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ORIGINAL PAPER
The role of intraspecific hybridization in the evolution
of invasiveness: a case study of the ornamental pear
tree Pyrus calleryana
Theresa M. Culley ÆNicole A. Hardiman
Received: 20 July 2007 / Accepted: 22 January 2008 / Published online: 28 October 2008
ÓSpringer Science+Business Media B.V. 2008
Abstract Hybridization between genetically dis-
tinct populations of a single species can serve as an
important stimulus for the evolution of invasiveness.
Such intraspecific hybridization was examined in
Pyrus calleryana, a Chinese tree species commonly
planted as an ornamental in residential and commer-
cial areas throughout the United States. This self-
incompatible species is now escaping cultivation and
appearing in disturbed habitats, where it has the
potential to form dense thickets. Using genetic
techniques incorporating nine microsatellite markers,
we show that abundant fruit set on cultivated trees as
well as the subsequent appearance of wild individuals
result from crossing between genetically distinct
horticultural cultivars of the same species that
originated from different areas of China. We con-
clude that intraspecific hybridization can be a potent
but little recognized process impacting the evolution
of invasiveness in certain species.
Keywords Callery Pear Evolution
Intraspecific hybridization Pyrus calleryana
Self-incompatibility
Introduction
Hybridization is a strong evolutionary force that can
potentially reshape the genetic composition of pop-
ulations and create novel genotypes that facilitate
adaptation to new environments (Stebbins 1950;
Anderson and Stebbins 1954; Arnold 1997). The
importance of hybridization in evolutionary processes
such as speciation has long been acknowledged
(Darlington 1940; Stebbins 1959,1969), but its
application to the field of invasion biology has only
more recently been discussed (Abbott 1992; Ellstrand
and Schierenbeck 2000; Cox 2004; Schierenbeck and
Aı
¨nouche 2006), as has the larger role of evolution
itself (Lee 2002; Lavergne and Molofsky 2007;
Novak 2007). Hybridization between genetically
distinct taxa has been proposed as a mechanism for
the evolution of invasiveness in introduced and native
species (Ellstrand and Schierenbeck 2000). Most
well-known examples involve interspecific or inter-
generic processes (Ellstrand and Schierenbeck 2000),
as in Spartina (Aı
¨nouche et al. 2003; Cox 2004)or
Senecio (Abbott 1992).
Less well studied has been intraspecific hybrid-
ization, defined as successful matings between
individuals from well differentiated populations
originally isolated from one another and consequently
with different gene frequencies (Stebbins 1950). As
such, this process does not pertain to crosses between
individuals from the same gene pool that possess
different alleles (Arnold 1997). If resulting F
1
hybrid
T. M. Culley (&)N. A. Hardiman
Department of Biological Sciences, University
of Cincinnati, 614 Rieveschl Hall, Cincinnati,
OH 45221-0006, USA
e-mail: theresa.culley@uc.edu
N. A. Hardiman
e-mail: hardimna@email.uc.edu
123
Biol Invasions (2009) 11:1107–1119
DOI 10.1007/s10530-008-9386-z
individuals or later generation hybrids are fertile,
recombination may lead to novel genetic rearrange-
ments which can allow hybrids to expand their
ecological tolerance and invade new niche environ-
ments (Stebbins 1959; Arnold 1997). Intraspecific
hybridization can also result in increased genetic
variance, altered epistatic interactions, masking or
unloading of deleterious alleles, and/or transfer of
favorable genes (Lee 2002). Alternatively, such
hybridization events can also produce outbreeding
depression by disrupting co-adapted gene complexes
and local adaptation in established species (Arnold
1997). Intraspecific hybridization has been carried
out artificially for centuries to improve agriculturally
or horticulturally important plant species (Khanduri
and Sharma 2002; Johnston et al. 2003), but it has
rarely been examined in natural populations, with few
exceptions (Hufford and Mazer 2003; Erickson and
Fenster 2006; Johansen-Morris and Latta 2006).
Within the context of invasion biology, intraspe-
cific hybridization could potentially explain the
recent spread of certain species, such as those with
extended lag periods (Sakai et al. 2001), during which
time hybridization and selection may act to create
invasive genotypes (Ellstrand and Schierenbeck
2000). Intraspecific hybridization is most likely to
follow multiple introductions of a species (Kolbe
et al. 2004), especially non-native species that are
transplanted from different parts of their native range
into a new locality. Multiple introductions may be
done deliberately, for example, when plant species
are imported for horticulture (Reichard and White
2001; Burt et al. 2007) or accidentally as when seeds
are introduced as contaminants during shipping
(Sakai et al. 2001). Once introduced, genetically
distinct individuals may cross-pollinate to create
novel genotypes through admixture that otherwise
would never have been possible in the native
environment (Arnold 1997; Novak and Mack 2005;
Roman and Darling 2007). In this way, among-
population variation present in the native range is
transformed into within-population variation in the
introduced area (Kolbe et al. 2004). Although most
novel genotypes may be inappropriate in the new
environment, production of individuals combined
with novel selection (e.g. release from native com-
petitors, predators or pathogens) may strongly favor
certain genotypes. Within native species, intraspecific
hybridization can also occur if new genotypes are
introduced from different parts of the native range.
