From Africa to Europe and back: refugia and range shifts cause high genetic differentiation in the Marbled White butterfly Melanargia galathea
© Habel et al; licensee BioMed Central Ltd. 2011
Received: 27 January 2011
Accepted: 21 July 2011
Published: 21 July 2011
The glacial-interglacial oscillations caused severe range modifications of biota. Thermophilic species became extinct in the North and survived in southern retreats, e.g. the Mediterranean Basin. These repeated extinction and (re)colonisation events led to long-term isolation and intermixing of populations and thus resulted in strong genetic imprints in many European species therefore being composed of several genetic lineages. To better understand these cycles of repeated expansion and retraction, we selected the Marbled White butterfly Melanargia galathea. Fourty-one populations scattered over Europe and the Maghreb and one population of the sibling taxon M. lachesis were analysed using allozyme electrophoresis.
We obtained seven distinct lineages applying neighbour joining and STRUCTURE analyses: (i) Morocco, (ii) Tunisia, (iii) Sicily, (iv) Italy and southern France, (v) eastern Balkans extending to Central Europe, (vi) western Balkans with western Carpathian Basin as well as (vii) south-western Alps. The hierarchy of these splits is well matching the chronology of glacial and interglacial cycles since the Günz ice age starting with an initial split between the galathea group in North Africa and the lachesis group in Iberia. These genetic structures were compared with past distribution patterns during the last glacial stage calculated with distribution models.
Both methods suggest climatically suitable areas in the Maghreb and the southern European peninsulas with distinct refugia during the last glacial period and underpin strong range expansions to the North during the Postglacial. However, the allozyme patterns reveal biogeographical structures not detected by distribution modelling as two distinct refugia in the Maghreb, two or more distinct refugia at the Balkans and a close link between the eastern Maghreb and Sicily. Furthermore, the genetically highly diverse western Maghreb might have acted as source or speciation centre of this taxon, while the eastern, genetically impoverished Maghreb population might result from a relatively recent recolonisation from Europe via Sicily.
The impacts of climatic oscillations on the earth's biota have been intensively studied . In the western Palaearctic, thermophilic organisms went extinct over major parts of Central and North Europe during cold stages and survived in the lowlands of lower latitudes in often distinct refugia [2–6]. Molecular studies revealed that most of these taxa exclusively survived glacial periods south of the European high mountain chains in the Iberian, Italian and Balkan peninsulas, and some even in additional extra-Mediterranean refugia [7, 8]. The long-term isolation of populations in these retreats over many thousands of years resulted in genetic differentiation . During the warmer interglacial periods, species expanded their distribution ranges northwards and extended their different genetic lineages over more northern areas [9, 10].
In contrast to the three more intensively studied Mediterranean refugia of southern Europe (Iberia, peninsular Italy and the Balkans), little is known about North African refugia and the biogeographical relation between the Maghreb and southern Europe separated by the two narrow sea straits of Gibraltar and Sicily. It has been shown that the Maghreb is often sub-structured following an east-west [e.g. [11–13]] or south-north differentiation pattern [e.g. [5, 14]]; in some cases, genetic continuity was demonstrated between the Maghreb and Sicily [e.g. [15, 16]]. Other studies underline the important role of Sicily as diversification centre for European taxa unravelling deep genetic splits between this island and peninsular Italy (e.g. Erinaceus europaeus: ; Pseudepidalea viridis: [18, 19]). Few molecular analyses also reveal the outstanding importance of North Africa as a refugium for thermophilic species during glacial periods [e.g. [12, 14, 20, 21]]. However, most studies focus either on the Maghreb or the southern European refugia and do not combine the distribution of species all over north-western Africa and throughout Europe.
To study the biogeographical importance of the Maghreb region and its connection with Europe, we selected the Marbled White butterfly species complex Melanargia galathea (Linnaeus, 1758) and Melanargia lachesis (Hübner, 1790) as a model system using two analytical tools (allozyme polymorphisms and distribution modelling). Today, M. galathea is widely distributed from the Maghreb region (mountain ranges of Morocco, Algeria and Tunisia) [22, 23] to the English Midlands , and from the Pyrenees  to the Baltic Sea in Poland . On the Iberian Peninsula, M. galathea is replaced by its sibling species M. lachesis. Thus, the Italian peninsula is the only possible link between North Africa and Europe for M. galathea.
Which refugia are of importance for the glacial survival of the M. galathea /lachesis species complex during the subsequent glacial periods?
Is there any evidence of genetic structuring within the North African and Italian refugia?
Which routes of expansion and retraction followed the butterfly throughout time?
