Pl. Syst. Evol.

259: 121–142 (2006)

DOI 10.1007/s00606-006-0416-y

Molecules and migration: biogeographical studies

in cruciferous plants
M. A. Koch and C. Kiefer

Heidelberg Institute of Plant Sciences, Biodiversity and Plant Systematics, Heidelberg University, Germany

Received October 12, 2005; accepted November 13, 2005

Published online: June 28, 2006

Springer-Verlag 2006

Abstract. In the past two decades our understand-
ing of plant biogeography has been improved
substantially by the introduction of various
molecular marker systems. Especially within the
angiosperms, maternally inherited chloroplast
DNA based data sets have elucidated not only
genetic relatedness but also geographic structuring
of genetic variation. These findings were based on
the observation that DNA molecules might
mutate during migration, which consequently
found its manifestation in the term phylogeogra-
phy introduced in the late 80s by John Avise.
However, other markers such as codominantly
inherited allozymes were used before the advent of
DNA techniques and were used in theoretical
population genetic studies. In actual phylogeo-
graphic studies, highly variable markers, such as
AFLPs (amplified fragment length polymor-
phisms), were needed to unravel recent species
histories (e.g. pleistocenic differentiation). The
levels of molecular variation at such markers are
closer to that of allelic variation measured with
allozymes. Hence, an increasing number of studies
have relied on highly polypmorphic markers, such
as DNA microsatellite loci.
Herein, we try to present an overview on the
various biogeographic and phylogeographic stud-
ies using various molecular (including isozyme)
markers and methodological approaches to ana-
lyse them, concentrating on studies done with
representatives of the Brassicaceae family.
Key words: Biogeography, Brassicaceae, molecular
markers, phylogeography, review.
Introduction
Facing the enormous diversity of organisms and
their continuous or disrupted distribution
ranges, researchers have attempted to explain
the shaping of the recorded distribution range
through time. In classical biogeography, present-
day distribution patterns of species, genera or
other taxonomic hierarchies were compiled (e.g.
Meusel and Jäger 1992) and either discussed in
the context of geological, climatic, or anthropo-
genic data; or compared to palaeobotanical
evidences such as macrofossils or pollen records.
One of the most important breakthroughs
in biogeographical research was the devel-
opment of molecular techniques and the
development of environmentally unbiased indi-
vidual-specific markers (Schaal et al. 1998).
The realization that geographical distribution
corresponds to both the distribution of genetic
diversity and also to genetic distances gave
birth to a new scientific field: Phylogeography
(Avise et al. 1987).
John Avise and co-workers introduced the
term phylogeography only in the late 80s
122 M. A. Koch and C. Kiefer: Biogeography in cruciferous plants

(Avise et al. 1987). Phylogeography examines
the spreading of taxa through space and time.
The spreading of a taxon may be influenced by
landscape morphology, soil composition, com-
petition, and climate. According to the Croll-
Milankovitch theory, warm periods and ice
ages alternated during the Pleistocene as a
consequence of regular variations in the
Earth’s orbit around the sun (Imbrie 1985).
The last ice age, which had its glacial maxi-
mum about 18,000 to 24,000 years ago in
northern parts of Europe and North America,
had a major influence on the distribution of
species as we find them today (Hewitt and
Ibrahim 2000). So today’s distribution patterns
are not only an outcome of habitat preferences
but also mirror colonization histories. During
the course of migration mutations may occur,
and modern molecular biology has delivered
the tools, such as DNA sequencing, which can
then be used to infer colonization histories
(Hewitt 2001).
A very recent development was the intro-
duction of the term ‘‘comparative phylogeog-
raphy’’ (Avise 2000) as it was found that
certain phylogeographical hypotheses not only
apply to a single taxon, but to multiple
taxonomic groups which are co-distributed
(Arbogast and Kenagy 2001). The first phy-
logeographic studies focused on animals, such
as the south-eastern pocket gopher (Geomys
pinetis), and only when appropriate marker
systems were developed was phylogeography
also applied in plant sciences (Schaal et al.
1998).
The Brassicaceae is a plant family of
special interest as it includes many crop
plants (Brassica oleracea, Brassica napus,
Armoracia rusticana and many more), orna-
mentals (Aubrieta, Iberis, Lunaria, Arabis,
Draba and others) as well as the model
organism in plant sciences: Arabidopsis
thaliana. The Brassicaceae family comprises
approximately 3500 species from at least 336
genera (see Appel and Al-Shehbaz 2003).
They show a worldwide distribution on all
continents except Antarctica (Fig. 1). Most of
the taxa are found in temperate regions of the