However, not all cases of intraspecific hybridization
will lead to invasiveness (Ellstrand and Schierenbeck
2000; Wolfe et al. 2007), but only when the right
combination of novel genetic rearrangements match
with the appropriate introduced environment in which
invasive traits can be selected.
The purpose of this paper is to examine the role of
intraspecific hybridization in the evolution of inva-
siveness in plant species. To do so, we first define the
process of intraspecific hybridization as it relates to
invasive species, citing specific examples in the
literature. Second, we focus on a case study of the
Callery Pear (Pyrus calleryana; Rosaceae), an
ornamental Asian tree that is increasingly invading
sites throughout the United States. Finally, we
conclude with suggestions for future research. Ulti-
mately, we maintain that intraspecific hybridization is
a potentially important and often overlooked stimulus
for facilitating invasiveness in certain species given
the right conditions.
Evidence of intraspecific hybridization
The process by which intraspecific hybridization can
lead to invasiveness (Wolfe et al. 2007) requires four
steps. If any of these steps do not hold, invasiveness
may not evolve through this mechanism. First,
founders from at least two genetically divergent
populations of a species must be introduced into the
same area. Evidence of such multiple introductions
consist of known introductory history of the species
(e.g., Luken and Thieret 1996) or genetic data tracing
back the origin of introduced populations to different
parts of the native range (e.g., Williams et al. 2005).
Second, individuals from these differentiated popu-
lations must cross and produce fertile offspring. In
some species, this may create novel recombinant
genotypes (i.e. admixture) with a selective advantage
in the new range. The offspring may also exhibit
elevated levels of genetic variation, especially if the
parental populations each experienced separate
genetic bottlenecks or founder events that lowered
levels of variation within their respective populations
(Husband and Barrett 1991; Cox 2004; Novak and
Mack 2005; but see Roman and Darling 2007). Third,
recombinant hybrids must be fit, generate offspring
and able to persist in new environments by possessing
1108 T. M. Culley, N. A. Hardiman
123
invasive characters that allow them to exploit resources
in current or new habitats. In some F
1
hybrids,
increased fitness may be evident because of heterosis
due to overdominance (Facon et al. 2005) and not
necessarily to recombination. Finally, natural selection
in the new environment must favor certain gene
combinations in hybrid individuals and consequently
their traits will persist and spread in populations.
There are several cases of invasive species in
which some or all of these steps are present. In the
tree species Schinus terebinthifolius for example,
there is evidence of multiple introductions into North
America from genetically different source popula-
tions along with post-introduction recombination
events (Williams et al. 2005,2007). The same is
also true for the grass Phalaris arundinacea (Laver-
gne and Molofsky 2004,2007), which at one time had
been suggested to be dominated by European culti-
vars that escaped cultivation (see Lavoie and
Dufresne 2005). Although multiple introductions
have been indicated in Alliaria petiolata (Durka
et al. 2005), Ambrosia artemisiifolia (Genton et al.
2005), Bryonia alba (Novak and Mack 1995), and
Hirschfeldia incana (Lee et al. 2004), it remains
unclear whether hybridization has subsequently
occurred because these studies were not designed to
examine recombination events.
Current behavior and past history of an invasive
species can also superficially resemble intraspecific
hybridization. For example, common reed (Phrag-
mites australis) is native to North America where it is
now spreading and forming dense monocultures
(Orson 1999; Wilcox et al. 2003). Recent genetic
evidence suggests that these invasive populations are
composed primarily of a single introduced Eurasian
genotype, which instead of hybridizing with native
genotypes, is now outcompeting and displacing them
(Saltonstall 2002; Wilcox et al. 2003; Lelong et al.
2007). A similar process may also be occurring in
ornamental fountain grass (Pennisetum setaceum), an
introduced Eurasian perennial in which invasive
populations in Hawaii and Arizona contain the same
genotype (Poulin et al. 2005). This genotype was also
found in noninvasive California populations, indicat-
ing phenotypic plasticity in invasiveness within the
species (Poulin et al. 2005). In another case, Silene
latifolia has undergone multiple introductions into
the United States from genetically structured Euro-
pean populations, but artificially crossing plants from
different source populations did not increase hybrid
reproductive output or survival in a common garden
(Wolfe et al. 2007). Consequently detailed examin-
ations of additional species are needed to fully
understand the impact of intraspecific hybridization
in the evolution of invasiveness.
