Download Phylogeography, Haplotype Trees, and Invasive

Ó 2003 The American Genetic Association
Journal of Heredity 2003:94(3):197–204
DOI: 10.1093/jhered/esg060
THE WILHELMINE E. KEY 2002 INVITATIONAL LECTURE
Phylogeography, Haplotype Trees, and
Invasive Plant Species
B. A. SCHAAL, J. F. GASKIN,
AND
A. L. CAICEDO
From the Department of Biology, Washington University, St. Louis, MO 63130 (Schaal and Caicedo) and USDA Agricultural
Research Service, Northern Plains Agricultural Research Laboratory, 1500 N. Central Avenue, Sidney, MT 59270 (Gaskin).
Address correspondence to Barbara A. Schaal at the address above.
Barbara A. Schaal is Spencer T. Olin Professor of Biology at
Washington University in St. Louis. She received her Ph.D.
in population biology from Yale University and did
postdoctoral work at the University of Georgia, and she
was on the faculty at the University of Houston and Ohio
State University before moving to Washington University in
1980. Dr. Schaal was president of the Botanical Society of
America and has served as executive vice president of the
Society for the Study of Evolution, for which she is currently
president-elect. Additionally, she has served on editorial
boards of numerous journals and was chair of the
Department of Biology, Washington University. Dr Schaal
currently serves as chair of the Scientific Advisory Council of
the Center for Plant Conservation, chair of the NRC
Committee on Agriculture, Biotechnology, Health and the
Environment, and as a member of the board of trustees,
Missouri chapter of The Nature Conservancy. She is a fellow
of the American Association for the Advancement of
Science, a John Simon Guggenheim Fellow, and a member
of the U.S. National Academy of Sciences.
Abstract
The distribution of genetic variants in plant populations is strongly affected both by current patterns of microevolutionary
forces, such as gene flow and selection, and by the phylogenetic history of populations and species. Understanding the
interplay of shared history and current evolutionary events is particularly confounding in plants due to the reticulating nature
of gene exchange between diverging lineages. Certain gene sequences provide historically ordered neutral molecular
variation that can be converted to gene genealogies which trace the evolutionary relationships among haplotypes (alleles).
Gene genealogies can be used to understand the evolution of specific DNA sequences and relate sequence variation to plant
phenotype. For example, in a study of the RPS2 gene in Arabidopsis thaliana, resistant phenotypes clustered in one portion of
the gene tree. The field of phylogeography examines the distribution of allele genealogies in an explicit geographical context
and, when coupled with a nested clade analysis, can provide insight into historical processes such as range expansion, gene
flow, and genetic drift. A phylogeographical approach offers insight into practical issues as well. Here we show how
haplotype trees can address the origins of invasive plants, one of the greatest global threats to biodiversity. A study of the
geographical diversity of haplotypes in invasive Phragmites populations in the United States indicates that invasiveness is due
to the colonization and spread of distinct genotypes from Europe (Saltonstall 2002). Likewise, a phylogeographical analysis
of Tamarix populations indicates that hybridization events between formerly isolated species of Eurasia have produced the
most common genotype of the second-worst invasive plant species in the United States.
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Journal of Heredity 2003:94(3)
There have been numerous advances in the study of
evolutionary biology over the past two decades. Clearly
one of the most important developments has been the use of
DNA sequences and markers for understanding both the
patterns and processes of evolution. Associated with the
application of molecular techniques have been both
conceptual and analytical advances. At the population level,
the use of DNA sequences to infer past evolutionary
processes has been enhanced by John Avise’s concept of
phylogeography, which examines the distribution of genealogical lineages of specific DNA sequences in a geographical
context. Phylogeographic approaches offer a way of determining the types of contemporary and historical processes
that have influenced the current geographic distribution of
variation (Avise 2000). The separation of a single lineage into
two separate lineages is perhaps the most interesting and
critical stage of genetic divergence, since in some cases it is
a prelude to speciation. In plants, lineage diversification has
been particularly difficult to analyze because of the reticulating, hybridizing nature of plant species.