Fig. 1. Schematic worldwide distribution of cruciferous plants. (redrawn with permission from Stevens (2001).
Locally distributed taxa (e.g. in mountain ranges on Madagascar or New Guinea) have been excluded
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
Northern Hemisphere. However, numerous
genera are also found in the Southern Hemi-
sphere (such as Draba, Lepidium and Card-
amine), and some of them are even endemic
to Southern regions (e.g. South African
genera: Heliophila, Silicularia, Brachycarpa,
Chamira, Schlechteria). In the tropics the
distribution of the Brassicaceae is limited to
mountainous and alpine regions. Here, Arabis
alpina represents the classical example of a
plant with a worldwide northern hemispheric
distribution in mountainous, alpine and arctic
habitats including East African high moun-
tains in Kenya, Tanzania and Ethiopia (Koch
et al. 2006).
The worldwide distribution of the Brass-
icaceae provides an excellent basis to perform
biogeographic and phylogeographic studies
on various taxonomic levels. However, spe-
cies diversity is not distributed equally; the
most important diversification centres are
found in the Irano-Turanian region (ca. 150
genera and ca. 900 species with 530 endem-
ics) and the Mediterranean region (ca. 113
genera and ca. 630 species with 290 endem-
ics). Adjacent regions in North America (ca.
99 genera and 778 species with 600 endemics)
and in the Saharo-Sindian region (ca. 65
300
250
200
total no. of genera
150
100
50
0
1-5 6-10 11-15 16-20 21-25 26-30 31-35 36-40 41-50 51-55 56-60
size class (no. of species)
Fig. 2. Distribution of the number of species (varying from 1 to 350) from 335 genera and 3303 species of the
crucifer family (calculated from descriptions in Appel and Al-Shebhaz (2003)
123
genera and 180 species with 62 endemics)
show a significant reduction in species diver-
sity (Al-Shehbaz 1984, Appel and Al-Sheh-
baz 2003, Hedge 1976). This reduction of
species diversity is continued in southern
regions (South America with 40 genera and
340 species; Southern Africa with 15 genera
and at least 100 species; Australia and New
Zealand with 19 genera and 114 species)
(Allan 1961, Al-Shehbaz 1984, Appel and Al-
Shehbaz 2003, Hewson 1982, Marais 1970).
This overall distribution pattern might pro-
vide some evidence for the origin of the
family in the Irano-Turanian region. Follow-
ing the basic ideas of Hedge (1976), the
origin of the Brassicaceae occurred in a
region encompassing the Mediterranean to
the Irano-Turanian territory. This region is
extremely diverse ecologically, altitudinally,
and geologically, and most of the species
diversity is found in this region.
It should be noted that the taxonomic
circumscription of many taxa, on the genus as
well as species level, is still provisional. Con-
sequently we find a curious distribution of
species number per genus (Fig. 2) with 62% or
72% of the genera with three, respectively five,
or less species.
...
124 M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
The application of modern DNA and pro-
tein-based molecular techniques has allowed for
the inference of systematic relationships within
the Brassicaceae (e.g. Francisco-Ortega et al.
1999, Heenan et al. 2002, Koch et al. 2001a,
Mummenhoff et al. 2001a; for a review Al-
Shehbaz and Beilstein 2006, Koch 2003). As
mutations may occur during migration, molec-
ular techniques enabled researchers to follow
migration routes by correlating phylogenetic
trees with geographical positions. At the dawn-
ing of phylogeography, isozymes were a widely
used marker system in plant systematics and
evolution. They were rarely used in biogeo-
graphic analysis, especially among cruciferous
plants (examples are Brochmann et al. 1991;
Hurka and Neuffer 1997; Koch and Hurka
1999; Koch et al. 1998a, b; Koch and Bernhardt
2004). In cruciferous plants, DNA based tech-
niques such as RFLP analysis of chloroplast
and nuclear DNA (Mummenhoff and Koch
1994, Koch et al. 1998c) were the most widely
applied technique before DNA sequencing
methods of various markers such as the nuclear
ITS (Internal transcribed spacer of ribosomal
RNA, e.g. Francisco-Ortega et al. 1999) and
chloroplast DNA sequences (e.g. trnL, trnF,
rpoC1; e.g. Dobeš et al. 2004b, Franzke et al.
2004) came into the methodological focus.
With the introduction of random DNA
markers (RAPDs: random amplified polymor-
phic DNAs; e.g. Neuffer 1996) at the beginning
of the 90s again population based marker
systems were available. Nowadays, AFLPs
(amplified fragment length polymorphisms;
e.g. Koch et al. 2003a) and microsatellites
(Dobeš et al. 2004a) are more widely used as
most recent results of marker development.
This bridges nearly two decades of research in
phylogeography since John Avise (1987) intro-
duced mitochondrial DNA as a ‘‘… bridge
between population genetics and systematics’’.
This review covers about 100 molecular studies
on biogeography and phylogeography of the
Brassicaceae. The studies represent a broad
spectrum of phylo-/biogeographic theories and
hypotheses and they also cover a broad geo-
graphical range. The summary table (Table 1)
is providing a schematic overview about the
research done in this field within the last two
decades.
Number of studies per region
We oversimplified geographical designation of
the various studies listed herein. Assigning the
studies to geographical regions (Table 1)
shows that the highest number of studies deals
with taxa native to Europe and North Amer-
ica. The number of studies available for Asia is
as low as for the circumarctic/subarctic region,
although species diversity is the highest in Asia
Minor. There are several reasons for this, but
the following two being the most important: 1)
Regions in Central Asia or the Near East have
traditionally been rarely visited by botanists
(long distances, poor infrastructure, and polit-
ical instability) and 2) Many species are poorly
known and sometimes only the record of the
type species exists. This also indicates the great
need and potential of the Brassicaceae as a
paradigm to solve general phylogeography
questions related to these areas.
For all other regions the number of studies
is in concordance with the number of taxa
found in the particular region (Fig. 3).
Number of investigated taxa
It is obvious from Table 1 that only a minor
fraction of the total number of genera has been
analyzed phylogeographically. According to
different taxonomic concepts these studies
comprise approximately 30–35 genera, repre-
senting roughly 10% of the total number of
genera. The number of genera/species is 335/
3303 (Appel and Al-Shehbaz 2003) and this
estimate differs to some extent from the most
recent calculations of 338/3709 (Warwick et al.
2006 - this issue), but it does not affect the
general picture. Although only 10% of the
genera are included in phylogeographical
studies so far, the genera investigated represent
taxonomic groups with high species numbers
such as Boechera (65 species), Biscutella (53
species), Cardamine (197 species), Draba (363
Table 1. A summary of studies focusing on cruciferous plants containing at least some aspects of biogeography or phylogeography. The number
provided with the ‘‘literature column’’ corresponds to the literature list
Genus Geographical region Selected addressed Literature
aspects
Arctic/ East/ Asia Africa Europe S-America N-America Australia/
subarctic Central Minor New
Asia Zealand
Alliaria + + Human influence on Meekins et al. (2001)
colonization
Arabidopsis/ + Human influence, Clauss et al. (2002)
Cardaminopsis glacial history Mummenhoff and
Hurka (1995)
+ Polyploidization, Comai et al. (2000)
hybridization Mummenhoff and
Hurka (1995)
+ Life-history Griffith et al. (2004)
variation, adaptation
+ Phylogenetic relationships Heenan et al. (2002)
+ + + + Simulation of Hoffman (2002)
potential distribution
+ + + Human influence, Hoffman et al. (2003)
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants

refugia,
range-expansion
+ Disjunction Jonsell et al. (1995)
+ + + Gene distribution Koch et al. (2000),
Koch et al. (2001a)
+ + + Genetic isolation Sharbel et al. (2000)
by distance
Arabis/ + Life history variation Bloom et al. (2001)
Boechera
+ Glacial refugia Dobeš et al. (2004a)
+ Impact of ice age, Dobeš et al. (2004b)
fast range expansion
+ + + Gene evolution and Koch et al. (2000),
geography, bridge Koch et al. (2001a)
species, molecular
clock
125
 126
Table 1. (Continued)
Genus Geographical region Selected addressed Literature
aspects
Arctic/ East/ Asia Africa Europe S-America N-America Australia/
subarctic Central Minor New
Asia Zealand
+ Hybrid formation, Koch et al. (2003b)
reticulation and
recolonization
+ QTL variation McKay et al. (2001)
+ Population biology Oyama et al. (1993)
+ Polyploids, refugia Sharbel and
and migration Mitchell-Olds (2001)
+ + + + Centre of origin, Koch et al. (2006)
migration, colonization
Biscutella + Pleistocenic history, Dannemann (2000)
refugia
+ Ploidy levels, relic Tremetsberger
populations et al. (2002)
Capsella + + Gene regulation Hurka and Düring (1994)
+ + + + + Origin, human influence Hurka and
on colonization Neuffer (1997)
+ + + + Human influence Hurka et al. (2003)
on colonization
+ + + Human influence Neuffer (1996)
on colonization
+ Life cycle, altitudinal Neuffer and
transsects Bartelheim (1989)
+ QTL variation Neuffer and
Hoffrogge (1999)
+ Adaption processes Neuffer and
Hurka (1986)
+ + Human influence on Neuffer and
colonization Hurka (1999)
+ Ecotypic variation Neuffer and
inman made habitats Meyer-Walf (1996)
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
 + + Human influence Neuffer et al. (1999)
on colonization
Cardamine + Hybridization Bleeker et al. (1999)
+ + + + Transoceanic dispersal Bleeker et al. (2002b)
+ Postglacial Franzke and Hurka (2000)
polyploidization
and migration
+ Allopolyploidisation Franzke and
Mummenhoff (1999)
+ + Continental disjunction Franzke et al. (1998)
+ Hybrid formation, Hurka et al. (2003)
invasive species
+ population biology Koch et al. (2003c)
+ + + + + Population extinction Lihova et al. (2004a)
during Quaternary
climatic oscillations
+ Geographical Lihova and
distribution Marhold (2003a)
+ Post glacial Lihova and
autopolyploidization Marhold (2003b)
+ Geographic distribution Lihova et al. (2003c)
and gene flow
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants

