Biological Journal of the Linnean Society, 2009, 98, 693–703. With 5 figures
Biogeographical connections between the Maghreb and
the Mediterranean peninsulas of southern Europe
JAN CHRISTIAN HABEL1,2*, PETRA DIEKER1,3 and THOMAS SCHMITT2
1
Musée National d’Histoire Naturelle Luxembourg, Section Zoologie des Invertébrés, L-2160
Luxembourg, Germany
2
University Trier, Department of Biogeography, D-54296 Trier, Germany
3
University Münster, Department of Community Ecology, D-48149 Münster, Germany
Received 28 January 2009; accepted for publication 4 May 2009
bij_1300
693..703
The glacial–interglacial cycles have caused severe range modifications of species’ distributions. In Europe,
thermophilic species had to retreat into geographically distinct southern refugia during glaciations. This process
produced strong genetic imprints, which are still detectable by the present pattern of genetic differentiation and
the distribution of regional diversity. To reveal the biogeographical imprints in the western Mediterranean, we
analysed 26 populations of the butterfly Maniola jurtina spread over large areas of its European and North African
distribution range. The samples were analysed using allozyme electrophoresis. We detected three genetic groups,
divided into Western Europe, Central/Eastern Europe, and Italy with the Maghreb. The North African samples
randomly cluster within the Italian samples. Even the population sampled in Morocco is genetically closely related
to these samples and not to the geographically neighbouring Iberian ones. Parameters of genetic diversity showed
similar values over the whole study area. The observed genetic pattern reflects possible glacial refugia in Europe
located in the Iberian Peninsula and the Balkans. For North Africa and Italy, our data reveal a colonization of
Africa originating from Italy. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society,
2009, 98, 693–703.
ADDITIONAL KEYWORDS: allozyme electrophoresis – butterflies – glacial refugia – Maniola jurtina –
stepping stone – Strait of Gibraltar – Strait of Sicily.
INTRODUCTION
The strong climatic oscillations of the Pleistocene
(Williams et al., 1998) repeatedly forced many species
to latitudinal and/or altitudinal range shifts (Reinig,
1938; De Lattin, 1967; Hewitt, 1996; Hewitt, 2004).
In Europe, temperate species survived the glacial
periods in distinct Mediterranean refugia where
populations often remained in isolation for many tens
of thousands of years (De Lattin, 1949). However,
because of the complex geography of the Mediterranean region, a multitude of different sub-centres with
independent evolutionary histories over at least the
last ice age have been postulated over several
decades; thus, De Lattin (1949) listed nine different
sub-centres scattered over this region. Being
*Corresponding author. E-mail: [email protected]
restricted to these centres during glaciations, many
species differentiated into distinct genetic groups,
with many cases studied by DNA and allozyme analyses and most published during the last decade
(Schmitt, 2007).
These studies strongly support the major importance of Iberian, Italian, and Balkan Peninsulas as
glacial retreat areas, differentiation centres, and
origins of postglacial northwards expansion (Hewitt,
2000). By contrast to these European peninsulas, the
importance of Northwest Africa (i.e. the Maghreb) is
still insufficiently understood (Hewitt, 2004; Schmitt,
2007). The classical biogeographical point of view
(De Lattin, 1949) merges Iberia and the coastal areas
of the Maghreb into one large continuous glacial
refuge area, the Atlantic–Mediterranean centre. This
hypothesis is supported by the distribution patterns
of many species (e.g. numerous Noctuid moths; Calle,
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 693–703
693
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J. C. HABEL ET AL.
1982) and distinguishes the more southern, warmer
and drier regions of the Maghreb as a separate evolutionary centre, the Mauretanian region. Peninsular
Italy was always classified as a distinct biogeographical unit, the Adriatic–Mediterranean region.