All enzyme loci had banding patterns consistent with known quaternary structures. While most loci were inherited autosomally, 6PGDH and ME were located on the Z chromosome so that hemizygous females (but not males) had a single copy . No general linkage disequilibrium was observed for any locus (all p > 0.05 after Bonferoni correction). A total of 13 analysed loci were polymorphic, but two loci (FUM, GPDH) were monomorphic throughout all samples. Allele frequencies for each enzyme and population are given in an additional file 1.
Sampling location and five parameters of genetic diversity for 41 populations of Melanargia galathe a from its western Palaearctic distribution area and one population of M. lachesis from the Pyrenees: number of individuals analysed (N), mean number of alleles per locus (A), percentage of expected (H e ) and observed (H o ) heterozygosity, percentage of polymorphic loci not exceeding 95% (P95) and total number of polymorphic loci (Ptot)
Date of sampling
H e (%)
H o (%)
T-Table de Yagurta
F-Col de Tende
RO-Porta di Fier Transilvanici
E-Col de Perbes*
Means of sample sizes and genetic diversities of the different genetic groups of Melanargia galathea and M. lachesis; p values of Kruskal Wallis ANOVAs among groups are given
36.0 ± 7.9
2.10 ± 0.19
17.0 ± 2.2
15.3 ± 2.8
34.5 ± 5.4
45.2 ± 9.4
36.0 ± 0.0
2.38 ± 0.10
18.4 ± 1.6
17.6 ± 3.0
36.7 ± 6.7
53.3 ± 5.4
37.4 ± 7.8
2.00 ± 0.17
13.9 ± 2.1
11.6 ± 2.4
33.3 ± 6.7
49.3 ± 8.9
37.7 ± 5.8
2.13 ± 0.13
15.8 ± 1.8
13.4 ± 1.3
33.3 ± 6.6
55.6 ± 10.2
Italy + SE France
35.3 ± 8.3
2.19 ± 0.24
17.9 ± 2.3
15.1 ± 2.6
38.1 ± 8.3
52.4 ± 11.2
eastern Balkans + Central Europe
36.8 ± 7.4
2.04 ± 0.15
17.8 ± 1.7
16.9 ± 2.0
33.7 ± 2.9
38.7 ± 3.6
26.5 ± 15.6
2.01 ± 0.22
15.3 ± 1.3
14.4 ± 1.1
31.6 ± 3.3
40.0 ± 5.5
p (Kruskal Wallis ANOVA)
eastern Balkans + Romania
35.7 ± 8.4
2.05 ± 0.15
17.1 ± 2.2
15.5 ± 1.8
33.3 ± 3.8
39.0 ± 4.6
37.7 ± 7.0
2.03 ± 0.16
18.5 ± 1.1
18.0 ± 1.4
34.0 ± 2.2
38.5 ± 2.9
p (Kruskal Wallis ANOVA)
Analyses of molecular variance for all Melanargia galathea populations and one population of M.lachesis
among individuals within populations
All galathea and lachesis
Sicily and Tunisia
Italy, Balkans, Central Europe
Italy and S France
west Balkan group
east Balkan and Central Europe
Hierarchical variance analyses of Melanargia galathea and M.lachesis among genetic groups
prop. of among groups variance of total variance among pops.
galathea vs lachesis
Tunisia + Sicily vs rest of Europe
Tunisia vs Morocco
Tunisia vs Sicily
Sicily vs Italy
Italy vs S France (Condat)
Italy vs SW Alps (Col de Tende)
east Balkans + Central Europe vs SW Alps (Col de Tende)
Italy vs SW Alps vs west Balkans vs east Balkans + Central Europe
east Balkans + Romania vs Central Europe
Morocco vs continental Europe
The genetic diversities among these genetic lineages showed significant differences (Table 2). Thus, the Morocco group showed the highest values achieved for A, He as well as Ho, and the means for P95 and Ptot were above average. On the other extreme, Tunisia had the lowest means for A, He and Ho, and the mean for P95 was well below average; the genetic diversities of Tunisia were lower (A, He, Ho, Ptot) or equal than in the otherwise rather similar populations from Sicily. The four groups from mainland Europe all have mostly intermediate genetic diversities scatted around the respective mean values.
Species distribution modelling
According to the classification of Swets , we received 'excellent' AUC values in our 100 models (average training AUC = 0.927, average test AUC = 0.902). On average, the 'temperature annual range' had the highest explanatory power (30.3%), followed by the 'minimum temperature of the coldest month' (16.8%), the 'precipitation of the warmest quarter' (14.8%), the 'annual precipitation' (10.2%), the 'maximum temperature of the warmest month' (8.2%) and the 'precipitation of the driest quarter' (7.2%). All other variables contributed less than 5% each. The average minimum training presence was 0.05, and the lowest 10 percentile training omission threshold was 0.36.
