Nieto Feliner • Southern European glacial refugia
TAXON 60 (2) • April 2011: 365–372
Southern European glacial refugia: A tale of tales
Gonzalo Nieto Feliner
Real Jardín Botánico (CSIC), Plaza de Murillo, 28014 Madrid, Spain; [email protected]
Abstract Interpretations of current diversity patterns based on the contraction/expansion model forced by climatic oscillations
during the last two million years are commonplace in phylogeographic literature. Of the wealth of scientific studies accumulated
during the past two decades in Europe, the ones we understand best are those mostly from higher latitudes, probably because
patterns were simplified to a great extent by major losses of diversity during glacial periods. In Southern European regions
(or in general, in those places where ice effects were less severe) the situation is quite different and to some extent opposite.
These regions are referred to as refugia because they are known to contain more genetic diversity than elsewhere. This is not
only due to preservation of genotypes that went extinct in other places, however, but also to the intensity and accumulation of
a number of processes in a patchy landscape across a varied topography. A lack of general phylogeographic patterns in these
regions is one consequence. Speaking of a single refugium to refer to each of the peninsulas, however, is an oversimplification. Even speaking of multiple unconnected refugia does not adequately reflect the complexity of the processes that shaped
the current genetic and specific diversity.
Keywords biodiversity; glacial refugia; hybrid zones; phylogeography; Southern Europe
INTRODUCTION
The term Biosystematics has been used for a wide range
of investigations aiming to understand living diversity and its
arrangement in classification (Nieto Feliner & Álvarez, 2001).
One of these emphases has been on evolutionary processes
(Stace, 1980). The main connection between Phylogeography
and Biosystematics is that well-sampled and well-analysed
phylogenies provide support and consistency to Systematics
at a relatively deep macro-evolutionary level, whereas wellsampled and well-analysed phylogeographies allow clarification of shallow systematics, especially species delimitation
and subdivision.
In 2002 an international meeting was held in Vairao (Portugal) on Phylogeography in Southern European Refugia,
and part of the papers presented there were published in a
special volume years later (Weiss & Ferrand, 2007). It was a
seminal meeting for calling attention to scarce information
available on patterns and dynamics associated with so-called
refugia in southern European peninsulas. In addition, the
meeting stimulated considerable research on ways in which
Pleistocene glaciations had affected the biota in higher and
lower European latitudes.
This paper is based on a talk that had similar aims to
those of the Vairao Meeting but was delivered in 2008 during
a meeting organized by IOPB in the Tatry Mountains, Slovakia.
Improvement in understanding patterns and processes within
southern European refugia has been due to at least two factors:
(1) a number of phylogeographic studies have concentrated, or
intensified their sampling, on southern European areas; (2) important conceptual issues have been explicitly addressed such
as the inapplicability of the simple scheme “one peninsula–one
refugium”, prevalent in the 1990s and early 2000s (e.g., Gómez
& Lunt, 2007). A number of misconceptions regarding southern
European glacial refugia are still seen in the literature, probably
caused by prevalence of models and views developed for areas
with markedly different climatic histories, such as in central
and northern Europe.
The purpose of this paper is to discuss some views and
arguments to stimulate further research on processes in less
severely glaciated areas in Europe (southern European peninsulas). This is done partly by using results from our research
group that has focused on the western Mediterranean. It is
not intended to be a thorough review but rather a series of
perspectives.
PARADIGM POSTGLACIAL COLONIZATION
PATTERNS AND HYBRID ZONES
The influence of Pleistocene climatic oscillations on phylogeographic patterns, and more generally on current distributions of genetic and species diversity, has long been realized
(Heusser, 1955; Haffer, 1982; Hewitt, 2000). When interpreting
current patterns of genetic diversity of plant and animal groups
in any part of Europe, it is difficult to neglect the potential impact of climatic oscillations during the past two million years.