This biogeographical scenario has recently been
supported by some genetic analyses; thus, the genetic
structure of the turtle Mauremys leprosa demonstrates a strong genetic split between a northern and
a southern group in the Maghreb, but no significant
difference between the northern Maghreb populations
and those from Iberia (Fritz et al., 2006). However,
support for this scenario is provided by only a small
minority of such recent genetic studies (Schmitt,
2007). Many of them show a remarkable barrier at
the Strait of Gibraltar and, in many cases, an old
split between Iberia and the entire Maghreb seen
through endemic lineages in North Africa distinct
from the European lineages, as shown for amphibians
(Arntzen & García-París, 1995; Plötner, 1998; GarcíaParís & Jockusch, 1999; Steinfartz, Veith & Tautz,
2000; García-París et al., 2003; Carranza & Wade,
2004; Carranza et al., 2004; Fromhage, Vences &
Veith, 2004; Martínez-Solano et al., 2004; MartínezSolano, 2004; Veith et al., 2004), shrews (Cosson et al.,
2005), and scorpions (Gantenbein & Largiadèr, 2003).
Flying species such as bark beetles (Horn et al., 2006)
or salt water-tolerating animals such as reptiles
(Lenk et al., 1999; Álvarez et al., 2000; Paulo et al.,
2002; Carranza et al., 2004; Carranza, Arnold & Pleguezuelos, 2006; Fritz et al., 2006), but also the frog
Hyla meridionalis (Busack, 1986), are not greatly
hindered in their dispersal by this sea barrier, and
thus show mostly similar genetic lineages on both
sides. Genetic differentiation in the shrew Crocidura
russula supports the recent colonization of Europe
from north-western Africa, with Iberia being colonized by a western Maghreb lineage and Italy by an
eastern Maghreb group (Cosson et al., 2005). Indeed,
cases are known in which colonization from the
Maghreb to Europe only occurred via Italy, as in the
marbled white butterfly Melanargia galathea (Habel
et al., 2008).
These data support the great importance of the
Maghreb region as glacial refuge centre, at least
as important as the three European peninsulas.
However, all of these species analysed for the
Maghreb and adjoining regions are typical western
or holo-Mediterranean species, so that, although dispersal occurred from Northern Africa, only some
species spread far north (Joger et al., 2007). By contrast, the Iberian populations colonized the great
expanses of Europe in most cases (Hewitt, 1999).
Therefore, we question the importance of northwestern Africa for biogeographical groups with
supposed eastern Mediterranean and south-western
Asian core area. We selected the meadow brown
Maniola jurtina as our study organism because this
species belongs to a genus with a predominantly
eastern Mediterranean to Central Asian distribution
(Lukhtanov & Lukhtanov, 1994; Hesselbarth, van
Oorschot & Wagener, 1995; Korschunov & Gorbunov,
1995). A recent allozyme study of M. jurtina (Schmitt,
Röber & Seitz, 2005a) revealed two genetic lineages
in Europe: one in Iberia and western Europe and the
other one in Central and eastern Central Europe,
most probably of Pontic-Mediterranean origin. These
data are corroborated by older allozyme analyses, as
well as the wing pattern and morphology of the genitalia (Thomson, 1987). However, the biogeographical
status of the Maghreb and Italy remained mostly
unresolved. Therefore, we collected butterflies in the
Maghreb region and in Italy to complete the biogeographical picture of M. jurtina and to address the
question of the status of eastern Mediterranean elements in north-western Africa.
MATERIAL AND METHODS
STUDY SPECIES
Maniola jurtina (Linnaeus, 1758) is widely distributed in Southern and Central Europe. Its northern
distribution border reaches Central Scandinavia. In
North Africa, the distribution area of M. jurtina
reaches from the Atlas in Morocco to Tunisia (Tolman
& Lewington, 1997; Tarrier & Delacre, 2008). The
species occurs in grasslands in high densities.
ELECTROPHORESIS
We analysed a total of 924 individuals of M. jurtina
from 26 populations (Fig. 1). The populations from
Portugal, France, Germany, Hungary, Slovakia, and
Pesina (northern Italy) were reanalysed from
(Schmitt et al., 2005a). The species were sampled at
meadows in summer 1996–98, 2007, and 2008. The
individuals were netted in the field, frozen alive in
liquid nitrogen, and stored under these conditions
until analysis (Table 1).