Case study of the Callery Pear
Pyrus calleryana is an ornamental tree species from
Asia that is in the early stages of spread in the United
States (Vincent 2005; Culley and Hardiman 2007;
Hardiman and Culley 2007). The species, commonly
known as the Callery Pear, is a popular cultivated tree
often planted in commercial and residential areas,
where it is prized for its early spring flowers, rapid
growth, and fall color. Until recently, the species was
considered unable to escape from cultivation or to
naturalize because of self-incompatibility, vegetative
propagation, and rare fruit production (Gilman and
Watson 1994). The species is currently recognized as
invasive because volunteer populations have been
reported with increasing frequency over the last
5 years in at least 26 states (Vincent 2005; Culley and
Hardiman 2007), concurrent with recent observations
of abundant fruit set in cultivated and escaped
individuals. Because of its present spread, the species
is now listed by the United States Fish and Wildlife
as a plant invader of Mid-Atlantic natural areas
(Swearingen et al. 2002) and is considered either
invasive or watch-listed in ten states (Culley and
Hardiman 2007).
The reproductive biology of Pyrus calleryana is
conducive to its ability to invade new areas. In early
spring before leaves appear, abundant flowers are
produced with 6–12 flowers per inflorescence (Cuizhi
and Spongberg 2003). Each flower contains 20
stamens and 2–5 fused carpels with two ovules per
locule, giving a maximum seed number of 10 (Jackson
2003). Pollen is dispersed by several generalist
pollinators, including honeybees (Apis mellifera L.),
bumble bees (Bombus terrestris L.) and hover flies
(Farkas et al. 2002). Fruits mature in autumn and are
dispersed by animals such as European starlings,
American Robins, and squirrels (Gilman and Watson
1994). Pyrus calleryana exhibits gametophytic self-
incompatibility (Zielinski 1965) in which compatible
crosses are only possible between haploid pollen and
The role of intraspecific hybridization in the evolution of invasiveness 1109
123
diploid pistil tissue that do not share a self-incompat-
ibility allele. In this system, crosses can result in full
compatibility, partial compatibility, or complete
incompatibility, depending on the genotypes of the
two individuals being crossed. In invasive popula-
tions, the self-incompatibility (SI) system acts to
maximize outcrossing and hence hybridization events
(Culley and Hardiman 2007) but its effectiveness
depends on the number of SI alleles present within
populations. In new populations, the SI system may
contribute to an Allee effect and slow invasion
(Taylor et al. 2004; Taylor and Hastings 2005)
because low density of individuals may limit the
number of compatible genotypes present and there-
fore their ability to reproduce with one another (i.e.
decrease fitness). However, the Allee effect can be
overcome with time as the number of introductions
increase and gene flow is facilitated by a variety of
pollen and seed dispersers, which in turn increases
diversity of SI alleles.
Here we provide evidence that the invasive nature
of P. calleryana has evolved via intraspecific hybrid-
ization, as outlined by some of the criteria above.
Namely, introduced populations of P. calleryana
consist of cultivars (i.e. cultivated varieties that have
been artificially selected for horticulturally import ant
traits) that represent native genotypes from different
areas of the Asian range. In addition, crossing
between these genetically distinct cultivars has cre-
ated recombinant hybrid genotypes that comprise
invasive populations. Currently we are examining the
fitness of these genotypes relative to the parental
cultivars to determine if they exhibit a fitness
advantage in field conditions. Because several char-
acteristics of P. calleryana described below are also
present in other introduced species, the case of the
Callery Pear can serve as a model for other poten-
tially invasive species.
History of multiple introductions
Pyrus calleryana was originally introduced to breed
fire blight resistance and provide compatible root-
stock for Pyrus communis, the common edible pear
(Culley and Hardiman 2007). The species was
imported into the United States beginning in the
early 1900s, primarily by the USDA plant explorer,
Frank Meyer and plant breeder Frank Reimer, both of
whom collected seed in various regions in China,
Japan and Korea in 1918. According to Meyer’s
(1918) correspondence, the species was found grow-
ing in a wide variety of habitats in China where it had
a thorny phenotype and sparsely occurred in small
populations. Meyer obtained P. calleryana seed from
at least five different geographic locations while
Reimer also collected seed in Korea and Japan
(Cunningham 1984), although Reimer’s seed collec-
tions were not maintained separately. Following
importation to the United States, the species was
primarily maintained and tested at the USDA Intro-
duction Station in Glenn Dale, Maryland and at
Corvallis, Oregon where large numbers of seedlings
were planted and monitored for fireblight testing and
as a source of rootstock for economically important
Pyrus species.
The species was first cultivated as an ornamental
flowering tree several decades later, beginning with
an attractive non-thorny tree found growing at the
Glenn Dale site and first sold commercially in 1962
as the ‘Bradford’ cultivar (Whitehouse et al. 1963).
