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SYNTHESIS
Crops gone wild: evolution of weeds and invasives
from domesticated ancestors
Norman C. Ellstrand,
1
Sylvia M. Heredia,
1
Janet A. Leak-Garcia,
1
Joanne M. Heraty,
1
Jutta C. Burger,
2
Li Yao,
1
Sahar Nohzadeh-Malakshah
1
and Caroline E. Ridley
3
1 Department of Botany & Plant Sciences and Center for Conservation Biology, University of California, Riverside, CA, USA
2 Irvine Ranch Conservancy, Irvine, CA, USA
3 United States Environmental Protection Agency, National Center for Environmental Assessment, Arlington, VA, USA
Introduction
Since the advent of agriculture humans have encountered
plants that have frustrated their goal to manage their
environment. Today, we call the plant pests that interfere
with agriculture ‘weeds’. In the last few centuries, humans
have taken an increasing interest in preserving and other-
wise maintaining the biodiversity of more ‘natural’ [i.e.,
‘less managed’ (Kaus and Go
´mez Pompa 1992)] commu-
nities. Here, too, plant pests frustrate human intentions.
In such situations, these plants are called ‘invasives’.
Weeds and invasives are problematic plants at ends of a
continuum of how intensively humans manage an ecosys-
tem, with manicured lawns and cultivated croplands at
one end, through forest plantations and rangelands, to
natural, deliberately lightly managed, areas at the other
end. Thus, the distinction between weeds and invasives,
though often clear, is occasionally fuzzy or arbitrary.
Some plants can become weeds and/or invasives with
the appropriate ecological opportunity (e.g., colonizing a
region where their primary predator is absent) and with-
out any genetic change. But an increasing body of
research has revealed that some plants have evolved to
become pests. Following the publication of the book, The
Genetics of Colonizing Species (Baker and Stebbins 1965),
evolutionary biologists began to focus on how weeds
might evolve (e.g., Baker 1974; de Wet and Harlan 1975;
Barrett 1983). The idea of evolution as a potential route
to invasiveness has become rapidly accepted in the last
two decades, not only for plants, but also for animals
and microbes (Blossey and No
¨tzold 1995; Ellstrand and
Schierenbeck 2000; Arnold 2006; Novak 2007; Prentis
et al. 2008; Schierenbeck and Ellstrand 2009).
With the goal of understanding whether and how
weediness and invasiveness evolve, empirical studies are
accumulating that compare problematic lineages with
their putative ancestral populations, in plants as well
as other organisms (Bossdorf et al. 2005; Dlugosch and
Parker 2008a). Some of these studies compare genetic
marker variation, often identifying changes in diversity
and population genetic structure. Other descriptive
studies compare phenotypic or ecological differences
Keywords
de-domestication, domesticate, endoferality,
exoferality, hybridization, invasive species,
rapid evolution, weed.
Correspondence
Norman C. Ellstrand, Department of Botany &
Plant Sciences and Center for Conservation
Biology, University of California, Riverside, CA
92521, USA.
Tel.: 1-951-827-4194; fax: 1-951-827-4437;
e-mail: ellstrand@ucr.edu
Received: 16 May 2010
Accepted: 21 May 2010
First published online: 14 July 2010
doi:10.1111/j.1752-4571.2010.00140.x
Abstract
The evolution of problematic plants, both weeds and invasives, is a topic of
increasing interest. Plants that have evolved from domesticated ancestors have
certain advantages for study. Because of their economic importance, domesti-
cated plants are generally well-characterized and readily available for ecogenetic
comparison with their wild descendants. Thus, the evolutionary history of crop
descendants has the potential to be reconstructed in some detail. Furthermore,
growing crop progenitors with their problematic descendants in a common
environment allows for the identification of significant evolutionary differences
that correlate with weediness or invasiveness. We sought well-established exam-
ples of invasives and weeds for which genetic and/or ethnobotanical evidence
has confirmed their evolution from domesticates. We found surprisingly few
cases, only 13. We examine our list for generalizations and then some selected
cases to reveal how plant pests have evolved from domesticates. Despite their
potential utility, crop descendants remain underexploited for evolutionary
study. Promising evolutionary research opportunities for these systems are
abundant and worthy of pursuit.