Half of the abdomen of each individual was homogenized in Pgm-buffer by ultrasound and centrifuged
at 17 000 g for 5 min. For allozyme electrophoresis, we
used cellulose acetate plates applying standard protocols (Richardson, Baverstock & Adams, 1986; Hebert
& Beaton, 1993). We analysed a total of 16 allozyme
loci for both species applied the electrophoretic conditions for M. jurtina (Schmitt et al., 2005a): Idh1, Idh2,
Mdh1, Mdh2, G6pgdh, Pgi, Pgm, Pep, Got1, Got2,
Gpdh, Fum, Me, Apk, Hbdh, and Mpi.
STATISTICAL
ANALYSIS
Alleles were labelled according to their relative mobility, starting with ‘1’ for the slowest.
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 693–703
BIOGEOGRAPHY OF THE WESTERN MEDITERRANEAN
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Figure 1. Overview of all locations of the 26 sampling stations of Maniola jurtina. Numbers are as indicated in Table 1.
The southern distribution limit is given by a dotted line.
Table 1. Overview of all regions, sampling sites, numbers of individuals sampled, and date of sampling of Maniola
jurtina
Region
Population
Site
Coordinates
Samples
Date of sampling
Iberia
P – Barão de S. João
P – Palmela
P – Montemor-o-Velho
F – Carol
F – Maillat
F – Velars
D – Perl
D – Kirchheimbolanden
D – Hilbringen
D – Beckingen
D – Birgel
D – Blumberg
SLO – Podhradie
H – Csákvár
H – Pilis
H – Josvafö
I – Pesina
I – Verona
I – Rieti
I – Mormanno
I – St Giorgio-Calabria
I – Valledolmo
I – Francavilla di Sicilie
M – Azrou
T – Ain Traham
T – Jendouba
P1
P2
P3
F1
F2
F3
D1
D2
D3
D4
D5
D6
SK7
H8
H9
H10
I1
I2
I3
I4
I5
I6
I7
M1
T2
T3
37′10;
38′36;
38′50;
42′32;
46′08;
45′57;
49′28;
49′40;
49′27;
49′24;
50′20;
47′52;
47′46;
47′26;
47′40;
48′30;
45′35;
45,31;
37′58;
39′54;
38′17;
37′45;
37′53;
33′27;
36′48;
36′56;
42
34
41
24
35
33
45
36
45
45
45
40
28
30
28
21
42
40
40
40
30
40
30
26
24
40
2 May 1997
8 May 1997
21 June 1997
29 July 1997
8 July 1998
17 July 1997
12 July 1996
5 August 1998
6 August 1998
7 August 1998
14 July 1996
4 August 1997
11 August 1997
13 August 1997
14 August 1997
15 August 1997
26 July 1996
9 July 2007
26 June 2007
6 July 2007
7 July 2007
4 July 2007
5 July 2007
6 June 2008
30 June 2007
28 June 2007
Western Europe
Central/Eastern Europe
Italy
North Africa
8′45
8′58
9′18
1′47
5′35
5′58
6′23
8′1
6.38
6.42
6′37
8′34
17′32
10′30
18′56
20′35
10′46
10,55
14′20
15′58
15′59
13′53
15′7
5′12
8′41
8′48
P, Portugal; F, France; H, Hungary; SK, Slovakia; D, Germany; I, Italy; M, Morocco; T, Tunisia. For the geographic
locations, see Fig. 1.
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J. C. HABEL ET AL.
Allelic richness (AR) and mean number of alleles
(A) were calculated using FSTAT (Goudet, 1995).