As a result of its widespread popularity nationwide,
several additional cultivars were subsequently intro-
duced through the latter half of the twentieth century.
Many of these cultivars are derived directly from
different introductions of Asian seed collected in the
earlier part of the century (Table 1). For example,
‘Bradford’ was selected from a seedlot sent to the
USDA in 1919 from Nanking, China while ‘Autumn
Blaze’ originated from Reimer’s 1918/1919 collec-
tion. A limited number of cultivars are also
potentially of hybrid origin; for example, ‘White-
house’ presumably resulted from a cross between
‘Bradford’ and an unknown P. calleryana (Accession
information for PI420995 at the National Clonal
Germplasm Repository; http://www.ars.usda.gov). To
maintain the uniform characteristics of each cultivar,
trees are vegetatively propagated by grafting the
desired cultivar (the scion) onto P. calleryana root-
stock; thus, all individuals of a given cultivar should
consist of genetically identical scions, although the
rootstock genotypes often vary (T.M. Culley, N.A.
Hardiman, unpublished data).
Today at least 25 different cultivars are available
(Table 1) with more being developed and the species
remains extremely popular among nurserymen and
horticulturalists. Over 1.5 million Callery Pear trees
were sold in 1998 alone totaling over $30 million
dollars (Li et al. 2004), and the ‘Chanticleer’ cultivar
1110 T. M. Culley, N. A. Hardiman
123
was named the Urban Street Tree of the Year in 2005
(Phillips 2004). Consequently, the popularity of this
species among the general public combined with its
commercialization has led to a situation where
different Asian genotypes (i.e. cultivars) have pur-
posely been introduced multiple times across the
country and are still planted today.
Genetic differentiation of source populations
Another criterion for intraspecific hybridization lead-
ing to invasiveness is that the introductions must be
from genetically differentiated source populations.
This seems likely in Pyrus calleryana given that
most cultivars originated as seeds collected from
Table 1 List of cultivars of Pyrus calleryana, including the year each became commercially available, the site of origin and the
source and/or parentage of the cultivar, if known
Cultivar Approx. year Site of origin Source
Aristocrat
Ò
1972 Independence, KY Chinese seed collected by Meyer; selected from
P. calleryana seedlings in 1969
Autumn Blaze 1978 Corvallis, OR Parent originated from Chinese seed from
Reimer’s 1917 or 1919 collection
Avery Park 1970s Corvallis, OR From a population of P. calleryana seedlings
planted in Avery Park, Corvallis, OR
Bradford 1962 Glenn Dale, MD Chinese seed purchased in Nanking, China in
1919; original tree planted at the USDA
station (Santamour and McArdle 1983)
Bursnozam (Burgandy
Snow
TM
)
1990s Perry, OH Unknown
Cambridge Abt 2003 Cambridge City, IN Unknown
Capital 1981 Washington, D.C. ‘Bradford’ 9unknown P. calleryana parent
Chanticleer
Ò
(Cleveland
Select, Stone Hill, Select,
Glenn’s Form)
1965 Olmsted Falls, OH &
Corvallis, OR
Original tree planted in Cleveland, OH was
derived from commercial seed purchased in
1946 (Santamour and McArdle 1983)
Cleprizam (Cleveland
Pride
Ò
)
1990 Perry, OH Unknown
Earlyred Unknown Vincennes, IN ‘Bradford’ 9unknown pollen parent
Edgewood
Ò
(Edgedell) 1997 DuPage County, IL P. calleryana 9P. betulifolia
Fronzam (Frontier
TM
) 1990s Perry, OH Unknown
Gladzam (Galdiator
Ò
) 1993 Perry, OH Unknown
Grant St. Yellow Abt 1980 OR Unknown
Jaczam (Jack
Ò
) 1999 Perry, OH Unknown
Jilzam (Jill
TM
) 1990s Perry, OH Unknown
Mepozam (Metropolitan
TM
) 1990s Perry, OH Unknown
New Bradford
Ò
(Holmford) 1996 Boring, OR Unknown
Princess 1976 Olmsted Falls, OH Unknown
Rancho 1965 Olmsted Falls, OH Unknown
Redspire 1975 South Brunswick township,
NJ
‘Bradford’ 9unknown pollen parent
Trinity
Ò
(XP-005) 1978 Portland, OR Purchased seed
Valzam (Valiant
Ò
) 1975 Perry, OH ‘Cleveland Select’ 9unknown pollen parent
Veyna Abt 2004 Visalia, CA ‘Aristocrat’ 9P. kawakammii unknown cultivar
Whitehouse 1977 Glenn Dale, MD ‘Bradford’ 9unknown P. calleryana at USDA
Station
Cultivars analyzed in the genetic study of differentiation (Hardiman and Culley 2007) are italicized
The role of intraspecific hybridization in the evolution of invasiveness 1111
123
populations in different regions of Asia that appear to
be genetically divergent (N.A. Hardiman, T.M.