Evolutionary Applications ISSN 1752-4571
494 ª2010 Blackwell Publishing Ltd 3(2010) 494–504
(including fitness correlates or biotic interactions) of the
invasive or weed and those of putative source populations
(Bossdorf et al. 2005; Dlugosch and Parker 2008a; Keller
et al. 2009). The latter can suggest evolutionary changes,
but ‘common garden’ experiments (e.g., Barrett 1983;
Brodersen et al. 2008; Dlugosch and Parker 2008b) in both
the invaded and the native range are often necessary to dem-
onstrate genetically-based phenotypic or ecological differ-
ences between problematic organisms and their presumed
progenitors (Hierro et al. 2005; Moloney et al. 2009).
Common garden studies have revealed adaptive evolu-
tion in both weeds and invasives. A classical case is that
of a variety of barnyard grass [Echinochloa crus-galli var.
oryzicola (L.) P. Beauv.], a noxious weed that has evolved
to mimic domesticated rice (Oryza sativa L.) (Barrett
1983). Barrett (1983) grew seedlings of E. crus-galli var.
oryzicola, its progenitor, E. crus-galli var. crus-galli, and
O. sativa in a common garden experiment measuring
numerous morphological characters. Multivariate analysis
of 15 quantitative characters revealed that, in their vegeta-
tive phase, rice and its weedy mimic are not significantly
different morphologically from each other, despite being
in different genera. However, both differed significantly
from E. crus-galli var. crus-galli (see Figs 1 and 2 in
Barrett 1983). Morphological crop mimicry is an adapta-
tion that is the result of continued selection by visually-
based human weeding. Indeed, barnyard grass individuals
in Japanese rice fields that most closely resemble culti-
vated rice plants morphologically are less likely to be
removed from rice fields by hand-weeding (Ehara and
Abe 1950). Apparently, thousands of years of hand-weed-
ing rice selected for a crop mimic that is almost vegeta-
tively indistinguishable from rice.
Similar studies have been conducted for invasives. In a
common garden experiment conducted in California,
Dlugosch and Parker (2008b) compared invasive Califor-
nia populations of the shrub Canary Islands St. John’s
wort (Hypericum canariense L.) with the native popula-
tions of that species, including the genetically-determined
precise source population (Tenerife of the Canary
Islands). They found that California populations had
evolved an increased growth rate relative to the source
population. They also found a diversification of flowering
phenology of the California plants that correlated with
their latitudinal origins. Such apparently adaptive evolu-
tionary changes are not uncommon, although some
authors caution that alternative explanations (e.g., climate
matching by populations with multiple geographic ori-
gins) can account equally well for the appearance of
adaptation (Colautti et al. 2009). Only a handful of
experimental studies report no evidence for adaptive
evolution in invasives relative to their putative source
populations (Brodersen et al. 2008).
The example of Dlugosch and Parker (2008b) is excep-
tional for invasives in that the progenitor population was
precisely identified, allowing for the appropriate experi-
mental comparison of progenitor and derived genotypes.
But most often detailed information about source popula-
tions is, at best, lacking or at worst, complicated by an
unknowable number of multiple introductions to multi-
ple locations over decades with little knowledge about the
time and place of initial invasion.
Crops gone wild
A subset of weeds and invasives has evolved from domes-
ticated ancestors, presenting certain advantages for study.
We note that weeds and invasives can evolve from
domesticate plants by two different pathways (Fig. 1).
Some, like California’s weedy rye (Burger et al. 2006) are
directly descended from a crop (endoferal ancestry, sensu
Gressel 2005a), though not all endoferal plant pests neces-
sarily arise via evolutionary change. Other problematic
plants, such as Europe’s weed beet (Mu
¨cher et al. 2000;
van Dijk 2004), are descended from hybrids between a
crop and another, usually wild, taxon (exoferal ancestry,
sensu Gressel 2005a). Knowledge about crop ancestors can
illuminate the evolutionary origins of these problematic
plants.