Allelic richness was preferred over uncorrected allelic
diversity (mean number of alleles per locus) because
it takes into account the differences in sample
sizes among sample locations. Hierarchical genetic
variance analyses (analysis of molecular variance),
observed (Ho), expected (He) heterozygosities and tests
of Hardy–Weinberg equilibrium and linkage disequilibrium were calculated with ARLEQUIN, version 3.1
(Excoffier, Larval & Schneider, 2005). The percentages of polymorphic loci (Ptot) and polymorophic loci
with the most common allele not exceeding 95% (P95)
were calculated following the allele frequencies computed using FSTAT.
STRUCTURE software (Pritchard, 2000) was used
to infer the most probable number of genetic clusters
without a priori definition of populations. We used the
batch run function to carry out a total of 100 runs: ten
each for one to ten clusters (i.e. K = 1 to K = 10). The
repetitions were run to see if there were deviations
among the different runs for a fixed K and to calculate
means and standard deviations. For each run, the
burn-in and simulation length was 150 000 and
500 000, respectively.
A population phenogram using the Neighbourjoining algorithm (Saitou & Nei, 1987) based on pairwise Cavalli-Sforza & Edwards (1967) distances was
calculated with ARLEQUIN, version 3.1 (Excoffier
et al., 2005). The phenogram was constructed with
TREEMAKER. Node support was assessed by means
of 1000 bootstrap replicates.
RESULTS
All enzyme loci had banding patterns consistent with
known quaternary structures for both species and no
general linkage disequilibrium was observed for any
locus. Therefore, further analyses were performed
using standard algorithms in population genetics.
Thirteen of the analysed loci were polymorphic, but
three loci (Mdh1, Fum, and Apk) were monomorphic throughout. We calculated the following parameters of genetic diversity: mean number of alleles
(2.38 ± 0.32), allelic richness (1.76 ± 0.18), expected
and observed heterozygosity (18.67% ± 3.48, 15.46% ±
3.64, respectively), and the percentage of polymorphic
loci (total: 72.80% ± 12.74 and with the most common
allele not exceeding 95%: 45.89% ± 12.49). All values of
five parameters of genetic variability are given in
Table 2.
A population phenogram using the Neighbourjoining algorithm (Saitou & Nei, 1987) based on pairwise Cavalli-Sforza & Edwards (1967) distances (Fig. 2)
and a Bayesian structure analysis (Fig. 3) showed
three genetic groups: Western Europe, Central/
F1
P3
P1
P2
80
F3
I2
F2
75
83
D2
D6
D5
I1
Cavalli-Sforza &
Edwards (1967)
0.05
D1
D4
SK8
D3
H9 H7
H10
Figure 2. Neighbour-joining phenogram based on the
genetic distances (Cavalli-Sforza & Edwards, 1967) of all
populations of Maniola jurtina that were analysed. Codes
of samples are as indicated in Table 1 and Fig. 1.
Eastern Europe, and Italy with North Africa with both
analytical approaches. The highest probability value
was calculated for K = 3. Furthermore, the allele frequencies of the loci PepPhePro and G6pdh clearly distinguished these three groups: the samples from North
Africa and Italy (excluding the northern-most sample)
were nearly fixed for the allele B of PepPhePro, whereas all
other samples showed mostly equal percentages of the
alleles B and C (Fig. 4A). For G6pdh, the samples from
Central and Eastern Europe show mostly equal percentages of the alleles C and D, whereas allele C was
dominant in all other populations and allele B was
endemic to Italy, reaching considerable percentages in
some of the populations there (Fig. 4B).
Seventeen alleles of M. jurtina occurred exclusively
in one of the three lineages (one in the western group,
eight in Italy with north-west Africa, and eight in the
eastern group); separating Italy and Africa, we found
six endemic alleles in Italy, of which one is restricted
to Sicily, and only two in North Africa. No parameter
of genetic diversity deviated significantly among the
three geographic groups (Kruskal–Wallis analysis of
variance: all P > 0.05).