Reconstructions of the genealogical relationships between genes through the use of haplotype networks or trees
can be used to analyze evolutionary processes at the time of
lineage separation. As lineages diverge, the assumptions of
population genetics that apply to processes within populations no longer hold. Such assumptions include equilibrium
between genetic drift and gene flow, an equilibrium only
rarely observed in plants, if at all. At the same time, the
assumptions of cladistics are not valid at the time of lineage
diversification. To apply, cladistic analysis lineages must be
isolated and nonreticulating. Plants, of course, are notorious for their ability to hybridize even between lineages that
have been separated over millions of years. Thus studies of
gene genealogies are particularly important in plants, where
below the species level mating is nearly always nonrandom,
and where above the species level hybridization is frequent.
Reconstructions of gene genealogies have great potential
for advancing our understanding of plant evolution; they
are a powerful tool that enables the testing of numerous
population-level hypotheses and they provide insight into
current processes that greatly affect biodiversity.
Construction of Haplotype Trees
The use of molecular-level data has become ubiquitous in
intraspecific studies in the past two decades. However, molecular population-level studies in plants still remain much
less common than similar studies in animals, primarily due
to the difficulty of finding genetic markers with appropriate intraspecific levels of polymorphism (Schaal et al. 1998).
Many plant studies have turned to genome-wide markers
such as random amplified polymorphic DNA (RAPD) and
amplified fragment length polymorphism (AFLP), but these
data cannot be historically ordered, which precludes the
construction of gene trees. The dearth of studies has had
a negative impact on the application of analytical tools
available for ordered data that are otherwise common in
animal intraspecific studies. This impact has been felt
198
especially in the field of phylogeography, where plant studies are far outnumbered by those in animals (Avise 2000;
Cruzan and Templeton 2000). The last 5 years, however,
have seen an increase in the identification of molecular
markers in plants that present variation at the intraspecific
level, in the nuclear genome (e.g., Gaskin and Schaal 2002;
Olsen and Schaal 1999; Strand et al. 1997), and in the
chloroplast (e.g., Maskas and Cruzan 2000) and mitochondrial genomes (e.g., Chiang et al. 2001). Thus the construction
of intraspecific phylogenies for plant groups is becoming
more common and important. Moreover, the use of these
phylogenies is allowing us to understand in greater detail the
historical and population processes that have governed the
evolution of plants, especially those that greatly affect human
affairs through agriculture or habitat degradation.
The properties of genetic relationships at the population
level have been reviewed extensively (Crandall et al. 1994;
Posada and Crandall 2001; Templeton et al. 1992). The main
aspects in which intraspecific genetic relationships differ
from those between species are the following:
1. There is a lower amount of divergence between
haplotypes.
2. Ancestral haplotypes usually remain within the species.
3. Single haplotypes can give rise to many others, leading to
multifurcations.
4. There is a greater possibility of recombination creating
homoplasious relationships (see Posada and Crandall
2001).
Because of these four properties, networks, rather than the
bifurcating trees used for between-species comparisons, are
the most appropriate way to represent the relationships
within a species.
As the use of networks has proliferated in intraspecific
studies, the terminology used to refer to them has grown
slightly confusing. We adopt the terminology used by Posada
and Crandall (2001). Within this classification scheme, a true
gene genealogy is a representation of the relationship of all
genes (at a particular locus) present in all individuals in
a sample. To determine a gene genealogy, pedigree data of
the individuals is necessary. This is the only way to determine
the true relationship between genes borne by individuals with
the same haplotype. Pedigree information is generally
unavailable for most population samples; however, within
a sample of genes from several individuals, we can generally
distinguish the relationship betweens genes differing by
mutations. Genes at a locus that differ by mutations are
known as alleles or haplotypes. Thus the depiction of
relationships between alleles or haplotypes within a species is
known as a haplotype or allele tree or network.
There are several methods for constructing the network
relationship between haplotypes in a sample (reviewed by
Posada and Crandall 2001). Determination of which method
is appropriate is an area of active debate. We have generally
found that in our datasets, which consist primarily of DNA
sequences, the levels of divergence and homoplasy are low
enough that the network can be built by hand following
a maximum parsimony criterion of minimizing the number
Schaal et al.
of mutations between haplotypes. Network construction can
also be greatly aided by TCS (Clement et al. 2000), a program
that uses statistical parsimony to estimate relationships between haplotypes. Statistical parsimony was developed by
Templeton et al. (1992) to allow the application of maximum
parsimony to intraspecific phylogenies. Under statistical
parsimony, the number of differences between haplotypes
that are due to a sequence of single mutations at each site,
with 95% confidence, are calculated. This number is known
as the limits of parsimony, and haplotypes differing by
a greater number of mutations will not be connected, as their
true relationship is more likely to be obscured by homoplasy
(Templeton et al. 1992). All haplotypes within the limits of
parsimony are connected, and the final network gives an
immediate visual representation of mutations distinguishing
any pair of alleles.