Because of their economic importance, domesticated
plants are often extraordinarily well-studied and well-
characterized; many are among the best studied plants.
Consider this dramatic illustration: Of the hundreds of
thousands of described plant species, roughly 1% are
domesticated, but of the eight completely sequenced plant
genomes, five belong to domesticated plants (NIH Plant
Genomes Website http://www.ncbi.nlm.nih.gov/genomes/
PLANTS/PlantList.html). Likewise, domesticated species
are attractive for many evolutionary biologists. Charles
Darwin’s The Variation of Animals and Plants under
Domestication (Darwin 1868) was published less than a
decade after his On the Origin of Species by Means of
Natural Selection (Darwin 1859).
Most domesticated species are easily available for experi-
mental and descriptive genetic comparison with their wild
descendants. Thus, the history of crop descendants can
often be reconstructed in some detail. For recently appear-
ing weedy or invasive lineages, historic ethnobotanical
information, confirmed by genetic data, can assign their
geographic origin to a limited region. Similar information
can sometimes be employed to determine which crop sub-
species or varieties might have been involved in the origin
of the troublesome lineage. Furthermore, domesticated
plants are selected to be grown easily. For example, annual
crop seeds typically exhibit no dormancy (Gepts 2004).
This tractability can facilitate common garden experiments
Ellstrand et al. Evolution of weeds and invasives from domesticates
ª2010 Blackwell Publishing Ltd 3(2010) 494–504 495
to identify significant evolutionary changes that correlate
with weediness or invasiveness.
Despite these apparent advantages as well as a recent
major treatment on crop ferality (Gressel 2005b), plants
with domesticated ancestors remain a largely under-
appreciated resource for studying how problem plants
evolve. Our original motivation was to understand how
natural selection works on the descendants of domesti-
cated species so that they are able to become weedy or
invasive. We were hoping to review the literature and
accumulate a large number of examples to determine
sweeping evolutionary generalizations such as whether
natural selection results in, for example, the evolution of
locally adaptation, of increased competitive ability, or of
better dispersal. Below we identify the best studied sys-
tems, those invasive and weedy plants that have been
genetically confirmed as descendants of domesticates. We
found enough examples to identify some potential trends,
but too few to make the broad generalizations that we
had hoped for. Following our general review, we chose a
few examples that provide some insights into the work
that needs to be done on systems such as these. In partic-
ular, in our discussion, we look to the future. We identify
plant pests that are worthy of more evolutionary scrutiny.
We also consider how information from already charac-
terized crop traits might illuminate which and how genes
evolve along the route to pest status. Finally, we discuss a
number of research questions in evolutionary biology that
might be fruitfully pursued in these study systems.
Plant pests descended from domesticates
We sought cases that demonstrate the evolution of inva-
siveness and/or weediness in plants with domesticated
ancestors. We concentrated on finding the most convinc-
ing examples supported by the literature. We used four
criteria for choosing our examples:
1We considered only cases involving ancestors that are
well-domesticated taxa. Here, we define well-domesticated
taxa as those that have been intentionally cultivated (and
thus under intentional or unintentional selection) for at
least 1000 years. This initial filter limits the potential num-
ber of cases to several hundred species (Smartt and Sim-
monds 1995) while eliminating most ornamentals, timber
trees, and forage grasses. Compared to highly-domesti-
cated plants that are well-differentiated from their wild
ancestors, weakly-domesticated taxa are genetically so close
to their wild ancestors that it would be almost impossible
to determine whether their problematic descendants from
have undergone any significant evolutionary change. To
illustrate, Lantana camara is a plant famous in the nursery
trade for escaping cultivation to become a globally signifi-
cant invasive (Sharma et al. 2005). But it is not clear that
the either the horticultural varieties of L. camara or their
invasive descendants are substantially genetically different
from the original wild L. camara populations that are the
original ancestors to both.
We started out search by examining the examples in
Gressel’s (2005b) edited tour de force on crop ferality.