The obtained allozyme data displayed in neighbour-joining phenograms, structure plots and hierarchical variance analyses indicate a profound genetic split between the two taxa, M. galathea and M. lachesis. Nazari et al.  supported this pattern by three lines of evidence: (i) differences of the male genitalia between M. lachesis and M. galathea, (ii) a stronger difference in wing patterns between these two taxa than between M. galathea population in Europe and the Maghreb and (iii) remarkable differences in DNA sequences of the nuclear wg gene between M. lachesis and M. galathea, but no major differentiation between M. galathea samples from Europe and the Maghreb. However, the sequences of the two mtDNA genes cox1 and 16S contradict the common pattern of allozymes, genital structures, wing patterns and nuclear DNA sequences: This marker is not well distinguishing M. galathea from Europe and M. lachesis, but shows remarkable differences between Europe and the Maghreb with this split being dated back to the Messinia Salinity Crises more than 5 My ago . Having in mind the differentiation pattern in all known marker systems, we believe that these two mtDNA lineages in the entire species complex might have originated at that time horizon, but were distributed to different geographical regions only much later by lineage sorting, maybe hereby exemplifying one case of the often observed difference between mtDNA on the one hand and nuclear DNA sequences, morphological characteristics and allozyme pattern on the other .
Our allozyme data further show strong differentiation within M. galathea into two major groups with respective subgroups: (i) Sicily - Tunisia with (i-a) Sicily and (i-b) Tunisia as well as (ii) all other M. galathea with (ii-a) Morocco, (ii-b) Italy with parts of southern France, (ii-c) western Balkan including the western Carpathian Basin, (ii-d) eastern Balkans with Romania and Central Europe, and (ii-e) the south-western Alps.
Atlantic-Mediterranean origin of the M. galathea/lachesisspecies complex
From the Maghreb to Europe
The deepest split in the M. galathea populations is between the Sicily - Tunisia group and all the other populations. As this split is about twice the genetic differentiation among their subgroups and less than half of the distance against M. lachesis, the onset of the Riss glaciation (about 310 ky BP)  might be the trigger for vicariance and thus the beginning of this differentiation. As (i) Iberia was continuously blocked for the expansion of M. galathea to Europe by M. lachesis [cf. 27] and (ii) all European M. galathea populations except Sicily are more similar to populations from Morocco than from Tunisia, a scenario with this split taking place in the Maghreb is little likely. This assumption is further supported by SDMs for ice age conditions predicting mostly continuous distributions over North Africa (Figure 3b) thus allowing vicariance in this region only during the relatively short interglacial stages. For these reasons, M. galathea must have reached Europe before the Riss glaciation.
As the region of the eastern Sahara in Egypt apparently always have been too dry for an expansion of M. galathea, this first expansion of M. galathea to Europe must have been from Tunisia to Sicily (Figure 4a), a sea strait known for biogeographical connections for many taxa [e.g. ; and references therein]. As the Strait of Sicily was considerably narrower during glacial periods due to eustatic sea level lowering, the transition from Mindel glaciation to Holstein interglacial with still low sea level but already higher temperatures might have been a suitable time period for this dispersal. After arrival to Sicily, the Holstein interglacial might have given suitable condition for the expansion of M. galathea over most parts of Europe, including the Balkans but excluding Iberia as this peninsula was already populated by M. lachesis (Figure 4a).
With the climatic cooling of the Riss ice age, which was considerably longer than the following Würm glaciation and had longer durations of minimum temperatures [33, 37], M. galathea most probably was nearly extinct in Europe only surviving in the southernmost possible retreats in Sicily and the southern Balkans (Peleponnesos), but also in the Maghreb; M. lachesis could survive in southern Iberia (Figure 4b). This vicariance might be the origin of the two major European lineages of M. galathea with the eastern one by chance evolving similarly in allele frequencies as the Morocco lineage, with this similarity therefore not representing recent biogeographical connection between them. Riss vicariance events most likely have also been responsible for other differentiation processes as e.g. in the Polyommatus coridon /hispana complex [e.g. ].