A simple example of how to construct a haplotype tree
and some of the types of information that can be obtained
from this representation can be seen in a study of RPS2
variation in Arabidopsis thaliana (Caicedo et al. 1999). RPS2 is
a gene involved in the recognition of a pathogenic bacterium,
Pseudomonas syringae pv. tomato. Functional alleles of RPS2
confer resistance to strains of P. syringae pv. tomato that carry
the avrRpt2 allele. RPS2 was sequenced in 17 accessions of
A. thaliana and seven distinct haplotypes were found. In this
case, a complete absence of homoplasy made it very easy to
deduce the haplotype tree relating these alleles. Figure 1
shows the most parsimonious relationship between haplotypes. The tree is not rooted. Although rooting for an
intraspecific tree is possible (discussed in Castelloe and
Templeton 1994), in many cases rooting is unnecessary for
the types of inferences that need to be made. Some studies
that reconstruct population history will require rooting of
an intraspecific tree. In the case of RPS2, we wanted to
determine the relationships between resistant and susceptible
alleles rather than a historical reconstruction. Among our
sampled haplotypes, 36 polymorphic sites were found. The
results showed varying degrees of divergence between RPS2
alleles in A. thaliana accessions. A significantly high level of
amino acid replacement substitutions were found to cluster
together on the tree, many leading to alternative alleles that
still conferred resistance to P. syringae expressing avrRpt2.
This indicated that certain nonsynonymous mutations did
not alter the resistance functionality of the gene. An
interesting finding was that all alleles found conferring
resistance were closely related to each other. However, this
cluster also included susceptible types. Susceptible alleles, on
the other hand, could be widely divergent from the resistant
haplotypes and each other.
This example illustrates how haplotype trees can provide
insight into the evolution of functional genes. Although it
has not been exploited much in plants, further insights in
functional gene evolution can be obtained by incorporating
analytical techniques developed for intraspecific phylogenies.
Haplotype trees in conjunction with phenotypic data and
nested cladistic analysis (Templeton 1988; Templeton et al.
1987) can be used to deduce associations between sequence
and phenotypic effect (Templeton 1995; Templeton and
Phylogeography, Haplotype Trees, and Invasive Plant Species
Figure 1. Haplotype of the RPS2 gene in A. thaliana.
Conservative a.a. change, c; nonconservative a.a. change, nc.
Sing 1993; Templeton et al. 1987, 1988, 1992). There is
justifiable concern over the lack of correlation between
neutral markers and the phenotype in question (Reed and
Frankham 2001), though that concern should be diluted
for genealogies that coalesce further into the past. As more
functional genes are identified and sequenced, this type of
analysis might become more useful, especially for agriculturally important traits.
The most frequent use of haplotype trees so far has been
to obtain information on historical processes. For example,
a number of excellent studies have established the migration
routes of important tree species from Pleistocene refugia in
Europe (e.g., Lumaret et al. 2002; Petit et al. 2002; Taberlet
et al. 1998). Other studies have documented the origin of
important crops species (Olsen 2000) and examined the
colonization and diversification of plant species in Asia (Ge
et al. 2002; Huang et al. 2001). Below we discuss how
haplotype trees and phylogeographic analyses have been
used to examine the origin of invasive plants, one of the
greatest threats to the biodiversity of the United States and
other regions of the world.
Invasive Species
The invasion of introduced species into regions of the world
has altered natural environments and severely threatened
native biodiversity. In many cases the species introduced
is noninvasive in its native land, while in other examples
a species may have recently become invasive. The root causes
of invasiveness are not clear and probably represent a
different suite of traits for each species (e.g., Baker 1965;
Williamson 1999). Causes can include intrinsic factors, such
as high seed set, or extrinsic factors, such as a loss of competitors or herbivores. A less studied aspect of invasive species
has been their underlying genetic structure. When a species
is transferred to new region, multiple genotypes are often
introduced, perhaps from different regions that are isolated,
and thus genetic recombination and reassortment may be
a factor affecting invasiveness.
