sample from Täschalp. However, the hemizygotic character of these three loci in females does not require further analysis because these are based on allele frequencies. No significant genetic linkage disequilibrium was detected. Therefore, further analyses could be performed using standard population genetics approaches.

The FST over all populations was high (29.1%, P < 0.0001; 28.3%, P < 0.0001 excluding the three samples representing less that 35 individuals). FIS was not significant for the autosomal loci (mean: 2.5%; all P > 0.05 except Pep: P < 0.01). Phenograms based on genetic distances (Nei, 1972) showed a division into two main clusters (1: Pyrenees and western Alps vs. 2: central and eastern Alps and Hruby Jesenik Mts). The UPGMA and the neighbour joining trees showed similar topologies; the latter is shown in Fig. 2. Hierarchical variance analyses revealed about 50.4% of the variance between populations between these two groups (FCT = 0.174, P < 0.0001; only samples >35 individuals: FCT = 0.183, P < 0.0001). Both groups were further subdivided: the Pyrenees/south-western Alps group had two subgroups: 1a: eastern Pyrenees vs. 1b: central Pyrenees/south-western Alps; the central/eastern Alps/Jesenik group had three subgroups: 2a: central southern Alps vs. 2b: eastern southern Alps vs. 2c: northern Alps/Jesenik. These five groups are supported by moderately high bootstrap values. amova distributed 73.0% of the variance among populations among these five groups and only 27.0% within groups (FCT = 0.240, P < 0.0001; only samples >35 individuals: FCT = 0.269, P < 0.0001). Within the two analysed high mountain systems, most of the genetic variance between populations was between groups [Alps (four groups): 71.5%, FCT = 0.249, P < 0.0001; Pyrenees (two groups): 67.0%, FCT = 0.118, P < 0.0001].

image

Figure 2. Neighbour joining diagram of the 16 analysed populations of E. epiphron based on genetic distances (Nei, 1972). Genetic groups are given in parentheses – see text. Values at the nodes of the branches indicate bootstrap percentages from 1000 iterations. Only values above 40% are given. Abbreviations: First part: Pyr, Pyrenes; Second part: country sign, in France with number of department; Third part: A, Aragon; AO, Aosta valley; BE, canton Bern; C, Catalunia; GR, canton Graubünden; SB, Salzburg county.

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Mean genetic distance (Nei, 1972) between all analysed populations was 0.071 (±0.039 SD) (>35 individuals: 0.085 ± 0.040 SD). Distances between populations belonging to different groups (mean: 0.083 ± 0.034 SD; >35 individuals: 0.100 ± 0.033 SD) were significantly higher than within these five groups (mean: 0.033 ± 0.025 SD; U-test: N = 120, Z = −6.21, P < 0.0001; >35 individuals: 0.036 ± 0.016 SD; U-test: N = 78, Z = −5.98, P < 0.0001).

Based on allele frequencies of the 13 analysed populations represented by at least 35 individuals, we calculated the means of four population genetic parameters (Summary results: Table 1). The means of genetic diversity were not significantly different among the five distinguished genetic groups for any of the four tested parameters after Bonferroni correction (Table 1). Detailed data for all populations and allele frequencies can be obtained on request from the corresponding author.

Table 1.  Mean number of alleles per locus (A), exected heterozygosity (He), percentage of polymorphic loci (Ptot: total; P95: with the most common allele not exceeding 95%).
 MeanEPCP/WACSAESANA/JH4,13P
  1. Given are the means over all populations and for each of the five geographical groups (EP, eastern Pyrenees; CP/WA, central Pyrenees and western Alps; CSA, central southern Alps; ESA, eastern southern Alps; NA/J, northern Alpes and Jeseník (CZ); only samples representing at least 35 individuals are included. H- and P-values refer to Kruskal–Wallis anovas testing for significant differences between the five genetic groups.

A2.09 ± 0.262.00 ± 0.002.29 ± 0.172.221.92 ± 0.041.69 ± 0.2010.190.037
He (%)15.4 ± 2.413.5 ± 1.516.4 ± 2.017.714.3 ± 1.512.0 ± 0.87.430.115
Ptot (%)69.7 ± 16.169.5 ± 3.977.8 ± 16.983.358.4 ± 3.950.0 ± 7.96.080.194
P95 (%)43.2 ± 7.244.4 ± 0.046.3 ± 5.750.038.9 ± 7.833.4 ± 7.86.120.191