The inferred contraction/expansion model that has resulted
from such oscillations has indeed a strong explanatory power
for current distributions of species and genetic variation. The
phylogeographic literature, starting two decades ago (Avise &
al., 1987; Avise, 2000), has grown rapidly (Avise, 2009), resulting in an augmentation of interest on effects of glacial cycles
and species distributions and evolution.
Phylogeographic investigations over these years have
mostly focused on recolonization patterns from areas where
species survived during cold periods (Taberlet & al., 1998; Petit
& al., 2003; Hewitt, 2004). Some of the conclusions reached by
those studies include identification of more or less unexpected
locations for refugia on the basis of their latitude, e.g., nunataks
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Nieto Feliner • Southern European glacial refugia
(Abbott & al., 2000; Anderson & al., 2006), or confirmation
of previously hypothesized refugia, e.g., in the Alps (Tribsch
& Schönswetter, 2003; Schönswetter & al., 2005). Another
finding has been that events shaping current diversity may be
fairly recent, and therefore postglacial migrations may explain
current patterns (e.g., in the North Atlantic Ocean, without
need to invoke either glacial survival in situ or tabula rasa
hypotheses; Brochmann & al., 2003). Underlying most biogeographic and phylogeographic European literature, however, is
the traditionally recognized idea that a significant part of the
glaciated areas in the continent were recolonized from southern
peninsulas, or at least that a significant portion of diversity lost
in higher latitudes was conserved in those peninsulas. Three
broad schemes have been proposed, what Hewitt (2001) calls
paradigm postglacial colonization patterns. These schemes
differ on how the refugial areas in Southern Europe (i.e., the
Balkans, Iberia and Italy) contributed to the repopulation of
central and northern parts of Europe after the ice retreat. Either
current northern areas are the result of postglacial expansion
primarily from a Balkan refugium, as in the case for the grasshopper Chorthippus parallelus, or are the result of expansion
from three main refugia in the three peninsulas, as is the case
with the hedgehog (Hewitt, 1999). The third pattern refers to
a scheme whereby distinct western and eastern lineages are
distinguished, suggesting recolonization from both an Iberian
and a Balkan refugium, as with the brown bear (Taberlet &
Bouvet, 1994).
These paradigm postglacial colonization patterns have
been challenged by studies of groups that are currently well
represented in southern peninsulas. One of the criticisms
stems from the unlikelihood that southern European peninsulas, particularly Iberia and the Balkans, offered a continuous and homogeneous refugial area that would justify
considering them as single glacial refugia. The topic was
reviewed in Gómez & Lunt (2007), who provided examples
from fish, amphibian, reptile, invertebrate and plant species,
supporting that those peninsulas contain genetically diverse
groups of populations. They propose, therefore, that instead
of single refugia we should speak of “refugia within refugia”.
There have been numerous other studies identifying several
glacial refugia within each of the southern European peninsulas. In Iberia, although the traditional recognition of a
southeastern Spanish biodiversity hotspot has been associated
with the concentration of refugia for many species there, pal­
ynological and phylogeographic studies have found evidence
of possible refugia in various other regions (Carrión & al.,
2003). Research in oaks, for example, both evergreen (López
de Heredia & al., 2007) and white (Olalde & al., 2002), has
identified potential refugia in north, south, east, west and central Iberia. Examples are not restricted to tree species, which
have the advantage of usually providing complementary pollen data, but to organisms with short generation times such
as Arabidopsis (Picó & al., 2008). The finding of multiple
refugia within Iberia is consistent with results from animal
groups as well (Vila & al., 2005; Spooner & Ritchie, 2006).
A similar situation of multiple refugia has also been inferred
in Southern Australia (Byrne, 2008), where effects of climatic
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TAXON 60 (2) • April 2011: 365–372
oscillations might have been of similar magnitude to those
in Southern Europe.