...and back to the Maghreb
As the time for differentiation between the four M. galathea lineages from continental Europe is assumed to be the result of one glacial cycle (see above) and as the differentiation between populations from Sicily and Tunisia are in the same order of magnitude, we assume that the onset of this differentiation is in the same time frame. As the genetic diversity is significantly higher in Sicily than in Tunisia and the warm and dry interglacial climatic conditions in Tunisia generally unsuitable for the survival of M. galathea, we assume that a colonisation most likely has taken place from Sicily to Tunisia. While the sea level was still considerably lowered at the transition from Riss to Eem thus facilitating dispersal between these two areas, this time period might be the most likely for this expansion event. During the following Eem interglacial, the Balkan refuge of M. galathea most probably could colonise most parts of Europe apart from Iberia and Sicily, which were occupied by other genetic lineages of this species complex (Figure 4b).
The existence of extra-Mediterranean refugia for thermophilic taxa
During the Würm ice age, which was not more severe than the two previous glaciations but with a shorter maximum , the Marbled White butterflies were not that much pushed to the South than in the previous cases. This is well matching the remarkable differentiation of the species in Europe allowing to distinguish five lineages (see above), which most likely are the result of survival of the Würm ice age in a larger number of different refugia.
This pattern implies at least two different refugia at the Balkan Peninsula at the western and the eastern flank; more in detail analyses also support a third Balkan centre in the peninsula's southern parts  (Figure 4c). This pattern of multiple refugia in the Balkans was already erected by Reinig  postulating different centres of survival in the western, southern and eastern Balkans and was later supported by genetic analyses showing genetic divergences between these areas for a variety of different animal species [e.g. [18, 40–42]].
Furthermore, different Würm refugia have to be postulated for Sicily and peninsular Italy, a pattern also repeated by other genetic analyses [e.g. [17, 43]]. Furthermore, other genetic studies show a remarkable genetic differentiation in the southernmost parts of peninsular Italy [e.g. [34, 44, 45]].
The last remaining lineage of M. galathea in the south-western Alps most likely is not representing a Mediterranean refuge of this species, but an extra-Mediterranean refuge area at the southern slopes of the glaciated Alps (Figure 4c). As already shown by Steward and Lister , glacial survival of temperate species in Europe was not only possible in the classical Mediterranean refugia sensu de Lattin , but also in small climatically buffered pockets in more northern regions [8, 48, 49]. Recent works especially highlight the southern and south-eastern parts of the Alps of particular importance for additional Würm ice age refugia for temperate species [e.g. [42, 50, 51]], and also for species formerly thought to be of exclusive Mediterranean origin [e.g. [52, 53]]. This apparently was also the case for the Marbled White.
During the Postglacial, several lineages of M. galathea were mostly blocked in their expansion by other lineages representing the respective leading edges [cf. 54]. In the case of M. galathea in Morocco, their northwards expansion was blocked by M. lachesis distributed in Iberia. The lineage surviving in the eastern Balkans apparently had the most important impact in the recolonisation of more northern parts of Europe as its dispersal was not hampered by any major mountain obstacle [cf. 9] so that this lineage could expand throughout Central Europe to the western parts of Germany (Figure 4c). However, the samples of north-eastern France and southern Germany show an intermediate genetic structure between this lineage and the south-western Alps lineage, making hybrid origin of these populations rather likely and thus expansion of the southern Alps lineage over the chains of the Alps.
Also the Italian lineage could expand beyond its refugium to southern France. Therefore the entire region of northern France and southern Germany might be a zone of mixing between these three lineages. Hybrid zones between different taxa are frequently observed in this region [e.g. [9, 55]]. Furthermore, the southernmost population in Calabria (southern Italy) has an intermediate genetic texture between the Italian and the Sicily group thus speaking for a postglacial contact and intermixing between these two groups in this region.
The hierarchical structure of our allozyme data set on M. galathea and M. lachesis is consistent with the chronology of the last four glacial-interglacial cycles. Based on this consistency, we derive the following scenario, which in our opinion is the most likely one: (i) The beginning of the Günz ice age might have affected the vicariance between the two species. (ii) M. galathea might have crossed from Tunisia to Sicily at the transition from Mindel ice age to Holstein interglacial and (iii) subsequently spread all over Europe, but retreated in the Maghreb to the higher elevations of the Atlas mountains. (iv) The members of this species complex survived the coldest periods of the Riss glaciation only in southern Iberia, Morocco, Sicily and the southern Balkans (Peleponnesos). (v) At the transition from Riss ice age to Eem interglacial, Tunisia was recolonised from Sicily. (vi) The southern Balkan group might have colonised major parts of Europe during the Eem interglacial including Italy and Central Europe. (vii) Populations of this group survived the Würm ice age in Italy, the southern margin of the Alps, the western and eastern flank of the Balkan peninsula; members of other lineages survived in Sicily, Tunisia, Morocco and Iberia. (viii) During the Postglacial, only the eastern Balkan and the Italian lineage showed major northwards range expansion. (ix) Hybridisation between lineages most probably occurred in western Central Europe and southern Calabria.