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Erebia epiphron exhibits a strong hierarchical genetic structure within and between the European high mountain systems. The observed differentiation is so strong that exclusive post-glacial origin is most unlikely. For example, the Woodland Ringlet E. medusa shows four major genetic lineages in Central Europe most probably evolving during Würm glacial isolation (Schmitt & Seitz, 2001a) with the observed differentiation [FST: 14.9%, genetic distance (Nei, 1978) between lineages 0.051 to 0.117] being not as strong as in E. epiphron. Also the differentiations due to glacial isolation in the Chalk-Hill Blue Polyommatus coridon [FST: 6.0%, genetic distance (Nei, 1978) between lineages: 0.041, Schmitt & Seitz, 2001b], the Marbled White Melanargia galathea [FST: 6.1%, genetic distance (Nei, 1978) between lineages: 0.034, Habel et al., 2005] and the Meadow Brown Maniola jurtina [FST: 3.4%, genetic distance (Nei, 1978) between lineages: 0.033, Schmitt et al., 2005b] are less pronounced than in E. epiphron. The differentiation between two lineages of the burnet moth Aglaope infausta evolving in multiple refugia in Iberia [FST: 40.4%, genetic distance (Nei, 1978) between lineages: 0.137, Schmitt & Seitz, 2004] was comparable to that of E. epiphron. Furthermore, the close relationship between populations separated by several hundred kilometres of lowlands (e.g. north-western Alps and Jesenik; central Pyrenees and south-western Alps) effectively excludes post-glacial evolution of this genetic pattern. Of course allozymes are subject to selection and this may influence considerably the allelic frequencies, as shown for the butterfly genus Colias in North America (Watt et al., 1996). However, this factor is unlikely to be of major importance for our analysis because some populations from rather different habitats with presumably different selective pressures (e.g. Grindelwald 2400 m.a.s.l. vs. Jesenik 1200 m.a.s.l.) were almost identical, and populations from very similar habitats separated by small geographical distances and presumably subjected to similar selective pressures were genetically rather different (e.g. Dondénaz vs. Täschalp vs. Berninapass). Furthermore, allozyme analysis and mtDNA sequencing revealed largely similar patterns in the Erebia tyndarus group, with the former being more clear-cut than the latter (Martin et al., 2002).

For all these reasons, we postulate that the onset of the observed differentiation was prior to the present post-glacial (i.e. during the Würm ice age or even a previous glaciation). The marked genetic division into two main groups with five subgroups strongly suggests a scenario with five or more allopatric centres of differentiation in the western part of Europe. In the light of information on paleoclimate and paleovegetation (Huntley & Birks, 1983; Coope, 1994; Gliemeroth, 1995; Williams et al., 1998; Elenga et al., 2000; Tarasov et al., 2000), it is likely that they were located (i) in the unglaciated parts of the eastern and especially south-eastern Pyrenees, (ii) extending westward from the central Pyrenees, spanning the mountain ranges of southern France and reaching eastward to the unglaciated lower parts of the south-western Alps, (iii) in the foot hills of the Alps at the north-western end of the Po valley, (iv) along the southern foot hills of the central and eastern Alps margin and (v) just north of the Alpine glaciers extending from east of the Black Forest (SW Germany) and reaching as far east as the Moravian Basin (E Czech Republic) (Fig. 3).

image

Figure 3. Hypothetical distribution patterns of E. epiphron in Western Europe during the last glaciation. Grey areas show mountain areas above 1000 m.a.s.l.

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There is recent phylogeographic evidence from other mountain species that suggest somewhat similar patterns. Thus, there is a close genetic relationship for Anthyllis montana (Kropf et al., 2002) and for Erebia cassioides (Martin et al., 2002) between Pyrenees and south-western Alps. Three plant species (Phyteuma globulariifolium, Androsace alpina, Ranunculus glacialis) consist of four genetic lineages along the chain of the Alps suggesting multiple differentiation centres along their southern and south-eastern periphery (Schönswetter et al., 2002, 2003, 2004). Finally, Pritzelago alpina shows both a close genetic relationship between the north-eastern Alps and the Carpathians, and a differentiation of south-eastern vs. central and north-eastern Pyrenees (Kropf et al., 2003). All these patterns appear combined in our study species, suggesting that it is a discriminating phylogeographic model.

But why did E. epiphron and many other high mountain species not occur all over the extended European glacial steppes? What triggered its even more scattered glacial distribution pattern compared to the recent one? The most plausible explanation is perhaps the rather dry and continental climate of European glacial steppes; these conditions were most probably not suitable for a butterfly with such humidity demands (SBN, 1987). This hypothesis is further supported by several genetic analyses of alpine and arctic-alpine plant species, where the genetic differentiation between different lineages increased with the species’ need for humidity (Despres et al., 2002; Schönswetter et al., 2002, 2003, 2004; Stehlik et al., 2002; Kropf et al., 2002,2003). Furthermore, another mountain lepidopteran, the burnet moth Zygaena exulans, is well adapted to dry continental mountain climates and shows no strong genetic differentiation between and within the Alps and Pyrenees (Schmitt & Hewitt, 2004). These results argue that dry and cold hardy species were widely distributed over the glacial tundras, but that cold hardy species not tolerant of dryness were strongly restricted to more humid areas around the glaciated high mountain systems. More generally they demonstrate the explanatory value of combining genetic measures with knowledge of species physiology and life history.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

We acknowledge the grant of the Forschungsfonds of the University of Trier enabling the field trip of TS to the Pyrenees and the Alps in 2003 and the allozyme electrophoresis. We thank many colleagues from Spain, France, Switzerland and Austria for their friendship and help to find many of the sampling localities and especially Martin Konvicka (Ceske Budejovice, CZ) for the sample from the Hruby Jeseník Mountains. We are grateful to the governments of Catalunia, Aragon and Salzburg for the sampling permits and to France, Switzerland and Italy not requiring special permissions.

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  2. Abstract
  3. Introduction
  4. Material and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
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