The total genetic variance among populations of
all M. jurtina populations was 0.1605 (FST: 10.6%,
P < 0.001), a variance of 0.1259 was found among
individuals within populations (FIS: 9.27, P < 0.001)
and 1.2323 within individuals. A hierarchical variance analysis located 56.4% of the variance among
populations among the three distinguished genetic
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BIOGEOGRAPHY OF THE WESTERN MEDITERRANEAN
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Table 2. Six parameters of genetic diversity of Maniola jurtina: mean number alleles per locus (A), allelic richness (AR)
percentage of expected heterozygosity (He), observed heterozygosity (Ho), percentage of loci with the most commonest
allele not exceeding 95% (P95), and total percentage of polymorphic loci (Ptot)
Region
Site
A
AR
He (%)
Ho (%)
Ptot (%)
P95 (%)
Western Europe
P1
P2
P3
F1
F2
F3
2.56
2.13
2.81
2.44
2.94
2.19
2.51
2.56
2.19
2.75
2.56
2.75
2.38
2.50
2.00
2.00
2.06
2.69
2.40
2.63
2.13
2.00
2.75
2.00
1.94
2.24
2.63
1.88
2.63
2.38
2.29
1.78
1.68
1.85
1.92
2.06
1.81
1.85
1.87
1.73
1.95
1.82
1.87
1.70
1.73
1.54
1.61
1.46
1.79
1.73
2.16
1.71
1.57
1.93
1.54
1.46
1.73
2.01
1.53
1.81
1.78
1.75
17.9
15.5
18.3
21.1
20.6
20.9
19.1
22.4
20.8
23.0
20.6
21.6
19.1
20.4
14.8
17.3
22.7
19.5
20.2
23.7
15.8
15.2
19.6
12.3
10.7
16.2
21.7
13.4
16.7
17.2
16.6
13.8
13.4
15.0
18.3
16.8
16.3
15.1
20.2
17.3
22.2
16.8
18.4
19.5
17.5
13.4
14.0
19.9
16.3
17.8
18.7
12.8
11.5
18.0
8.3
9.2
13.1
13.1
9.7
11.5
11.4
12.5
68.7
68.7
87.5
81.2
93.7
81.2
80.2
81.2
68.7
87.5
68.7
87.5
87.5
75.0
62.5
68.7
68.7
81.2
76.1
56.2
50.0
68.7
87.5
50.0
50.0
60.4
68.7
62.5
81.2
70.8
63.9
50.0
37.5
56.2
50.0
75.0
62.5
55.2
50.0
50.0
56.2
56.2
50.0
50.0
37.5
37.5
43.7
56.2
50.0
48.8
18.7
37.5
31.2
50.0
31.2
25.0
32.3
56.2
31.2
43.7
43.7
36.1
Mean (±SD)
Central/Eastern
Europe
Mean (±SD)
Italy
Mean (±SD)
North Africa
Mean (±SD)
Mean North
Africa + Italy
Mean (±SD)
D1
D2
D3
D4
D5
D6
SK7
H8
H9
H10
I1
I2
I3
I4
I5
I6
I7
M1
T2
T3
(±0.33)
(±0.30)
(±0.35)
(±0.43)
(±0.36)
(±0.13)
(±0.15)
(±0.27)
(±0.24)
(±0.25)
(±2.19)
(±2.5)
(±4.8)
(±4.2)
(±4.4)
(±1.50)
(±2.6)
(4.4)
(±1.7)
(±3.7)
(±10.01)
(±9.2)
(±15.1)
(±9.5)
(±13.9)
(±12.76)
(±6.7)
(±10.8)
(±12.5)
(±12.0)
All abbreviations of populations are as indicated in Table 1. The population from Pesina (Italian pre-Alps) was included
in the Central/Eastern European group and not in the Italian one as it genetically clearly belongs into this first lineage.
Figure 3. Structure plot of all populations of Maniola jurtina analysed over Europe and North Africa (NA). Population
codes are as indicated in Table 1.
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J. C. HABEL ET AL.