Likewise, Andersson and de Vicente’s (2010) book on
crops and their wild relatives provides detailed informa-
tion on what is known about feral, weedy, and invasive
lineages that have emerged from the world’s most impor-
tant crop species. Some other examples came from prior
treatments that focused on exoferality (e.g., Schierenbeck
and Ellstrand 2009 and references therein).
Crop-to-crop exo-ferality
x
Crop A
Crop A
Crop B
Crop B
Evolution
Crop-to-wild exo-ferality
Evolution
Crop A
Crop A
Wild
Wild
x
Endo-ferality
Crop A
Crop A
No evolution
Evolution
Figure 1 Pathways from domesticated plant to problem plant. Pest
plants directly descended from domesticated plants (‘endoferal’ sensu
Gressel 2005a) can occur with or without evolutionary change. Plants
that are the result of hybridization between a domesticated taxon and
another taxon (‘exoferal’ sensu Gressel 2005a) are necessarily evolu-
tionarily different than their crop progenitor(s).
Evolution of weeds and invasives from domesticates Ellstrand et al.
496 ª2010 Blackwell Publishing Ltd 3(2010) 494–504
2We required genetic or historical evidence that the
problematic lineage has evolved from a domesticated
taxon. Thus, we excluded from our list plant pests that
are known to have well-domesticated ancestors but for
which no evidence of evolutionary change has yet been
reported (e.g., invasive strawberry guava, Lowe et al.
2000).
Likewise, we excluded problematic plants that may be
descended from a crop but could also be descended from
a close wild relative of the crop. Consider the case of wild
sunflowers (Helianthus annuus) that are a substantial
weed and/or invasive problem in their native continent of
North America as well as in parts of Europe (Berville
´
et al. 2005). While they are the same species as cultivated
sunflower, it has not yet been established whether any of
the H. annuus pest populations are descended from the
crop or if they are simply descended from the North
American wild populations that were the progenitor of
the crop. Interestingly, such research on wild sunflowers
is reported to be underway (Berville
´et al. 2005). But at
the moment, we cannot include such plants in our analy-
sis.
Generally, we treated genetic evidence for a history
intertaxon hybridization (exoferality) as ipso facto
evidence that the lineage is genetically different from its
crop progenitor.
3After filtering our list through the first two criteria,
we asked whether evidence existed that the feral lineage is
indeed problematic. For example, many ornamental crops
escape from cultivation and persist (Kowarik 2005), but
only a few become problematic. In most cases, the pri-
mary literature was sufficient to answer the question [e.g.,
de Wet (1995) characterizes weedy finger millet as
‘obnoxious’]. But if the primary literature simply
described a feral lineage as a ‘weed of agriculture’, we
tried to assess its significance elsewhere, such as a major
weed and/or invasive compendium (e.g., Holm et al.
1977, 1997) or official listing as a weed or invasive by a
national or regional authority according to where the
lineage has been reported. For example, Bagavathiannan
et al. (2010) report that feral alfalfa in Canada is
evolutionarily derived from the crop, but a search of
Agriculture and Agri-Food Canada’s website (http://
www.agr.gc.ca/) revealed that that species is not a signifi-
cant pest plant in that country.
4Finally, we required evidence that the lineage is more
problematic than its crop progenitor (in the case of endo-
ferals) or each of its progenitors (in the case of exoferals),
that is, that it actually evolved to become a pest. We
avoid cases in which a wild invasive taxon has picked up
a few crop alleles via hybridization on its invasive spree
without a relevant evolutionary change to increased inva-
siveness.
We found 13 examples of plant pest lineages are des-
cended from crop progenitors. These are enumerated in
Table 1. Ten are primarily noxious weeds of agriculture,
one is an invader of nonmanaged ecosystems, and the
remaining two are both weedy and invasive. Six have an
endoferal ancestry; six are descended from hybrids
between a domesticated taxon and a wild relative. In the
remaining case, the plant pest lineage is descended from
hybrids between two cultivated taxa.