+ Polyploids, bottlenecks Lihova et al. (2004b)

and long distance
dispersal
+ Relics, polyploids Marhold et al. (2002a)
and migration Lihova et al. (2003c)
+ hybrid formation Marhold et al. (2002b)
+ Neuffer and Jahncke (1997)
+ Geographical Perny et al. (2004)
isolation
by glaciation
+ Polyploids and Perny et al. (2005)
distribution
+ Human impact on Urbanska et al. (1997)
hybrid populations
and the parent species
127
Table 1. (Continued)
128

Genus Geographical region Selected addressed Literature

aspects
Arctic/ East/ Asia Africa Europe S-America N-America Australia/
subarctic Central Minor New
Asia Zealand
Caulanthus + Heavy metal tolerance Mayer and Soltis (1994)
+ Biotope depletion Pepper and
Norwood (2001)
Clausia + Range contraction and Franzke et al. (2004)
expansion during ice-age
Cochlearia + Population structure, Koch (2002)
source for
recolonization
+ Polyploids, divergence, Koch et al. (1996)
centres of origin Koch et al. (1999b)
+ Postglacial migration, Koch et al. (1998a)
allele diversity
+ Ecotypical Nordal et al. (1986)
differentiation
+ Lowland relicts Koch et al. (2003a)
Coelonema + Long-distance dispersal, Chen et al. (2005)
continental
uplift, ice-ages
Crambe + + + + + Origin, disjunctions, Francisco-
long-distance dispersal Ortega et al. (1999)
Dentaria + + + Phylogeny Sweeney and Price (2000)
Diplotaxis + + + + + Colonization Hurka et al. (2003)
Draba + Phylogeny with respect Beilstein and
to geography Windham (2003)
+ Hybrid formation and Brochmann (1992)
postglacial migration
+ Brochmann et al. (1991)
+ Brochmann
et al. (1992a)
+ Brochmann
et al. (1992b)
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
 + Brochmann et al. (1992c)
+ Grundt et al. (2004)
+ Scheen et al. (2002)
+ + Suture zones, Koch et al. (2002)
hybrid formation
+ Postglacial hybrid Widmer and
formation Baltisberger (1999a)
+ Refugia and postglacial Widmer and
migration Baltisberger (1999b)
Lepidium + + + + + + + Transoceanic Bowman et al. (1999),
migartion, Mummenhoff and
intercontinental Franzke (2006),
dispersal Mummenhoff
et al. (2001a)
+ + + + + + + Intercontinental Lee et al. (2002),
hybridization, Mummenhoff and
allopolyploidization, Franzke (2006),
colonization Mummenhoff
et al. (2004),
Mummenhoff
et al. (2005)
+ Centre of origin Mummenhoff
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants

et al. (1992)
+ + + + radiation, long Mummenhoff
distance dispersal et al. (2001a)
+ hybridization Mummenhoff et al. (2004)
and immigration
Microthlaspi + Polyploidy and Koch and
hybridization Bernhard (2004)
+ + Polyploidization, Koch and Hurka (1999)
diversity centre,
refugia, migration
+ + Polyploidization, Koch et al. (1998c)
diversity centre,
refugia, migration
Nasturtium + Hybrid formation and Bleeker et al. (1999)
postglacial migration
129
Table 1. (Continued)
130