A
B
Figure 4. Distribution of allele frequencies analysed for the loci PepPhePro (A: grey, allele B; white, allele C; dark grey, all
other alleles) and for G6pdh (B: dark grey, allele B; white, allele C; black, allele D; light grey, all other alleles).
groups (FCT: 7.39%; FSC: 5.72, P < 0.001). The genetic
differentiation among the populations of the western
lineage (FST: 0.51%) and among the Northwest
African populations (FST: 2.13%, P < 0.001) was low
compared to the respective differentiation levels
within Italy (FST: 11.1%) and the eastern lineage
(FST: 9.33%, P < 0.001). The genetic differentiation
between Northwest African and all European M.
jurtina samples is relatively weak (0.0576; FCT:
3.68%, P < 0.01) because most of the variance is
located within these groups (0.3676, FSC: 9.97%,
P < 0.001); we detected low differentiation among
Italy with Sicily and the populations located on the
opposite coastline in North Africa (0.0349; FCT:
2.75%, P < 0.01) (Tables 3, 4).
DISCUSSION
GENETIC
DIVERSITY AND DIFFERENTIATION
The mean genetic diversity of M. jurtina populations
over large parts of the species’ European and North
African distribution is high compared to other species
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 693–703
BIOGEOGRAPHY OF THE WESTERN MEDITERRANEAN
699
Figure 5. Hypothetical postglacial recolonization pathways of Maniola jurtina. Hatched areas, hypothesized ice age
refugia; arrows, postulated postglacial range expansions.
Table 3. Nonhierarchical variance analyses of several Maniola jurtina groupings in Europe and North Africa
Groupings
FST (%)
FIS (%)
Within
individuals
All populations
Western lineage
Eastern lineage
Central lineage
Italy with Sicily
Northwest Africa
Southern Italy and Tunisia†
10.57** (0.1605)
0.51 (0.0071)
9.33** (0.1459)
9.40** (0.1299)
11.11** (0.1588)
2.13 (0.0268)
10.45 (0.1486)
9.27** (0.1259)
10.79** (0.1493)
3.61* (0.0511)
15.94** (0.2006)
12.77** (0.1621)
25.40** (0.3133)
14.48 (0.1844)
(1.2323)
(1.2339)
(1.3660)
(1.0576)
(1.1086)
(0.9201)
(1.0890)
The respective FST and FIS values are accompanied by their referring variance components (in parenthesis). *P ⱕ 0.05,
**P ⱕ 0.01.
†For sampling sites, see Fig. 1B.
Table 4. Hierarchical variance analyses of several Maniola jurtina groupings around the Strait of Sicily
Groupings
Among groups
FCT (%)
Among populations
within groups FSC (%)
Three lineages
Europe versus North Africa
Italy versus Sicily
Sicily versus Tunisia
Italy versus Sicily versus Tunisia
Italy/Sicily versus Tunisia
7.39**
3.68**
n.s.
0.28**
2.75**
2.33**
5.72** (0.0824)
9.97** (0.3676)
16.63** (0.2345)
11.35** (0.1333)
9.80** (0.1297)
10.12** (0.1392)
(0.1151)
(0.0576)
(0.0033)
(0.0349)
(0.0321)
The respective FCT and FSC values are accompanied by their referring variance components (in parenthesis). *P ⱕ 0.05,
**P ⱕ 0.01.
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J. C. HABEL ET AL.
of the subfamily of Satyrinae (Porter & Geiger, 1988;
Porter & Shapiro, 1989; Schmitt & Seitz, 2001; Wood &
Pullin, 2002; Habel, Schmitt & Müller, 2005; Schmitt
et al., 2006a; Besold, Huck & Schmitt, 2008a; Besold
et al. 2008b; Habel et al., 2008). This observed level of
genetic diversity is characteristic for a rather widespread and common butterfly species. The genetic
diversity of the populations is fairly evenly distributed
over the whole study area and does not show genetic
impoverishments, neither along geographic clines, nor
among regional groups, as also demonstrated for other
generalistic butterfly species (Schmitt, Gießl & Seitz,
2003; Habel et al., 2005). The observed pattern of
genetic differentiation into strongly divergent lineages
shows the imprints of the last glaciation and suggests
long-lasting differentiation processes in allopatry in
different refugia, as has been observed for other butterflies with quite similar genetic structures (Habel
et al., 2005; Schmitt, Varga & Seitz, 2005b; Schmitt,
Hewitt & Müller, 2006b; Besold et al., 2008b; Schmitt
& Haubrich, 2008).