Alleles were labelled according to their relative mobility, starting with "1" for the slowest. All laboratory results were stored on cellulose acetate plates. These banding patterns were (re)analysed by one person (JCH). Allele frequencies, Nei's standard genetic distances  and parameters of genetic diversity (i.e. mean number of alleles per locus, A, expected heterozygosity, He, and observed heterozygosity, Ho, total percentage of polymorphic loci, Ptot, and percentage of polymorphic loci with the most common allele not exceeding 95%, P95) were computed with G-Stat . As sample sizes do not differ significantly, the calculation of allelic richness correcting for population sizes was not necessary. For detecting differences of means of genetic diversities among genetic lineages and sublineages, we calculated U-tests using STATISTICA. Conventional F statistics, AMOVAs, hierarchical genetic variance analysis, tests of Hardy-Weinberg equilibrium and linkage disequilibrium were calculated with ARLEQUIN 3.1 . Phenograms using the neighbour joining algorithm  were constructed with PHYLIP , including bootstrap-values (calculated based on 1,000 iterations). To define individual based genetic clusters we performed STRUCTURE analyses . As burn-in and simulation lengths we used 100,000 and 300,000 iterations per run based on the admixture model with correlated gene frequencies comparing different groupings (from K = 2 to K = 10).
Species Distribution Modelling
Over the last few decades, Geographic Information System (GIS) based Species Distribution Models (SDMs) have become vital tools used to predict the potential distribution of species under current conditions and climate change scenarios [62–64]. In combination with palaeoclimatological data, SDMs have been suggested as a mean of inferring species' past distributions [65, 66], especially when combined with phylogeographic techniques .
We compiled a set of 3,483 species records of M. galathea from online data bases (Global Biodiversity Information Facility - GBIF; http://www.gbif.org) and our own field surveys. The accuracy of all records was checked in DIVA-GIS 5.4  and only those which could be unambiguously assigned to a single grid cell with a resolution of 2.5 arc min (ca. 4 km in the study area) were used for further processing. Since unequal spatial clumping of species records may cause problems when computing SDMs, the species records were filtered in geographic space, leaving only 1 record per 10 arc min. The final data set comprised 535 records (Figure 3a) scattered all over the known range of the species in Europe and North Africa.
We obtained information on current and past climate as describedby the Community Climate System Model (CCSM; http://www.ccsm.ucar.edu) with a spatial resolution of 2.5 arc min from the Worldclim data base (; http://www.worldclim.org). Original palaeoclimatological data were previously processed as described by Peterson and Nyári (2007) . A total of 19 BIOCLIM variables were previously suggested as suitable for SDM computation [71, 72]. However, inclusion of too many inter-correlated variables or biologically irrelevant predictors may hamper the transferability of SDMs through space and time [73–76]. Therefore, we first computed a pair-wise correlation matrix based on Pearson's correlation coefficients among all 19 predictor variables and excluded those with R 2 > 0.75. Subsequently, we chose a final set of eleven predictors describing biologically relevant climate conditions for the long-term persistence of M. galathea populations (i.e. annual mean temperature, maximum temperature of warmest month, minimum temperature of coldest month, temperature annual range, mean temperature of wettest quarter, mean temperature of driest quarter, annual precipitation, precipitation of wettest quarter, precipitation of driest quarter, precipitation of warmest quarter, precipitation of coldest quarter).
For SDM computation, Maxent 3.3.2 was applied [77, 78] using the default program settings. Random background records were automatically sampled by Maxent within the study area. Species records were split 100 times into 70% used for model training and 30% for model evaluation via the area under the receiver operating characteristic curve (AUC; ). Subsequently, the average predictions for current and past conditions of the logistic output of the 100 models were computed and transformed into presence/absence maps applying the average minimum training presence and average 10% training omission as thresholds.
We acknowledge financial support by the German Academic Exchange Service (PostDoc Programme) and the Musée national d'histoire naturelle Luxembourg to JCH as well as from the Ministry of Education, Science, Youth and Culture of the Rhineland-Palatinate state of Germany to DR (project: 'Implications of global change for biological resources, law and standards'). We thank Claas Damken (Auckland, New Zealand) and Marc Meyer (Luxembourg) for field assistance. We thank the Fonds National de la Recherche Luxembourg for covering the publication fees.
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