Two of the studies contributing to our list found both
a crop origin and a noncrop origin for what has been
considered to be a single taxon; that is, some, but not all,
of the populations studied had crop ancestors. With
regards to weedy rice in the United States, Londo and
Schaal (2007) found that most of the accessions geneti-
cally analyzed and compared with an array of putative
ancestors were either descended from hybrids (mostly
‘strawhull’ weedy rice) or from the crop (mostly ‘black-
hull’ weedy rice). But a single accession from California
appeared to be descended directly from the wild ancestor
O. rufipogon. In the similar study of wild artichoke thistle
(Cynara cardunculus L.) in California (Leak-Garcia 2009),
of the 12 wild populations analyzed, four were found to
have domesticated ancestry and eight were found to be
descendants of Old World wild artichoke thistle.
The list in Table 1 is diverse. The plants are annuals
and perennials whose seed and pollen are dispersed in a
variety of ways. Cultivated progenitors include both agro-
nomic and horticultural crops. Given the importance of
the grass family for human sustenance, it is not surprising
that most of the examples are from that family.
A few generalizations are apparent. With the exceptions
of rice and wheat with endoferal ancestry, all other cases
involve at least one parent that is predominantly
outcrossing; in most of the cases at least one parent is
self-incompatible. It is certainly possible that outcrossing
could facilitate the recombination of genetic diversity
between previously isolated lines, creating a burst of vari-
ation that can generate an array of phenotypes for a selec-
tive substrate (Ellstrand and Schierenbeck 2000;
Schierenbeck and Ellstrand 2009). Whether this general-
ization will hold up as more systems are studied remains
to be seen.
Also, many of the reported evolutionary changes repre-
sent de-domestication, the evolutionary loss of traits
accumulated under domestication (Gressel 2005a). Nine
of our examples show an evolutionary shift to readily dis-
persed seeds or fruits. Typically, agronomic crops that are
grown for their seeds have evolved under human selection
to be ‘nonshattering;’ that is, the infructescence or fruit
holds seeds on the plant until harvest (Gepts 2004). The
wild ancestors of those crops have the ‘shattering’ trait
for dispersal. So, too, do more than half of our examples,
Ellstrand et al. Evolution of weeds and invasives from domesticates
ª2010 Blackwell Publishing Ltd 3(2010) 494–504 497
Table 1. Invasives (I) or weeds (W) determined to have evolved from domesticated plants.
Common name
of plant pest
Progenitor(s)
Type of ferality
Source location of
crop descendant
studied
Key evolved traits
relative to crop ancestor Habit Citations
I Artichoke
thistle (in part)
Artichoke (Cynara cardunculus var. scolymus)*
Endoferal
California, USA Development of spininess, smaller more
numerous heads, leaves deeply dissected,
delayed and extended flowering period
Perennial herb Leak-Garcia (2009)
W Semi-wild
wheat
Bread wheat (Triticum aestivum)*
Endoferal
Tibet, China Easily broken rachis which facilitates
shattering
Annual grass Sun et al. (1998);
Ayal and Levy (2005)
W Weedy finger
millet
Finger millet (Eleusine coracana subsp.
coracana)* ·wild finger millet
(Eleusine coracana subsp. africana)
Exoferal
Africa Disarticulating spikelets Annual grass Hilu et al. (1978);.