THREE GENETIC LINEAGES AND THREE RESPECTIVE
MEDITERRANEAN GLACIAL REFUGE AREAS FOR
M. JURTINA
The populations analysed represent three genetic
groups: (1) a western group including all populations
from Iberia and France; (2) an eastern one composed of
the samples from Germany, Slovakia and Hungary, but
including also the northern-most population from
Italy; and (3) a central group including all other
samples from Italy and the Maghreb. Two other allozyme studies on M. jurtina (Thomson, 1987; Schmitt
et al., 2005a) did not detect this third central group.
However, Schmitt et al. (2005a), applying a similar set
of allozyme loci, did not analyse samples from this area
and Thomson (1987) did not score the locus peptidase
(PhePro), which is essential for the discrimination of
this central lineage from the other two. Morphological
characters also failed to separate this Italian–Maghreb
group from the others (Thomson, 1987).
The biogeographic pattern obtained is in accordance with postglacial northwards expansions from
the Mediterranean refuge centres, Iberia in the west
and the Balkans in the east. The third group from a
refugium in Italy and/or the Maghreb (see below) did
not expand to areas beyond the Alps. Comparing this
pattern with the four paradigms of postglacial terrestrial range expansions in Europe (Hewitt, 1999;
Habel et al., 2005) reveals a strong concordance with
the bear paradigm with expansion from the Iberian
and Balkan areas, but not from Italy as a result of the
barrier of the Alps (note that Ursus arctos in its
eastern lineage is not following the bear paradigm;
Taberlet & Bouvet, 1994).
OUT
OF
EUROPE
Whether (1) the Maghreb and Italy represent one
continuous refugial and differentiation centre for M.
jurtina or (2) the species survived the last ice age only
in Italy later colonizing north-western Africa or (3)
vice versa is still debatable. However, four aspects of
our data and the biogeography of M. jurtina allow
discussion of the origin of this lineage.
First, the detected genetic differentiation in Italy is
much higher than in North Africa with populations
sampled from Morocco to Tunisia. Similarly strong
genetic differentiation was obtained in Italy for other
species for which glacial refugia in the Apennine
Peninsula were postulated, often with the assumption
of allopatric subrefugia as a result of the geomorphological complexity of the mountain chains of
southern Italy (Di Giovanni et al., 1998; Nagy et al.,
2002; Canestrelli, Cimmurata & Nascetti, 2007a;
Canestrelli, Verardi & Nascetti, 2007b). The great
genetic uniformity of the M. jurtina populations
throughout the species’ entire African distribution
from Morocco to Tunisia supports a recent (i.e. postor late Würm glacial) fast phalanx-like colonization of
this entire area; identical patterns were also observed
for some other species (Filippucci, 1992).
Second, the number of alleles endemic to Italy
(N = 6) is considerably higher than for the Maghreb
(N = 2), thus supporting Italian origin of African
M. jurtina.
Third, Italy is almost completely populated by the
central lineage, which reaches the southern edge of
the Alps where it meets the eastern lineage of Balkan
origin. This contradicts a Maghreb origin of M.
jurtina. Organisms having their refugia in the
Maghreb would have started their colonization of
Italy via Sicily in its extreme south, with an other
colonization from the north (e.g. from the Balkan
refuge area via Dalmatia and Istria) forming a secondary contact zone in central Italy, as in the case of
the bark beetle Tomicus destruens (Horn et al., 2006)
and not in the northern Italian pre-Alps, as in the
case of M. jurtina.