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Journal of Heredity 2003:94(3)
Figure 2. Haplotype network of two noncoding chloroplast
regions from P. australis. Gray ovals represent haplotypes
recovered. Small black squares represent inferred haplotypes
not recovered in the sample. Each link between haplotypes
corresponds to one mutational difference, with indels coded as
single characters. Native North American haplotypes are
indicated by brackets. The invasive haplotype M, which is
discussed in the text, is in the large circle.
If it is the duty of systematists and population biologists
to apply their skills toward critical ecological problems, along
with attaining fundamental knowledge of evolutionary
events, then the current problem of plant species invasion
warrants substantial attention. Invasion of nonnative species
into natural areas ranks second behind only habitat destruction as the largest ecological disaster worldwide (Wilson
1997). Of the 972 plants and animals listed by the U.S.
Endangered Species Act, approximately 400 are at risk
primarily due to competition from and predation by nonnative species (Stein and Flack 1996). For these reasons, the
control of selected invasives is becoming an integral part
of ecosystem stewardship. Methods of controlling invasive
plants include manual removal, fire, herbicides, biological
control, and legislation concerning the importation and use
of certain plant species. But control efforts often begin
before there is a basic understanding of the invasion. Exactly
which species is invading? What genotypes of the species
are present in an invasion and where did they come from?
Which other species, genera, and families are most closely
related to the invasive species? Is there gene flow between
the invasive and closely related native species? All of these
questions can be addressed by molecular studies, and in
particular by the construction of haplotype tress and phylogeographical analyses.
Case Studies: Phylogeography of Plant
Invasions
Phragmites
The common reed (Phragmites australis) is a tall (up to 4 m)
perennial grass found in marshes and along river and lake
edges. The species is cosmopolitan, but in the last 150 years it
has expanded its distribution and increased its density
dramatically in the United States. The success of this species
was hypothesized to have been due to human-mediated disturbance and pollution, but an alternate explanation focuses
on the introduction of an aggressive, cryptic, nonnative genotype. In an exemplary study, Saltonstall (2002) sequenced two
200
noncoding chloroplast regions of 345 plants worldwide,
including herbarium samples collected before and after the
range expansion in 1910. She found 27 haplotypes worldwide,
and the older North American haplotypes were quite
differentiated from those found in other parts of the world
(Figure 2). A very common ancestral haplotype (M) was
found throughout Europe and continental Asia. Before 1910,
this haplotype M was detected just four times (6.4%) in the
United States, and only along the coast of New England.
Since 1960, this haplotype has expanded its range across the
entire United States and is now the most widespread and
common (61.5%) genotype found in North America. There
has been a corresponding drop in diversity of the native P.
australis genotypes during the last century. Saltonstall also
broke down her samples into 20-year intervals for a portion
of the New England area, illustrating the haplotype
distribution pattern over time. From mapped distributions,
one can conclude that haplotype M has found its way from
port areas to more inland locations, becoming essentially the
only genotype in the area as the native genotypes appear to
become regionally extinct. This study illustrates how cryptic
invaders can be just as devastating to native terrestrial communities as easily recognized invaders, and illustrates the
utility of phylogeographic studies in elucidating historical
evolutionary events. The presence of a cryptic invasion may
indicate that this haplotype will be an eternal dominant of
many wetland areas, or that populations will have to be
genotyped as native or exotic prior to any control efforts.
Polysiphonia
A second phylogeographic study looked at an invasion of
a red alga. Marine invasions are especially numerous due to
the increase in ocean transport and the associated ballast
water used by ships. The number of invasions may be
underestimated because of the difficulty in distinguishing
morphologically similar sibling species. The red alga
Polysiphonia harveyi is considered exotic on the Atlantic coast
of Europe, showing up in various locations there in the last
two centuries, and conspecific populations are known from
Atlantic North America and Japan. Typical of algal invasives,
P. harveyi is eurythermal, weedy, and attaches to artificial
substrata. McIvor et al. (2001) looked at rbcL sequence
analysis, karyology, and interbreeding data from P. harveyi and
various congeners in the Pacific and North Atlantic Oceans
to determine how this species first got to the British Isles.
Possible invasion origins included the Pacific Ocean near
Japan, which contains specimens morphologically similar to
the invasive, or from the eastern coast of North America.