It is symptomatic that a reinterpretation of the peninsular single-refugium scheme has been also made in one of the
classic examples of the three paradigm postglacial colonization patterns, namely, the case of the grasshopper Chorthippus parallelus (Hewitt, 1993). This long-term case study has
substantially contributed to the conceptual development of
the hybrid zone theory (Barton & Hewitt, 1985). Subspecies
parallelus is widely distributed throughout Europe and has
been known to hybridize with the Iberian subsp. erythropus
in the Pyrenees, where they form a stable hybrid zone. Subsequent studies in this grasshopper system, however, have found
further genetic differentiation within the Iberian subsp. erythropus with the identification of an X-chromosome variant in
central and southern Spain. This is indicative of an additional
refugium within Iberia or, more likely, of a more complex
picture (Bella & al., 2007). The scheme depicting populations of subsp. parallelus from Italian, Balkan and Caucasian
refugia meeting Iberian populations at the Pyrenees to form
a hybrid zone as a consequence of the contraction-expansion
cycles is not challenged. What is open to question is the assumption that Iberian subsp. erythropus originated in a single, largely homogeneous refugium in the Iberian Peninsula
(Bella & al., 2007). The original attribution of the classical
Pyrenean grasshopper hybrid zone to a tension zone model
(Virdee & Hewitt, 1994), whereby hybrids are assumed to be
intrinsically unfit and maintenance of the hybrid zone relies
on a balance between dispersal and selection against hybrids
(Barton & Hewitt, 1985), is also questionable. Unlike other
models (Arnold, 1997), in the tension zone model, positive or
negative interaction between hybrid genotypes and environment does not play a role in maintenance of the hybrid zone.
Yet, a recent discovery of differential infection patterns in the
grasshoppers across the hybrid zone by the endosymbiont Wolbachia suggests that these bacteria may play a role in hybrid
zone structure and dynamics (Zabal-Aguirre & al., 2010); this
would also challenge the tension zone model.
Hybrid zones have been considered as natural laboratories to study evolutionary processes (Harrison, 1990; Barton
& Hewitt, 1985). The concept of hybrid zones has been useful
for the paradigm postglacial colonization patterns because
the former are in theory complementary to the main refugia.
The southern European refugia “produced subdivisions of
species into a patchwork of genomes, often delimited with
sharp hybrid zones” (Hewitt, 2004). In other words, when climatic cycles forced migration and contact between genomes
differentiated previously in allopatry, hybrid zones protected
those genomes from merging and only allowed permeability of some genes and traits (Hewitt, 1993, 1996). This idea,
which was postulated already by Anderson (1949), is even
more consistent if the suture zone concept is accepted, that
is, hybrid zones for different groups of organisms clustering in the same locations (Remington, 1968); this concept,
however, has been criticised in North America (Swenson &
Howard, 2004). Hybrid zones, therefore, somehow frame the
refugial paradigms.
TAXON 60 (2) • April 2011: 365–372
Isolation and differentiation within refugia, however,
has not always been followed by expansion and formation of
hybrid zones. Hybrid zones, especially those that cluster to
form suture zones, are typically the consequence of contact
between genomes that suffered geographical displacement
after periods of allopatry. This situation occurred primarily in widely glaciated areas such as in northern and central
Europe. In contrast, southern European peninsulas offered
a great number of suitable areas within a much more limited space for organisms to survive during critical periods.