Culley, unpublished data). It is thus possible to
confirm the genetic differentiation of cultivars (i.e.
native genotypes). To do so, we used nine microsat-
ellite markers that were originally designed for
closely related P. communis and Malus domestica
(Yamamoto et al. 2002; Gianfranceschi et al. 1998),
and which successfully amplify in P. calleryana
(Hardiman and Culley 2007). To examine genetic
differentiation among cultivars, we acquired samples
from each of eight commercially available cultivars
in Southwestern Ohio (2–22 individuals sampled per
cultivar; Fig. 1) and individual samples from seven
additional cultivars from the National Clonal Germ-
plasm Repository (NCGR; Table 1). Genotypes of
the multiple samples for each of the eight cultivars
were also compared to test whether individuals within
each cultivar were genetically identical.
Most cultivars were genetically differentiated from
one another and identifiable based on their multilocus
genotypes. In a Principle Coordinates Analysis (PCoA)
based on all possible pairwise genetic distances
calculated according to Smouse and Peakall (1999;
Fig. 1), each cultivar generally clustered away from all
others, indicating that it is genetically distinct. ‘Brad-
ford’, ‘Valzam’, ‘Whitehouse’, and ‘Capital’ each
contained a unique private allele and ‘Grant St.
Yellow’ contained two private alleles. However,
‘Chanticleer’, ‘Cleveland Select’ and ‘Stone Hill’
cultivars were all genetically identical, which is
consistent with anecdotal accounts that they are
derived from the same street tree in Cleveland, Ohio
(Hardiman and Culley 2007). Within each cultivar,
individuals were genetically identical, except for
‘Redspire’, ‘Autumn Blaze’ and one ‘Cleveland
Select’ sample. These anomalous individuals differed
by only a single allele at one to four loci, and were
obtained from the same nursery indicating potential
contamination or mutation within the growers stock. In
addition, an AMOVA provided evidence for signifi-
cant genetic differentiation among cultivars, with the
majority of variation explained by genetic structuring
among cultivars (U
PT
=0.961, P\0.001) rather than
within cultivars. These data do not include rootstock
genotypes, which in preliminary analyses are always
genetically different than the scions with which they
are paired (T.M. Culley, N.A. Hardiman, unpublished
data); thus the rootstock has the potential to cross with
the scions if allowed to sprout and flower. Conse-
quently the introduced populations of cultivars of
P. calleryana in the United States represent a mixture
of genetically different Asian genotypes.
Hybridization and genetic recombination
Given that genetically different cultivars are fre-
quently planted in residential and commercial areas
across the United States, there is potential for these
cultivars to naturally outcross-pollinate and produce
fertile hybrids. This is critical because as a self-
incompatible species, fruits cannot be produced in
P. calleryana through selfing or cross-pollination of
individuals of the same cultivar. The ability of
cultivars to successfully hybridize with one another
was examined two different ways.
Axis 1 (44.9%)
Axis 2 (18.9%)
Aristoc
Bradfo
Chantic
Clevela
Stoneh
Redspi
Capital
Faurie
Autumn
Early R
Valzam
Princes
Grant S
Whiteh
Avery P
rat
rd
leer
nd
ill
re
Blaze
ed
s
t. Yellow
ouse
ark
(N = 18)
(10)
(4)
(22)
(2)
(14)
(8)
(1)
(2)
(1)
(1)
(1)
(1)
(1)
(1)
Fig. 1 Principle
coordinates analysis based
on pair-wise genetic
distance (calculated
according to Smouse and
Peakall 1999) showing
genetic differentiation
among cultivars of P.
calleryana sample sizes are
given in the legend
1112 T. M. Culley, N. A. Hardiman
123
First, we performed hand-pollinations in a common
garden over 3 years comparing fruit set among
reciprocal crosses of four common cultivars: ‘Brad-
ford’, ‘Chanticleer’, ‘Aristocrat’ and ‘Redspire’.
Hand-pollinations were performed on multiple indi-
viduals of each cultivar, using emasculated flowers on
days 3–4 of anthesis. Each cross combination between
cultivar pairs was replicated at least twice. Self-
pollinations or crosses within each cultivar were also
preformed and occasionally resulted in fruit formation,
but no viable seeds were obtained. Reproductive
success across all cultivar cross combinations was
high, with four of the cross combinations resulting in
100% fruit set and an average percent fruit set of 75%
(Table 2). Overall, few differences were found among
cross combinations, indicating that cultivars are capa-
ble of freely crossing with one another. The single
exception was the ‘Bradford’ 9‘Chanticleer’ cross
with ‘Bradford’ as the maternal parent in which no
fruits were formed, but this was based on a small
sample size. Differences in fruit set across cross
combinations may be primarily driven by the game-
tophytic SI system in P. calleryana, which is currently
being tested at the genetic level. Fruits on average,
yielded approximately 2 seeds (range: 1–4), with
over 87% seed germination expressed in most crosses
(N.A. Hardiman, T.M. Culley, unpublished data);
seedlings are now being monitored in a common
garden to quantify early establishment and photosyn-
thetic performance. Generalist pollinators were also
observed moving frequently between unmanipulated
flowers of different cultivars with fruits developing
soon thereafter, suggesting that hybridization events
are likely under natural conditions. Overall, these
results indicate that with few exceptions, most culti-
vars are cross-compatible and capable of producing
viable hybrid offspring.