Alternatively the North American specimens may have been
the result of an introduction from the Pacific. Six rbcL
haplotypes were identified, all interfertile and similar in chromosome number, with the four most divergent haplotypes
observed in Japan. One of the other two haplotypes was
distributed on the eastern and western coasts of North
America and in New Zealand, and the last haplotype was
found exclusively on the Atlantic coast of Europe and Nova
Scotia. The inability to match putative invasive haplotypes
Schaal et al.
with native haplotypes might have been solved with more
intensive sampling, but the utility of sequence markers that
vary at the population level is still clear. Once again we see
that cryptic species and genotypes can make it difficult to
estimate the magnitude and number of invasions without the
use of molecular systematic and phylogeographic analyses.
Tamarix
Several species of the genus Tamarix L. (common name
saltcedar or tamarisk, family Tamaricaceae) are, as a group,
considered one of the worst plant invasions in the United
States, exceeded only by purple loosestrife (Lythrum salicaria)
(Stein and Flack 1996). Tamarix is an Old World genus of
approximately 54 shrub and tree species found in salty, dry,
or riparian habitats.
Eight to 12 species were brought to the United States
from southern Europe or Asia in the 1800s to be used for
shade and erosion control (Baum 1967), and a subset of these
species has taken over more than 600,000 riparian and
wetland hectares (Brotherson and Field 1987). This invasion
is expanding by 18,000 hectares/year (Di Tomaso 1998)
throughout the western United States, including major river
systems and national parks. In the United States, Tamarix
escaped nearly all of its biological enemies (DeLoach et al.
2000) and has proven difficult to control on a large scale by
either manual or chemical methods.
Researchers at the U.S. Department of Agriculture
(Agricultural Research Service) are currently searching for
and testing candidate biological control insects as an
alternative means of suppressing this invasion (DeLoach
and Tracy 1997; DeLoach et al. 2000). Initial biological
control tests of the saltcedar leaf beetle (Diorhabda elongata)
show differential survival on what appear to be a single
species of Tamarix collected from different regions of the
United States and grown in common garden plots (DeLoach
and Tracy 1997), perhaps suggesting that certain genotypes
are more resistant to control agents. Many species of Tamarix
are widespread in Eurasia (Baum 1978), and it is unlikely that
all of the genotypes of any one species were imported to the
United States. For these reasons, biological control researchers wanted to know how many genotypes are represented in
the U.S. invasion, and to what degree we can pinpoint their
Eurasian origins.
The most dominant U.S. Tamarix invasion consists of
two morphologically similar species: T. chinensis, native to
China, Mongolia, and Japan; and T. ramosissima, which is
widespread from eastern Turkey to Korea (Baum 1978). The
ranges of these two species putatively overlap for approximately 4,200 km across China and Korea.
A total of 269 vouchered DNA samples of Tamarix were
collected from the western U.S. (155 plants) and Eurasian
native populations of T. chinensis and T. ramosissima (114
plants), with one to eight individuals per population (Gaskin
and Schaal 2002). An intron of the phosphoenolpyruvate
carboxylase gene, approximately 900 bases in length, was
sequenced, and this contained 144 variable sites in the
species investigated.
Phylogeography, Haplotype Trees, and Invasive Plant Species
A total of 58 haplotypes were found among the 269
individuals (a total of 538 alleles). All populations except one
in China (T. chinensis) had more than one haplotype represented, and some had up to 11 different haplotypes in six
plants. The four haplotypes common to the United States
and Asia were used to manually construct a maximum
parsimony gene genealogy or minimum spanning network
(Figure 3), which represents the mutational relationships
among the haplotypes.
In the native Eurasian range, by far the most common
genotypic combinations were 1/1 and 2/2, which belong
to T. ramosissima and T. chinensis, respectively (Figure 3). In
contrast, within the U.S. invasion these genotypes were
the second and third most common. The most common
genotype in the United States was 1/2, a morphologically
cryptic hybrid of T. ramosissima and T. chinensis which was not
detected in Eurasia. Even though both species are putatively
found all across China (Baum 1978), the 1/1 genotype was
found exclusively west of central China and the 2/2 genotype
exclusively east of central China (Figure 3). In Asia there
are no known physical barriers between the two species
except their putative edaphic affinities (Baum 1978), and
in the United States the T. chinensis (2/2) and T. ramosissima
(1/1) genotypes were found growing together in five populations as close as 2 m from each other on disturbed homogenous soil.