In these conditions, organisms were not forced to react to
climatic changes with large latitudinal shifts. As stated by
Hewitt (2001), genomes in Southern Europe (and southeastern
U.S.A.) survived and diverged without large geographical
displacement, because the varied topography allowed altitudinal shifts in range during climatic changes. For example, a
geographical barrier as the Pyrenees likely concentrated and
stopped the southward expansion of organisms after large
latitudinal shifts, which in some groups resulted in contact
with Iberian congeners and hybrid zones. In contrast, in the
Betic (Andalusian) mountains, organisms only needed short
altitudinal shifts across the intense orography—upwards
or downwards—to find suitable niches following climatic
changes. In southern peninsulas, although older lineages were
preserved from interspecific hybridization after differentiation and effective reproductive isolation, a common outcome
of altitudinal displacements was secondary contact and hybridization between species, and this presumably took place
in spatially less defined and less stable locations as compared
to major hybrid/suture zones (Comes & Kadereit, 1998; Albaladejo & al., 2005; Marhold & Lihová, 2006). Thus, the
patchy nature of the landscape in mountainous areas across
southern European peninsulas allowed partial differentiation in allopatry but subsequent easy contact with previously
differentiated genomes from close locations. It follows from
this that neither a single refugium for each of the peninsulas
nor simply multiple unconnected refugia within them seem
to adequately represent evolutionary histories within Iberia,
Italy or the Balkans. Another consequence is that the hybrid
zone concept associated with climatically-driven migrations
is one that is suitable for higher latitudes in Europe (Hewitt,
1999), but it is not so useful to uncover evolutionary history
of organisms in highly compartmentalized Southern regions.
In sum, my opinion is that the paradigm postglacial colonization patterns, although useful as general patterns at the
continental scale, do not tell much about evolutionary patterns
and processes that took place within the southern European
peninsulas.
ABOUT THE CONCEPT OF GLACIAL
REFUGIA
The concept of glacial refugia has traditionally been covered with a veil of mystery. It is suggestive of sanctuary, that
is, a place where biological diversity has been preserved from
Nieto Feliner • Southern European glacial refugia
extinction. Also, it is usually the case that refugia for specific
groups are only imprecisely known, so that they have yet to
be found or discovered. Despite this veil, they have a highly
applied interest in conservation policies since an area that
has facilitated long-term survival of species and populations
throughout several climatic oscillations seems to be a good
choice to be designated as a protected area in the long-term
(Tzedakis, 2004). Altogether, searching for glacial refugia is
somehow like looking for the holy grail of evolution from the
last three million years.
But, is there an agreement on what a glacial refugium
is and how to identify it? The basic idea would be that it is
a reservoir of old diversity (genetic and specific) preserved
through Pleistocene glacial periods. Médail & Diadema (2009)
have given a more specific definition: “an area where distinct
genetic lineages have persisted through a series of Tertiary or
Quaternary climate fluctuations owing to special, buffering
environmental characteristics”. However, the concept seems
to have been used for many purposes (Bennet & Provan, 2008)
and this has led to some confusion. Some of it is related to
scale and to the inappropriateness of applying the term refugium to places as complex and rich as the whole Iberian,
Italian or Balkan peninsulas, i.e., the refugia-within-refugia
theme (Gómez & Lunt, 2007). But there are other sources of
confusion. It is not always realized that species have different
environmental requirements. It is not appropriate, therefore,
to assume that “favourable” and “adverse” periods across
the Quaternary climatic oscillations were coincident for all
species, and that suitable refugia were universal (Bennet &
Provan, 2008; Médail & Diadema, 2009). In other words, not
all plants were escaping from cold temperatures. For instance,
in Africa, the so-called Rand Flora accounts for a pattern
that arose as a consequence of glacial-induced aridification,
which forced some plant species to mesic or less arid refugia
at continental margins (Thiv & al., 2010; I. Sanmartín, unpub.). Other concepts, such as cryptic refugia (Birks & Willis,
2008), revolve around the difficulty of predicting location of
refugial areas based exclusively on latitude and elevation. To
restrict the standard concept, Médail & Diadema (2009) propose three types of refugia in the Mediterranean basin based
on geographical and environmental characteristics. These
include: moist mid-altitude refugia, less arid than grasslands,
and less cold than high altitudes or latitudes; deep gorges or
closed valleys with continuous moisture; and low-altitude
areas. To avoid ambiguity of the refugial concept, Provan
& Bennet (2008) suggest focusing on distribution and abundance through time. Terms such as palaeorefugia (Tertiary)
and neorefugia (Quaternary) (Nekola, 1999) seem to be too
simplistic as well.