Genus Geographical region Selected addressed Literature

aspects
Arctic/ East/ Asia Africa Europe S-America N-America Australia/
subarctic Central Minor New
Asia Zealand
+ Hurka et al. (2003)
+ Long distance dispersal Franzke et al. (1998)
Noccaea + + Pleistocenic migration Koch and
Al-Shehbaz (2004),
Koch et al. (1993)
Pachycladon + Radiation, relationships Heenan et al. (2002)
+ Tertiary/Quarternary Heenan and
adaptive radiation, Mitchell (2003)
recolonization,
distribution maps
+ Population biology Mitchell and
Heenan (2002)
Pritzelago + Origin, diversification, Kropf et al. (2003)
range contraction
and expansion
Rapahanus + Influences Huh and Ohnishi (2001)
on distribution,
diffusion, population
structure
Rorippa + Human impact Bleeker and Hurka (2001)
on hybrid
formation
and survival
+ Bleeker et al. (1999)
+ + + + + + Long distance Bleeker et al. (2002a)
dispersal
+ Colonizing hybrid Hurka et al. (2003)
+ Origin of Mitchell and
New Zealand Heenan (2000)
Rorippa
Sisymbrium + + + + Polyphyletic origin Warwick et al. (2002)
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
Smelowskia + + + Origin, migration Warwick et al. (2004)
Streptanthus + Population disjunction Mayer and Soltis (1994)
+ Population divergence, Mayer et al. (1994)
palaeoendemic origin,
neoendemics
+ Biotope depletion Pepper and
Norwood (2001)
Teesdalia + + Climatic Hoffmann (2000)
differentiation
Thlaspi + + Human influence on Heenan et al. (2002)
migration,
pleistocenic
migration
+ Human dispersal Koch et al. (1998b)
+ + Sequence divergence Mummenhoff
and Koch (1994)
+ + Pleistocenic Koch and
differentiation, Al-Shehbaz (2004)
migration
Warea + Reproductive biology Evans et al. (2000)
Yinshania + Reticulation Koch and
Al-Shehbaz (2000)
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants

Notes:
Coelonema has been integrated into Draba
Dentaria belongs to a widely defined genus Cardamine
Thlaspi s.l. comprises several aggregates such as Noccaea or Microthlaspi
For more details refer to the contributions of Suzanne Warwick and Ishan Al-Shehbaz presented in this volume.
131
132 M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
Fig. 3. Comparison of relative number of studies available for eight defined geographical regions (for definition
see Table 1)
species), Lepidium (231 species), Diplotaxis (32
species), Rorippa (86 species), Sisymbrium (95
species), Caulanthus (17 species), Cochlearia
(19 species), Crambe (35 species), Streptanthus
(34 species) and others. Consequently, nearly
half of the species known have been analysed
either phylogeographically in a strict sense or
are embedded in evolutionary studies discuss-
ing biogeographical questions.
Hypotheses and theories on the distribution
history of various Brassicaceae Taxa
The following paragraphs should introduce a
few pieces of information compiled in Table 1.
Refugia and postglacial colonization. The
effect of the Quaternary ice ages is still
reflected by today’s distribution of species
diversity (Hewitt 2000). Several studies aim
to trace back the migration routes of species to
certain glacial refugia where the plants sur-
vived until a warmer climate allowed recolon-
ization of their original habitats.
For the European flora and fauna three main
refugia have been defined: the Iberian Peninsula,
Southern Italy and the Balkan region (Taberlet
et al. 1998). In America the southern Rocky
Mountains and the Sierra Nevada served as
glacial refugia. Among the Brassicaceae, glacial
refugia have been defined for taxa of the genera
Biscutella (Dannemann 2000), Cochlearia (Koch
2002), Draba (Widmer and Baltisberger 1999b)
or Boechera (Dobeš et al. 2004a, b; Sharbel et al.
2000).
Biscutella laevigata, a European, yellow-
flowering hemikryptophyte shows a disjunct
distribution in Germany. Diploid populations
are found outside areas that had been glaciated
during the last ice age while tetraploid popu-
lations are found in formerly glaciated regions.
The diploid populations are thought to be relic
populations and survival of Biscutella laevigata
during the last ice age in the lowlands of
Germany is assumed (Dannemann 2000).
The genus Cochlearia L., section Cochlea-
ria comprises several polyploid species of
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
pleistocenic origin. Postglacial recolonization
histories were inferred for several taxa within
this genus. Koch et al. (2003a) showed that
C. excelsa, which is found in the Seckauer
Tauern, an area which was heavily glaciated,
probably originated from populations in the
Gurktaler Alpen, which also served as a glacial
refuge area for non-Brassicaceae taxa such as
Saponaria pumila (Tribsch et al. 2002). Peri-
glacial survival is obvious for Cochlearia
species in southern germany in a permafrost
area during the last maximum glaciation
(Koch 2002) on in East Austrian lowlands
(Koch et al. 2003a).
Draba aizoides is a common species in
alpine limestone habitats. Widmer and Baltis-
berger (1999b) detected unusually high
cpDNA haplotype diversity in the Swiss Alps.
As Draba aizoides grows above timberline it
would be expected that populations went
through bottlenecks during the ice age and
that haplotypes were lost during recoloniza-
tion both leading to a decrease in diversity.
Draba aizoides is known from many relict
populations, suggesting that it survived glacial
periods in a variety of glacial refugia in
proximity to the Alps that consequently
reduced the loss of genetic variation.
Boechera, formerly included into the genus
Arabis, is distributed throughout North Amer-
ica including Greenland. Considering the three
most widely spread taxa within the genus,
B. holboellii, B. stricta and B. x divaricarpa,
genetic diversity was found to be highest in the
Rocky Mountains from Idaho and Montana
south to Utah and Colorado. This area prob-
ably served as a glacial refugium, in addition to
arctic and boreal regions in Alaska near the
Great Lakes (Dobeš et al. 2004a).
Postglacial recolonization histories were
inferred for Cochlearia officinalis (Koch et al.
1998a) and Cardamine amara ssp. austriaca
(Lihova et al. 2003b). For Cochlearia officinalis
a decrease in allele number per population
with latitude was observed in Scandinavia
leading to the conclusion that C. officinals
immigrated into Scandinavia post-glacially
(Koch et al. 1998a).
133
Cardamine amara ssp. austriaca, an auto-
polyploid derivative of ssp. amara recolonized
open areas offered by the retreating glaciers in
the Eastern Alps (Lihova et al. 2003b). Colo-
nization scenarios in Central Europe are also
available for Arabidopsis thaliana based on
several molecular markers (Schmuths et al.
2004; Sharbel et al. 2000; for review see
Charlesworth and Vekemans 2005). Arabidop-
sis thaliana is native to Eurasia and North
Africa and has become widely naturalized in
the Western Hemisphere following European
settlers. It was hypothesized by Sharbel et al.
(2000) that post-glacial colonization of Europe
happened from refugia on the Iberian Penin-
sula as well as from Asia. A putative suture
zone is probably located in Eastern Europe.
Periglacial range expansions were demon-
strated for Arabis alpina (Koch et al. 2006)
with a center of origin in Asia Minor.
Pritzelago alpina, a high alpine plant,
appears to be of pre-Quaternary origin
(Kropf et al. 2003). Four different major
mountain lineages were recognized by the
analysis of AFLP data and divergence within
the species as well as between the mountain
lineages was shown to be low (Kropf et al.