de Wet et al. (1984);
de Wet (1995)
W Johnsongrass Grain sorghum (Sorghum bicolor)* ·Johnsongrass
(S. halepense)
Exoferal
Nebraska and
Texas, USA
Perennial, shattering, rhizomatous Perennial grass Morrell et al. (2005)
W Columbus
grass
Grain sorghum (Sorghum bicolor)* ·
S. propinquum
Exoferal
‘Diverse geographic
origins’
Perennial, shattering, rhizomatous Perennial grass Paterson et al. (1995)
W Forrageiro Radish (Raphanus sativus)*
Endoferal
Rio Grande do
Sul, Brazil
Resistance to ALS-inhibiting herbicides Annual or
biennial forb
Snow and
Campbell (2005)
I/W California wild
radish
Radish (Raphanus sativus)* ·Jointed
charlock (R. raphanistrum)
Exoferal
California, USA Earlier bolting, earlier flowering,
increased flower number,
unexpanded hypocotyl, increased
fruit number, increased seed number
Annual or
biennial forb
Hegde et al. (2006)
Ridley et al. (2008);
Ridley and
Ellstrand (2009)
W Weedy rice Rice (Oryza sativa japonica)*
Endoferal
Liaoning, China Shattering Annual grass Cao et al. (2006)
W ‘Blackhull’
weedy rice
Rice (Oryza sativa indica)*
Endoferal
Southeastern USA Seed dormancy, shattering Annual grass Londo and Schaal
(2007)
W Weedy rice Rice (Oryza sativa japonica)* ·Rice (O. s. indica)*
Exo-endoferal (feral lineage descended from
hybrids between two crops)
Bhutan Seed dormancy, shattering Annual grass Ishikawa et al. (2005)
W ‘Strawhull’
weedy rice
Rice (Oryza sativa indica)* ·Brownbeard rice
(O. rufipogon)
Exoferal
Southeastern USA Seed dormancy, shattering Annual grass Londo and Schaal
(2007)
I/W Weedy rye,
feral rye
Rye (Secale cereale)*
Endoferal
California and
Washington, USA
Shattering, smaller seed,
delayed flowering
Annual grass Suneson et al. (1969);
Burger et al.
(2006, 2007)
W Weed beet Sugarbeet (Beta vulgaris subsp. vulgaris)* ·
Sea beet (B. v. maritima)
Exoferal
France, Germany, Italy Shift to annual from
biennial habit, woody root
Annual forb Mu¨ cher et al. (2000);
van Dijk (2004)
*Domesticated plant.
Evolution of weeds and invasives from domesticates Ellstrand et al.
498 ª2010 Blackwell Publishing Ltd 3(2010) 494–504
indicating the evolutionary reversal of this trait in the
successful derived populations. Three of our examples
display the evolution of increased seed dormancy relative
to their crop ancestors. Some dormancy in the wild is the
rule for monocarpic plants; it has long been interpreted
as an evolutionary ‘bet-hedging’ strategy by plant evolu-
tionary ecologists (Venable 2007). As noted above,
domesticated annual crops typically have no dormancy,
an anthropogenic adaptation that permits quick and uni-
form germination when sown (Gepts 2004).
In at least one case, the key evolutionary change from
a domesticated plant to a pest did not involve the evolu-
tionary reversal of de-domestication. Cultivated radish
(Raphanus sativus L.) in southern Brazil has evolved resis-
tance to ALS-inhibiting herbicides, the herbicides of
choice in that region for no-till agriculture (Snow and
Campbell 2005). The resulting lineage called ‘forrageiro’,
is now a weed of both winter and summer crops. That
trait is not present either in the crop or in its progenitors;
thus, its evolution is not a case of de-domestication.
In contrast with the examples of divergence from
domesticated ancestors discussed above, in some of our
cases certain domesticated traits are retained in the feral
lineages. Those traits have not evolved because they pre-
sumably provide an evolutionary advantage. In particular,
several of the cases in Table 1 are successful because they
retained traits making them functional crop mimics.
Weedy rice, weedy beet, weedy rye, and semi-wild wheat
are hard to control because until they flower, they are
morphologically hard to distinguish from their relatives.
Thus, their survival is enhanced under hand-weeding.
One of the two most significant generalizations is that
the list is short. As we worked our way through the 25
contributed chapters of Crop Ferality and Volunteerism
(Gressel 2005b), we were surprised that many of the
treatments of feral plants offered only agronomic and
ecological detail, but very little insight into whether they
had evolved from their cultivated ancestors. We contend
that the other significant generalization is that there is
much to learn from these systems. With few exceptions,
our list is simply a recounting of studies that combine
data from genetic markers with ethnobotanical history to
establish that problem plants evolved from domesticates.
Even data regarding the traits that make these plants
problematic are largely superficial.