In accordance with lack of agreement regarding concepts
of refugia, there are also different approaches to identifying
them. Traditional ideas on plant refugia have been based on pollen data (Bennet & al., 1991), but phylogeographic approaches
have provided useful complementary information, particularly
in trees (Taberlet & al., 1998; Heuertz & al., 2004). In fact,
phylogeographic patterns in tree species may conform better
to Hewitt’s paradigm postglacial colonization patterns than
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Nieto Feliner • Southern European glacial refugia
in herbs (Petit & al., 2002). Other recent attempts to locate
refugia have been made by combining phylogeography with
other approaches, such as ecological niche modelling or palaeoclimatic reconstructions (Richards & al., 2007; Waltari & al.,
2007). Médail & Diadema (2009) have pointed out difficulties
of applying these combined approaches to the Mediterranean
area due to insufficient information, e.g., palaeoclimatic reconstructions due to environmental heterogeneity and ultimately
biogeographical complexity. It is worth considering, therefore,
the relevance of searching for glacial refugia within southern
European peninsulas (see below).
CLIMATIC OSCILLATIONS IN SOUTHERN
EUROPEAN PENINSULAS
As stated by Hewitt (2001), unravelling the genetic history of genomes in southern peninsulas is more complex than
in northern regions. This has hampered attempts to develop
models accounting for the effects of climatic oscillations on
the evolutionary history of organisms in these areas. Hampe
& Petit (2005) stated that “no theoretical or modelling exercise
has so far explicitly explored the behaviour of rear edge populations”. The most explicit model involving southern European
peninsulas proposes the sequential involvement of haplotypes
preserved in southern refugia in the recolonization of northern
glaciated areas following the leading edge model (although not
excluding episodic long-distance dispersal events; Nichols &
Hewitt, 1994; Hewitt, 1996). Hewitt’s model, however, was
mainly developed to explain the process of recolonization of
glaciated areas in higher latitudes and not to account for dynamics in lower latitudes. It illustrates, therefore, the significant
gap in knowledge concerning contraction-expansion schemes
in southern European peninsulas.
A synthesis of hypothetical Quaternary scenarios in southern European peninsulas based on available studies may be that
climatic oscillations forced shifts in distributions, with less
displacement in altitude and latitude as compared to higher
latitudes, and that extinction of both genotypes and populations was minimized. Therefore, each adverse period, rather
than erasing species or populations, caused their movement
across a wide possibility of patches and altitudes due to varied
topography. The consequence was dynamism of lower spatial
scale but with more source diversity involved at the genotype,
population and species level. This implied that differentiation
in allopatry achieved in a variety of niches was sometimes
interrupted, or at least influenced, by new contacts that resulted in gene flow, hybridization and even hybrid speciation
at the homoploid or polyploid level. Thus, the main features of
species and populations in the southern European peninsulas
across the Ice Ages were probably preservation, accumulation, complete or incomplete differentiation, and admixture
not restricted to spatially stable areas (hybrid zones). I am not
claiming that such a scenario, and especially those processes,
have not occurred in higher latitudes, e.g., in the Alps, but their
intensity and thus influence are inferred to have been greater in
southern European regions as judged from evidence gathered
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TAXON 60 (2) • April 2011: 365–372
over more than a century of biosystematic work and more than
two decades of molecular data.
Due to the complex patterns resulting from such a scenario, general models are effectively difficult to develop.
However, our research group has proposed hypothetical models for some case studies in the Sierra Nevada massif that
have the potential to be applicable to other systems. These
include the frequent occurrence of hybridization following
altitudinal migrations driven by Quaternary climatic oscillations (Gutiérrez Larena & al., 2002). These conclusions
were mainly based on cpDNA haplotype sharing patterns. But
fine-scale studies of ribosomal and cpDNA sequences also
suggest contact zones (admixture and hybridization) resulting from short-distance expansion following some degree of
isolation (Nieto Feliner & al., 2004; Gutiérrez Larena & al.,
2006). Hybridization fostered by climatic oscillations seems
to be particularly relevant for plant groups in the southern
Spanish ranges where, as mentioned above, suitable niches
were available at short distances in altitude or latitude and
where a minimization of extinction of populations and genotypes as compared to northern regions provided the necessary
substrate for secondary contact to take place. Certain systems
have been revealed to be more prone to extensive and adaptive
hybridization, in some cases following the compilospecies
model by which some species are able to extend their niches
through hybridization with congeners (Fuertes Aguilar &
al., 1999). The above examples provide some clues as to how
hybridization has been one of the relevant features in the
southern European peninsulas.