2003). This may be an effect of interglacial
vicariance (short interaction) as well as inter-
gradation during glacial periods when popu-
lations that descended from high altitudes
came into contact in lower altitude refugia
(long lasting interaction). This means that
Pritzelago alpina had different glacial (long
term) and interglacial (short term) refugia
(Kropf et al. 2003).
Quaternary ice ages were marked by the
repeated advance and retreat of glaciers
(Hewitt 2000). Repeated cycles of recoloniza-
tion of deglaciated areas and retreat from the
expanding glaciers highly influenced the dis-
tribution of species and their genetic diversity
as we find it today. Apparently, Clausia
aprica, a steppe plant in Central Asia has
undergone several cycles of range contraction,
isolation and range expansions leading to
repeated hybridization events (Franzke et al.
2004).
134 M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
Migration and long distance dispersal.
Migration often happened along defined
migration routes (Hewitt and Ibrahim 2000).
Arabis alpina has its putative centre of
origin in Asia Minor and three colonization
routes led the plant into the Circummediterra-
nean as well as into East Africa where it is
found in afroalpine habitats. Arabis alpina
reached the East African mountains via the
mountain ranges on the Arabian Peninsula
(Koch et al. 2006), a route which was also
confirmed for Lepidium (Mummenhoff et al.
2001a), Rorippa (Bleeker et al. 2002a) and
Cardamine (Bleeker et al. 2002b).
Different Draba taxa reached North Amer-
ica via the Bering Bridge from high mountains
in Central Asia as well as from circumarctic
areas leading to the formation of a ‘‘continen-
tal-wide’’ hybrid zone (Koch and Al Shehbaz
2002). The same route was used by other taxa
such as Noccaea (Koch and Al-Shehbaz 2002)
or Lepidium (Mummenhoff et al. 2001a).
North-South American disjunctions have been
shown for various genera from a monophyletic
American lineage (‘‘halimolobine’’ crucifers)
such as Pennellia or Mancoa (Bailey et al.
2002).
Microthlaspi perfoliatum has its centre of
diversity in the East Mediterranean and
migrated into North Africa and into the
Western European Mediterranean. From these
areas polyploid lineages migrated northwards
(Koch and Bernhardt 2004, Koch and Hurka
1999, Koch et al. 1998c) and colonized Central
Europe postglacially.
In cruciferous plants long distance dispersal
played an essential role in the colonization of
Australia by Lepidium species. Lepidium prob-
ably originated in a region covering the Med-
iterranean and Irano-Turanian. The genus
comprises about 230 species and is distributed
worldwide. This worldwide distribution was
reached by migration as assumed for the
colonization of Africa (immigration into North
and North West Africa as well as into South
Africa by the East African route described
above) and North America (via the Bering
Bridge) and long-distance dispersal into the
Hawaiian Archipelago as well as to Australia
and New Zealand. Source areas for the colo-
nization of Australia were South Africa and
North America and Australian Lepidium taxa
were found to be of hybridogenous origin
between African and North American taxa
(incongruence of cpDNA and nuclear DNA
phylogenies). Long distance dispersal into
Australia was probably mediated by migrating
birds (Mummenhoff et al. 2004).
The immigration of Rorippa (Bleeker et al.
2002a) and Cardamine (Bleeker et al. 2002b)
into Africa was also explained by long distance
dispersal. The population structure of Coelo-
nema, a monotypic genus (only C. draboides)
endemic to the Qilian Mountains of the
Qinghai-Tibet Plateau (Chen et al. 2005) might
also be explained by long distance dispersal.
The major part of the genetic variation
(RAPD) was found to be within the popula-
tions rather than between them which may be
explained by high rates of recombination
within and a large amount of gene flow
between the populations. This was also true
for populations separated by distances as large
as 200 km. Gene flow between those popula-
tions was assumed to be not due to pollen but
due to long-distance dispersal of seeds by
winter storms and creeks. The general impor-
tance of long-distance dispersal combined with
alloploidization was reviewed by Mummenhoff
and Franzke (2006).
Endemics. Several studies focus on the
evolutionary history of endemics. A present
day status of endemism might be either the
result of migration and subsequent diversifica-
tion, migration and subsequent extinction of
source populations or local differentiation
within the original distribution range. Popula-
tions of members of the Streptanthus glandu-
losus complex in North America are found to
be highly disjunct on serpentine soils. It is
hypothesized that Streptanthus glandulosus ssp.
glandulosus, the putative ancestor of the whole
genus, was widely distributed until range
fragmentation occurred (Mayer and Soltis
1994, Mayer et al. 1994). Neoendemics formed
rapidly due to chromosome repatterning.
M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
Another rare serpentine endemic is Caulanthus
amplexicaulis var. barbarae which also belongs
to the Strepthantoid group. Pepper and Nor-
wood (2001) suggested a biotype depletion
scenario for the origin of this taxon. In
contrast to those North American heavy metal
tolerant taxa, Thlaspi caerulescens was able to
recolonize the whole Central European range
(Koch et al. 1998b) and heavy metal tolerance
most likely has been constituted several times
independently.
Evolutionary history was also analysed for
narrowly distributed endemics such as Coch-
learia bavarica in Bavaria/Germany. The
parental species of C. bavarica were found to