The ability of cultivars to cross-fertilize was also
examined a different way by focusing on the parent-
age of existing invasive individuals. If these
individuals result from recent hybridization between
nearby cultivars as proposed (e.g. Vincent 2005), the
genetic contribution of each cultivar should be evident
in the invasive genotypes. Using nine microsatellite
loci (Hardiman and Culley 2007), invasive individuals
were genotyped in three populations in Ohio (OH),
Tennessee (TN), and Maryland (MD) representing
different ages of invasion. The Cincinnati, OH
population recently formed in the last 7 years and is
hypothesized to contain mostly F
1
hybrids while the
older Nashville, TN population is expected to contain
more advanced generation hybrids. Because the oldest
population occurs in Glenn Dale, MD where the
species was first introduced in the early 1900s, this
population is expected to consist largely of advanced-
generation hybrids with parentage reflecting both
original Asian genotypes and cultivars in the neigh-
boring area. To quantify cultivar composition at each
site (i.e. putative parents), samples were also collected
from cultivars planted in residential and commercial
areas surrounding each invasive population.
Cultivar identification of neighborhood trees in the
residential and commercial areas near each site was fist
assigned with GeneClass2 (Piry et al. 2004)using
Rannala and Mountain’s (1997) Bayesian method.
Results indicated that neighborhood trees always con-
sisted of a mixture of cultivars but the exact combination
differed between sites (Fig. 2). For example, ‘Bradford’
was the most common cultivar in the OH (55.1%), TN
(79.4%), and MD (8.3%), while ‘Aristocrat’ was the
second most popular tree in OH (15.4%) but was absent
from the TN and MDsites where it is more susceptible to
fireblight infection. There was also a higher proportion
of unknown cultivars in the MD neighborhood
(61.1.9%) than in OH (2.6%) or TN (11.9%), most
likely reflecting the greater diversity of Chinese geno-
types historically planted around the USDA station
(Culley and Hardiman 2007).
The relative genetic contribution of these cultivars
as well as admixture within invasive populations was
next examined at the three sites using the Bayesian
genotype clustering program Structure v2.0 (Falush
et al. 2003). This technique determines the most likely
Table 2 Percent fruit set resulting from a 3 year hand-polli-
nation study of Pyrus calleryana cultivars in a common garden
Maternal
source
Paternal source
Aristocrat Bradford Chanticleer Redspire
Aristocrat 0 100% (3) 67% (21) 60% (5)
Bradford 75% (12) 0 0% (4) 100% (4)
Chanticleer 58% (24) 81% (16) 0 70% (10)
Redspire 90% (10) 100% (8) 100% (7) 0
The upper diagonal represents fruit set with the given cultivar
as a pollen donor and the lower diagonal represents the given
cultivar as the pollen receiver. Sample sizes indicating the
number of crosses are shown in parentheses next to each
percentage value
The role of intraspecific hybridization in the evolution of invasiveness 1113
123
number of genetic populations (K) given the observed
data and assigns individuals to those populations
based on their multilocus microsatellite genotypes.
The most likely value of Kis that which maximizes
the log-likelihood of obtaining the observed sample of
multilocus genotypes. Using the admixture model
with correlated allele frequencies, we ran 20,000 steps
with a burn-in of 30,000 for each Ktested. The highest
model log-likelihood was obtained with K=11,
which corresponded to the eight cultivars and popu-
lations at the three sites. The analysis confirmed that
cultivars are genetically distinct (Fig. 3) and that the
invasive populations in Ohio, Tennessee and Mary-
land each consist of a mixture of cultivar genotypes.