At the phylogeographic level, one consequence of biogeographical complexity in these areas is the lack of patterns, e.g.,
in alpine plants (Vargas, 2003), plus uncertainties in recovering
evolutionary histories of groups (Lihová & al., 2004; Valcárcel & al., 2006). The outcome of the hypothetical Quaternary
scenario for the southern peninsulas explained above is the
accumulation of genetic and species diversity (hotspots) in
these southern Peninsulas (Médail & Quézel, 1999), which in
fact can be refined by identifying particularly rich areas at a
finer scale that can be considered refugia (Médail & Diadema,
2009). However, the appropriateness of searching for glacial
refugia within southern European peninsulas is in itself a matter of discussion.
The concept of glacial refugia makes special sense as the
source(s) of recolonization in areas where effects of climatic
oscillations were more severe. In fact, one of the methods
used to locate refugia in North America was based on tracing the pathways of postglacial migration routes in those areas (Swenson & Howard, 2005). Focusing on the southern
European peninsulas, it would be theoretically relevant to
discover refugia if they exist, that is, the so-called refugiawithin-refugia (Gómez & Lunt, 2007). When considering
the variety of dynamic processes that took place in them,
however, which are based on adding and mixing diversity
(as opposed to plain extinction or wide latitudinal migration
in northern regions), a clear-cut set of minor refugia nested
within the larger so-called refugia (peninsulas) is not a major
expectation.
TAXON 60 (2) • April 2011: 365–372
In my opinion, the relevant questions would be to ask not
just where populations were preserved during climatically
adverse periods, because this question is not simple even in
northern areas if refugia did not persist across cycles, but
instead: How did populations survive? What processes took
place during the climatic oscillations? What consequences
did those processes have on the genetic structure and identity
of species?
PROSPECTS FOR STUDYING THE EFFECTS
OF CLIMATIC OSCILLATIONS iN SOUTHERN
EUROPEAN REFUGIA
Processes and mechanisms involved in the complex biogeographical history of the whole Mediterranean Basin in general, and in southern European peninsulas in particular, have
contributed to shape current diversity of these areas and are
therefore subjects of great interest (Thompson, 2005). How to
disentangle the role and effects of those processes is difficult,
both in a general sense, i.e., for most organisms, and for particular case studies. Phylogeographic patterns across different
organisms are consequence of geologic and/or climatic phenomena that have affected the entire biota. The more dramatic
those forces have been, the stronger will have been uniformity of patterns of diversity and distribution in the biota. Since
the history of southern peninsulas has been of preservation
rather than dramatic events, replicated patterns should be more
scarce than in northern regions. In this respect, the quotation
from Byrne (2008) from Southern Australia seems to fit nicely
the situation in the Mediterranean Basin: “… major biotic responses to climatic change involve persistence and resilience
rather than large-scale migration, indicating the importance
of dynamic evolutionary processes and a mosaic of habitats in
heterogeneous landscapes for species to persist though changing environmental conditions”.
To understand the importance of processes in southern
European peninsulas, some ideas might be worthwhile to consider. Selecting simplified systems, e.g., linear distributions,
as objects of study is important (Clausing & al., 2000; Piñeiro
& al., 2007; Escudero & al., 2010).