Fourth, the evolutionary centre of the genus
Maniola is located in the eastern Mediterranean,
western and Central Asia with numerous species
(e.g. in the western Tien-Shan and the Hindukush;
Thomson, 1987; Lukhtanov & Lukhtanov, 1994;
Hesselbarth et al., 1995; Korschunov & Gorbunov,
1995). When expanding westwards, M. jurtina most
likely first reached Italy before colonizing the
Maghreb, thus making absence of M. jurtina from
Italy during the last ice age an unlikely scenario.
When comparing M. jurtina with the chorologically
similar butterfly M. galathea, the latter species
most probably has colonized Italy form the
© 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98, 693–703
BIOGEOGRAPHY OF THE WESTERN MEDITERRANEAN
Maghreb, but, in contrast to M. jurtina, this species
belongs into a genus with a western Mediterranean
core area (Varga, 1977; Tolman & Lewington, 1997;
Tarrier & Delacre, 2008).
Considering such evidence makes an early postglacial or late Würm colonization of the Maghreb from
Italy a more likely scenario than the reverse colonization, or a long-lasting persistence in both of these
regions.
STRONG
GENETIC COHESIVENESS BETWEEN
AND THE
ITALY
MAGHREB
Sea straits are barriers for species, which restrict
exchanges of individuals and thus gene flow, and the
width of such a strait is often used as a predictor for
its isolating power. Therefore, the Strait of Gibraltar
should act much less as a biogeographical barrier
than the Strait of Sicily. Consequently, the biogeographical connectivity over the Strait of Gibraltar is
supported by genetic analyses (Cosson et al., 2005),
but more studies emphasize the biogeographical split
between the Maghreb and Iberia (Beerli, Hotz &
Uzzell, 1996; De Jong, 1998; Castella et al., 2000;
Palmer & Cambefort, 2000; Harris & Sá-Sousa, 2002;
Gantenbein & Largiadèr, 2003); this is also underlined in many Mediterranean species only occurring
on one side of this sea strait, as, for example, in
lepidopterans (only Iberia: Leptidea sinapis, Satyrium
spini, Polyommatus bellargus, Melitaea parthenoides,
Hipparchia semele, Aulocera circe; only Maghreb:
Tomares mauretanicus, Taurucus rosaceus, Polyommatus punctifera, Hipparchia hansii, Coenonympha
arcanioides, Thymelicus hamza; Tolman & Lewington, 1997, García-Barros et al., 2004; Tarrier &
Delacre, 2008).
For the much broader Strait of Sicily (approximately 140 km), one would therefore expect a rather
stronger isolation. Nevertheless, this strait has not
hindered the dispersal of M. jurtina, and, even more,
has not produced any genetic bottleneck in this
species. Other genetic studies on a flying and a nonflying mammal species also showed similar genetic
patterns (Cosson et al., 2005; Stöck et al. 2008).
This apparently paradoxical situation might be best
explained by the lowering of the sea level by approximately 120 m during the ice ages (Thiede, 1978;
Giraudi, 2004). This lowering resulted in some reduction of the width of the Strait of Gibraltar, but dramatically reduced the distance between Tunisia and
Sicily to approximately 40 km, with the island of
Panteleria representing an additional stepping stone.
Consequently, this sea strait would not have acted as
an important biogeographical barrier during ice age
maxima, neither for our studied butterfly, but also not
for many other species.
701
ACKNOWLEDGEMENTS
We acknowledge a grant from the National Fonds
for Research Luxembourg (FNR) (grant number
FNR/08/AM2c/31) and financial support from the
Natural History Museum Luxembourg and the Förderpreis provided by Boehringer Ingelheim Pharma
GmbH (Ingelheim, Germany). We thank Norbert Zahm
(Schmelz/Hüttersdorf, Germany) for valuable information about suitable sample sites and Claas Damken
(Auckland, New Zealand) and Martin Husemann
(Osnabrück, Germany) for field assistance.
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