be C. pyrenaica and C. officinalis and it is
supposed that C. bavarica is of inter- or
postglacial origin. The fragmented populations
as they are found today for C. bavarica are
thought to be the remnants of a formerly
continuous distribution range (Koch 2002).
Another narrowly distributed endemic is
Warea carteri, a fire stimulated annual en-
demic of the Lake Wales Ridge in Florida.
Genetic infraspecific variation in Warea carteri
is low and the small amount of genetic
diversity is observed is geographically struc-
tured. Such information is of great value in
respect of species conservation (Evans et al.
2000).
Endemics may also evolve as a result of
isolation as it is true for example for island
endemics e.g. some members of the New
Zealand genus Pachycladon. Pachycladon
underwent radiation during the late Tertiary/
Quaternary (Heenan et al. 2002, Heenan and
Mitchell 2003). In general New Zealand
Pachycladon is divided into three lineages, of
which each contains endemic species such as
P. exilis (three sites in Otago on calcareous
substrates), P. stellata (southern Marlborough
on weakly metamorphosed greywacke) and
P. walli (Caples terrane on sandstone and
semi-schist).
Colonizing weeds and human influence on
dispersal and survival. Some plants are better
colonizers than others. Many invasive plants
are short lived and autogamous which often
135
leads to low intrapopulational genetic diver-
sity. Good colonizers quickly expand their
distribution ranges and conquer the world
sometimes aided by other colonizing species.
Capsella bursa-pastoris is an example of an
extremely successful colonizer. It originated in
Eurasia and spread to the New World only
during the past 500 years following European
settlers. Several studies indicated that Capsella
bursa-pastoris was introduced into America
several times originating from different parts
of Europe depending on the home-countries of
the settlers (Hurka and Düring 1994, Hurka
and Neuffer 1997, Hurka et al. 2003, Neuffer
1996, Neuffer and Hurka 1999, Neuffer et al.
1999). It should be noted here, that Capsella
bursa-pastoris is one of the best-analysed
example for worldwide propagation influenced
by men (see the various papers of Hurka and
Neuffer). A similar colonizing history into
North America was also described for Alliaria
petiolata (Meekins et al. 2001) and Arabidopsis
thaliana (Sharbel et al. 2000, Hoffmann et al.
2003). Settlers in North America also intro-
duced Alliaria petiolata only about 125 years
ago. Since then it has become a pest in North
America. Alliaria petiolata is a short-lived
biennial capable of producing vast amounts
of seeds with low dispersability. Thus dense
populations form quickly and spread via an
advancing front from an established popula-
tion centre.
Cultivation of plant species or creation of
new habitats by human activities may have an
effect on dispersal and survival of taxa. This is
especially true of hybrid species, which often
grow in disturbed or intermediate habitats,
and are dependent on the preservation of their
niche. The formation and persistence of Nas-
turtium x sterile (hybrid between N. micro-
phyllum and N. officinale) for example is
greatly dependent on human activities. The
introduction of N. officinale into the natural
habitats of N. microphyllum lead to the
formation of the successful hybrid but also
the hybrid itself was cultivated as brown cress
on the British Isles. In northwest Germany N.
x sterile grows in drainage ditches and its
136 M. A. Koch and C. Kiefer: Biogeography in cruciferous plants
persistence is therefore dependent on the
management of these ditches by farmers
(Bleeker et al. 2002a). Drainage ditches in
northwest Germany also play a role in the
evolution of Rorippa hybrids as they favour
hybridisation zone formation (Bleeker and
Hurka 2001).
Another example of a species depending on
site management is Cardamine insueta (C.
rivularis x amara) at Urnerboden in Central
Swizerland (Urbanska et al. 1997).
Concluding remarks
A continuously increasing number of phyloge-
netic studies are available for various
cruciferous taxa of different taxonomic levels
(Al-Shehbaz and Beilstein 2006, Beilstein et al.
2006). The reconstruction of a first compre-
hensive phylogeny based on more than 1.500
available ITS sequences has been completed
(Bailey et al., in press), and the integration of
various phylogenies based on different molec-
ular markers into a comprehensive family-wide
phylogeny is possible e.g. using ‘‘Super Trees’’
algorithms (SplitsTree, Huson et al. 2004).
These data not only provide the basis for
phylogeographic hypothesesof various taxo-
nomic levels, but also offer the possibility to
understand the biogeographic history of the
whole family with an increasing number of
phylogeographic studies. Consequently, rather
than simply considering Brassica and Arabid-
opsis thaliana as dicotyledonous model organ-
isms, the whole Brassicaceae family can be
used as an example to understand phylogeo-
graphic patterns – the evolution of taxa in
space and time – in a broader, worldwide
context.
We are grateful to Eric Schranz for critical
reading, helpful discussion and improvement of
the manuscript. Our research on Brassicaceae
discussed in this review has been substaintially
supported by the German Research foundation
(DFG), German Academic Exchange Service
(DAAD), the Austrian Science Fund (ASF) and
Humboldt-Foundation.
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Address of the authors: Marcus A. Koch (e-mail:
marcus.koch@urz.uni-heidelberg.de), Christiane
Kiefer, Heidelberg Institute of Plant Sciences,
Biodiversity and Plant Systematics, Heidelberg
University, Im Neuenheimer Feld 345, 69120
Heidelberg, Germany.