Specific testable hypotheses regarding changes in distribution motivated by climatic changes should be formulated, if
possible, within some definite small timescale. In this regard,
relatively modest geographically-restricted hypotheses (such
as the occurrence of altitudinal migrations or horizontal transfer resulting from them) are better than whole evolutionary
histories across several climatic cycles, because they allow
making predictions of expected patterns. In any case, the influence of preglacial diversity should not be neglected. For instance, Kropf & al. (2006, 2008) have addressed the prediction
that the postglacial retreat of cold-adapted species into high
elevations progressed from south to north (“successive vicariance” model) and that, in Iberia, this would result in greater
genetic distance between populations from Sierra Nevada and
the Pyrenees than between the Pyrenees and the Alps. These
authors have found concordance with such a prediction in
Nieto Feliner • Southern European glacial refugia
some study cases, but not all, which might be due, among
other factors, to the existence of preglacial genetic structure
that cannot be accounted for with only postglacial processes.
Attention must be paid, however, that simplified systems do
not allow inferring general models that can be extrapolated
to every case. Whether or not simplified systems are available, it is also important to consider further factors that might
have been relevant for understanding the effects of climatic
oscillations. For instance, recent research on Mediterranean
groups has focused on testing hypotheses that have been rarely
considered, such as the effects of eustatic sea-level movements
during glacial periods on coastal insular species (Mansion &
al., 2008; Molins & al., 2009).
Using both wide-scale and fine-scale studies with appropriate sampling designs is important to detect occurrence
of the various phenomena that might be involved as well as
different time scales at which they might have operated. For
instance, an unexpected geographic structure of variation of
nuclear ribosomal ITS data, independent of taxonomy, was
confirmed both at a fine-scale level (Nieto Feliner & al.,
2004) and at the generic level (Fuertes Aguilar & Nieto Feliner, 2003). This strengthened reliability of the unexpected
pattern found. A wide sampling strategy also minimizes the
probability of confounding molecular uniqueness with hybridization (Comes & Kadereit, 1998). In this regard, biogeographic
influence from North Africa has contributed significantly to
biodiversity in southern European peninsulas, particularly
Iberia and the Balkans (Ortiz & al., 2007; Guzmán & Vargas,
2009). The Strait of Gibraltar has been an important barrier for
some groups as well (Escudero & al., 2008; Terrab & al., 2008).
Combining different strategies and sources of evidence
is usually an insightful approach to understand evolutionary
history in these areas. Ecological niche modelling studies
(species distribution models) provide independent information on the ecological grounds for current and past distributions (Guisan & Zimmermann, 2000; Waltari & al., 2007;
Marques & al., 2010; Rodríguez-Sánchez & al., 2010). The
main limitation is how far back we can obtain reliable detailed
paleoclimatic reconstructions. The closer we get to the present
(Benito Garzón & al., 2007), the more accurate and therefore
informative our inferences will be. In wind-pollinated species
for which pollen is available, this constitutes an invaluable
source of evidence (Petit & al., 2002). Because of this and
because general patterns in southern European regions are
scarce, more detailed studies are needed not only of trees but
also of herbs to try to understand how species and populations
evolved during those periods (“Southern comfort—behind the
front”, Hewitt, 2001).
CONCLUSIONS FOR CONSEQUENCES OF
CLIMATIC OSCILLATIONS IN SOUTHERN
EUROPEAN PENINSULAS
• No single refugium in each of the southern peninsulas.
• Complex phylogeographic structure resulting from processes that tend to minimize extinction of genotypes,
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Nieto Feliner • Southern European glacial refugia
populations, and species rather than unconnected multiple refugia.
• Lack of general patterns/models as a result of minimization of dramatic effects from climatic oscillations.
• Partial differentiation in allopatry, secondary contact,
and frequent hybridization across small scales rather
than large hybrid zones and suture zones.
• Looking for processes is more interesting than looking
for small refugia.
AcknowledgementS
I appreciate useful comments by Isabel Sanmartín, Peter Schöns­
wetter, Josep A. Rosselló, Javier Fuertes and Pablo Vargas.
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