Haplotype 12 was the third most common in the United
States, found throughout the invasion, and it differed from
haplotype 1 by 14 mutations, and was found only once
in Eurasia in a homozygous plant (genotype 12/12) in
Azerbaijan. The 2/12 genotype, found only in the United
States, may be another novel hybrid (though perhaps a very
rare one) given the disjunct native range of the haplotypes
(China and Azerbaijan, respectively). Haplotype 7 was the
only other T. ramosissima or T. chinensis haplotype common to
the United States and Eurasia. It differs from haplotype 1 by
five mutations, and was found in only one population in
Idaho. In Eurasia it was found in the Republics of Georgia,
Turkmenistan, and Kazakstan.
The smallest native region that contained all of the
detected T. ramosissima haplotypes common to Eurasia and
the United States (1, 7, and 12) consists of the Republics of
Georgia and Azerbaijan. Designating the native range of
invasive genotypes has practical applications for biological
control agent searches involving pest species with a widespread native distribution, but would require more extensive
sampling than was provided in this study.
These data, taken in total, indicate little if any hybridization among T. ramosissima and T. chinensis in their
native range, even though their ranges putatively overlap.
The 1/2 genotype may certainly occur in these areas, but
given the 4200 km overlap of the two species’ ranges, it was
surprising not to find T. ramosissima haplotypes in the eastern
half of China, where they putatively exist. In contrast, there
was extensive hybridization among two of the invasive
Tamarix species within the United States. The 1/2 genotype,
representing a T. chinensis 3 T. ramosissima hybrid, was the
most common plant found in the invasion, ranging from
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Journal of Heredity 2003:94(3)
Figure 3. Distribution maps and network for haplotypes of T. ramosissima and T. chinensis common to the United States and Asia.
Each link between haplotypes corresponds to one mutational difference.
Oklahoma to Washington to California. Less extensive
hybrids exist in the invasion, involving combinations of T.
ramosissima and T. chinensis with other invasive species such as
T. parviflora and T. gallica. The abundance of cryptic hybrids
helps explain why identification of species in the United
States using morphology has been, and will continue to be,
problematic.
202
What do these results mean for the biological control of
Tamarix? An effective and safe control agent should have
high host specificity, the result of a shared evolutionary
history. The hybrid Tamarix genotypes of the United States
may be as little as 200 years old (Horton 1964) and thus have
essentially no shared evolutionary history with any genotypespecific predators or diseases. The presence of a successful
Schaal et al.
novel hybrid in the U.S. invasion may potentially confound
biological control results, depending on the control agent’s
level of host specificity. Moreover, the results reported here
allowed the circumscription of a native area that contains all
detected T. ramosissima haplotypes common to both the
United States and Eurasia, information that may help focus
future biological control agent searches. The widespread
presence of hybrid Tamarix in its introduced range serves as
an additional warning for how continued accidental or
intentional importation of plant species can unexpectedly
alter the genotypic composition of naturalized populations
and potentially contribute to the ecological devastation
caused by exotic species invasion.
Conclusion
Haplotype trees and phylogeographic analysis have provided
insights into many areas of evolutionary biology and holds
promise for addressing practical issues as well. The studies of
invasive plants discussed here are the beginning of a new
understanding of the genetic structure of invasive plants. The
scenarios of invasions constructed from morphological
analysis can be misleading and it is clear that in some critical
examples, the identity of the invasive plant has been poorly
or incorrectly characterized. In fact, the ability to control an
invasive plant may rely on understanding its origin and genetic structure. As more genetic data are forthcoming, we
hope that some general patterns will emerge for the evolutionary history of invasive plant species. Such an understanding will increase our ability to confront and control the
ongoing ecological disasters created by nonnative plants.
Acknowledgments
This lecture was delivered at the 2002 American Genetic Association Annual
Symposium on Molecular Evolutionary Genetics, which was organized by
Dr. Philip Hedrick and held at Arizona State University, Tempe, AZ, March
22–24, 2002. The paper was supported by grants from the National Science
Foundation and U.S. Department of Agriculture, and by a Guggenheim
Fellowship (to B.A.S.). J.F.G. was also supported by an EPA STAR
Fellowship, the National Geographic Society, and the Mellon Foundation’s
support of Missouri Botanical Garden graduate students.
Phylogeography, Haplotype Trees, and Invasive Plant Species
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Corresponding Editor: Philip Hedrick