Invasive individuals of a single cultivar genotype
were never detected, indicating that cultivars them-
selves are not escaping into natural sites. As expected,
there was a large number of F
1
hybrids (i.e. possessing
approximately 50% of two cultivar genotypes) in the
youngest Ohio population and greater recombination
and advanced generation hybrids (containing geno-
typic contributions from 3 or more cultivars) in the
older populations. In Ohio, most of the F
1
individuals
resulted from crosses between ‘Bradford’ and ‘Aris-
tocrat’, which were also the most common cultivars
planted in the surrounding residential neighborhood
(Fig. 2). In Tennessee, many hybrids exhibited ‘Brad-
ford’ parentage, consistent with the popularity of that
(a) (b) (c)
N=78 N=59 N=36
55%
15%
13%
10 %79%
12%
7%
2%
61%
25%
8%
6%
3%
3%
1%
Aristocrat Bradf ord Chanticleer Redspire Ca pital Fa ur ie Unknown
Fig. 2 Proportion of cultivars growing in residential and
commercial areas surrounding invasive populations in (a)
Ohio, (b) Tennessee, and (c) Maryland. Sample sizes are
shown below each graph. Unknown individuals could not be
matched to genotypes of 13 reference cultivars and may
represent cultivars yet to be identified
Fig. 3 Graphical output from structure in which each vertical
bar represents an individual tree for (a) multiple individuals of
known cultivars and (b) invasive populations in Ohio
(N=102), Tennessee (N=60) and Maryland (N=97). The
color of the bar indicates the cultivar group to which an
individual has been placed, and the extent of the color is the
percent of the genotype attributable to the corresponding
group. Individuals containing approximately half of each
genotype of two cultivars are considered F
1
plants. Cultivars
include ‘Aristocrat’ (A), ‘Bradford’ (B), ‘Redspire’ (R),
‘Capital’ (C), ‘Chanticleer’ (Ch), and ‘Autumn Blaze’ (AB)
1114 T. M. Culley, N. A. Hardiman
123
cultivar in the surrounding neighborhood. Maryland
populations contained a greater number of unknown
genotypes, which may represent additional unknown
cultivars or Asian genotypes (Culley and Hardiman,
2007). Overall, these data indicate that a diverse
combination of cultivar genotypes contribute to the
invasive populations, consistent with intraspecific
hybridization.
Conclusions and future directions
As indicated by the our ongoing study of the Callery
Pear, intraspecific hybridization can be an important
stimulus for the evolution of invasiveness provided
that specific conditions are met. Namely, at least two
introductions of genetically distinct populations must
occur in the same locality with subsequent hybrid-
ization of different individuals, resulting in novel
genotypic combinations with adaptive potential in the
new environment. Just as only a small number of
introduced species become invasive, intraspecific
hybridization will not lead to invasiveness in every
case (e.g. Wolfe et al. 2007). With the increasing
globalization of our world today, however, introduc-
tions of new populations and species continue, thus
increasing the probability of future hybridization
events. Given the high economic and ecological costs
associated with only a few invasive species (Pimentel
et al. 2000,2005), it is crucial that we identify
evolutionary processes that facilitate invasiveness so
as to prevent and control future problem species.
We are still at an early stage in understanding how
frequently intraspecific hybridization leads to inva-
siveness but the cases identified so far (Lavergne and
Molofsky 2004,2007; Williams et al. 2005,2007;
Culley and Hardiman 2007) indicate that it can occur in
several unrelated species. Even studies in which
evidence does not support intraspecific hybridization
(e.g. Wolfe et al. 2007) are still valuable as they
provide the context for establishing the overall
frequency. Additional investigations are now needed
to determine the extent and effect of intraspecific
hybridization in introduced and native plant taxa.
These studies must take into consideration that intra-
specific hybridization may proceed alongside other
processes promoting invasiveness such as polyploidy
(Schierenbeck and Aı
¨nouche 2006), interspecific
hybridization (Ellstrand and Schierenbeck 2000) and
escape from native predators or competitors (Sakai
et al. 2001). In invasive Spartina in California for
example, both intra- and interspecific hybridization
have been documented (Aı
¨nouche et al. 2003; Bando
2005). Some introduced species also may possess
preadaptive traits that are not a product of hybridiza-
tion per se but rather act to enhance invasiveness once
hybridization produces recombinant genotypes. For
example, P. calleryana in its native Asian range is
tolerant of diverse soil moisture conditions, which is
consistent with its ability to invade wet, mesic or dry
sites in the United States (Culley and Hardiman 2007).
In addition, reed canary grass undergoes intraspecific
hybridization (Merigliano and Lesica 1998; Lavergne
and Molofsky 2007) and typically exhibits high
competitive growth especially in nutrient rich habitats
(Lavergne and Molofsky 2004).
The propensity for a species to undergo intraspe-
cific hybridization will depend in part on traits and
processes that promote outcrossing. Breeding systems
such as dicliny, heterostyly or self-incompatibility
maximize fertilization between genetically distinct
individuals and thus increase the potential for hybrid-
ization. Although such systems may induce an Allee
effect in an initial population, the effect may quickly
disappear as outcrossing occurs between populations,
especially with the contribution of multiple introduc-
tions. For example, two plant species with strong
evidence of intraspecific hybridization are dioecious
(Schinus terebinthifolius; Williams et al. 2005,2007)
or self-incompatible (Pyrus calleryana), traits also
noted in several perennial weeds (Price and Jain 1981).
Such obligatory outcrossing is in contrast with the
traditional characterization of invasive species as self-
compatible (Baker 1974; Price and Jain 1981; Roy
1990; but see Novak and Mack 2005). This suggests
that species in which outcrossing is actively promoted
may be more likely to become invasive through
intraspecific hybridization than selfing species. In
P. calleryana, different bee species indiscriminately
visit flowers and often carry pollen between neigh-
boring cultivars, resulting in hybrid fruit set. Finally,
intraspecific hybridization will also be enhanced by
animal-mediated seed dispersal which often results in
seeds being carried long distances (Schiffman 1997),
thus promoting movement of novel recombinant
genotypes across the landscape. In P. calleryana,
most seedlings bear no genetic similarity to nearby
mature trees, presumably because these seedlings
The role of intraspecific hybridization in the evolution of invasiveness 1115
123
originated from seeds defecated indiscriminately as
birds forage across an area. Overall, traits that promote
outcrossing and gene flow have the potential to
produce intraspecific hybridization, if combined with
multiple introductions of genetically distinct individ-
uals. Consequently, it is important to closely examine
the reproductive biology of introduced species when
determining their potential for spread.
Future investigations of intraspecific hybridization
should especially consider the impactof horticulture and
agriculture on plant invasions, which can facilitate
multiple introductions of cultivated plant species.
Compared to natural processes, commercialization
allows these species to spread more quickly and
extensively because genetically differentiated cultivars
can be mass-produced and sold nationwide to gardeners
and landscapers who plant them in combination within a
variety of locations. In addition, the horticultural
industry is largely driven by consumer demand for
unique and novel plant species, which in turn facilitates
introduction of non-native species. Although the vast
majority of horticulturally important plant species never
become invasive (Reichard and White 2001), there are
cases of invading species that have a horticultural origin,
including honeysuckle (Amur spp.; Luken and Thieret
1996; Schierenbeck 2004), English Ivy (Hedera spp.;
Clarke et al. 2006) and Brazilian peppertree (Schinus
terebinthifolius; Williams et al. 2005,2007). In some
cases, invasive genotypes may originate unintentionally
after crossing occurs between different cultivars planted
in the landscape, as in P. calleryana (described above)
and Lythrum salicaria (Anderson and Ascher 1993).
Cultivar selection prior to introduction itself can also
increase invasiveness, as with selection for showy
appearance and dense foliage of Japanese Ardisia
crenata in the United States (Kitajima et al. 2006).
Consequently, some plant breeders have begun exam-
ining individual cultivars for invasive traits (Anderson
et al. 2006), such as abundant seed set and high seed
germination (e.g. Lehrer et al. 2006;WilsonandKnox
2006). The next stepis to determine if crossing between
cultivars of particular species results in potentially
invasive genotypes before they are released. In some
cases, sterile cultivars of highly popular species are
being developed (Li et al. 2004) and voluntary initia-
tives have been proposed to minimize plant invasions
(Burt et al. 2007).
Finally, the importance of intraspecific hybridiza-
tion in species invasions has several implications for
management. Control plans of invasive species must
first determine if intraspecific hybridization is present
and if so, every effort must be made to prevent
introduction of new genotypes into an area. Because
genotypes may be morphologically indistinguishable
from one another, land managers need to work
closely with scientists to use genetic techniques to
identify problematic genotypes for early removal. In
cases where different genotypes have already been
widely released into the environment, as with the
popular Callery Pear, it is unrealistic that the invasive
species will ever be completely eradicated and
therefore control measures that prevent formation of
new populations will be most effective. These should
involve the following: (1) quick removal of invasive
populations in natural areas after their detection;
(2) replacement of cultivated parental plants with
non-invasive species whenever possible, especially in
locations near natural areas; (3) consideration of
voluntary self-regulation or legislative measures that
minimize introduction of new, compatible genotypes;
(4) education of the general public on the importance
of using suitable alternatives. To this end, the
development of completely sterile cultivars of
highly popular horticultural species may reduce the
number of parental genotypes capable of spawning
invasive populations while still providing a profitable
alternative for the nursery industry. Ultimately,
understanding how invasiveness may evolve in light
of intraspecific hybridization is of paramount impor-
tance to preventing or controlling invasive species
before they exert substantial ecological and economic
impacts on the environment.
Acknowledgments The authors thank D. Ayers, N. Ellstrand
and K. Schierenbeck for organizing the symposium that led to this
special issue, as well as enlightening discussionsand comments on
the manuscript. K. Manbeck provided an invaluable perspective
from the green industry while M. Klooster, S. Rogstad and two
anonymous reviewers provided helpful suggestions that greatly
improved the manuscript. This research was supported by a grant
from the US Department of Agriculture, Cooperative State
Research, Education, and Extension Service, to T.M.C. (USDA
CREES 06-35320-16565).
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