However, we found three systems worthy of deeper dis-
cussion. First, we highlight the evolution of weedy rice
because it illustrates how what is often perceived as a sin-
gle problematic lineage is, in fact, a polyphyletic set of
lineages with a diversity of evolutionary pathways that
capture the breadth of how plant pests evolve from crop
ancestors. In contrast the monophyletic story of endoferal
weedy rye has been shown to have undergone both rapid
evolutionary divergence from its progenitor as well as
regional evolutionary diversification in considerably less
than a century. We conclude with the curious case of
California wild radish, an exoferal derivative of two
species that spontaneously hybridize throughout the
world; interestingly, that hybridization has yielded a prob-
lematic lineage in only one region.
Three examples of the evolution of problematic
plants from domesticated ancestors
Weedy rice in China, the United States, and Bhutan
Native to Asia, cultivated rice (Oryza sativa japonica and
O. sativa indica) is the world’s most important food crop.
Weedy rice (O. sativa f. spontanea), also known as ‘red
rice’, has been an important weed of cultivated rice
worldwide for hundreds of years (Holm et al. 1997). Veg-
etatively, weedy rice is a crop mimic (Valverde 2005), but
its infructescence shatters, and its seeds typically exhibit
some dormancy. When it co-occurs with rice, the crop
suffers depressed yields, and, when co-harvested, the seeds
of the weed degrade the quality of the harvested grain.
Because it is the same species as cultivated rice, with
similar morphology and physiology, it is very difficult to
control by both weeding and chemical means.
The evolutionary origin of weedy rice has been contro-
versial. Its putative ancestry includes various hypotheses:
that is a wild relative of rice that has evolved crop mim-
icry, that it is descended directly from cultivated rice, or
that it is an exoferal lineage descended from hybrids
between a wild taxon and cultivated rice (Vaughan et al.
2005).
Three recent genetic studies of weedy rice have
addressed its evolutionary origins. After decades of suc-
cessful suppression, in the last decade weedy rice has
emerged as a problem in the rice fields of certain regions
of China (Cao et al. 2006). Motivated by the resurgence of
this pest, Cao et al. (2006) compared 20 DNA based SSR
markers from 30 populations of weedy rice collected from
China’s Liaoning province with those of wild O. rufipogon
as well as selected rice varieties from the two major culti-
var groups, japonica and indica. Statistical analysis of the
genetic data revealed the local Liaoning cultivar (a
japonica type) clustered within the array of weedy rice
populations. Another major Chinese japonica cultivar
showed much less affinity. The wild O. rufipogon and
domesticated indica types were even more distantly related
from the Liaoning weeds. The authors conclude ‘weedy
rice populations from Liaoning most probably originated
from Liaoning rice varieties by mutation and intervarietal
hybrids’. We agree that an intertaxon hybrid origin for
Liaoning weedy populations is unlikely; if hybridization
had occurred, it is likely that some O. rufipogon alleles
Ellstrand et al. Evolution of weeds and invasives from domesticates
ª2010 Blackwell Publishing Ltd 3(2010) 494–504 499
would have been retained in the weedy lineages in the
short time that they have been problematic.
Weedy rice has been a problematic weed of rice in the
southeastern United States for well over a century (Gealy
2005). To identify the origins of this weed Londo and
Schaal (2007) took a similar approach to Cao et al. (2006),
genetically analyzing 29 different United States weedy rice
accessions from six different states to ‘cover the entire
range of US rice culture’. For comparison, they chose 113
accessions representing a variety of indica and japonica cul-
tivars, O. rufipogon, and other wild relatives. They used data
from both sequencing a nuclear pseudo-gene (p-VATP)
and 21 DNA-based microsatellite loci. The authors used
the program STRUCTURE (Pritchard et al. 2000) to infer
the origin of the weedy rice accessions and their possible
history of hybridization. STRUCTURE uses a Bayesian
approach to examine the relationships of multilocus geno-
types of individuals by differences in allele frequency and
the nature of linkage disequilibrium. In the United States,
the vast majority of cultivars are japonica types, but
STRUCTURE analysis assigned almost all of the US weedy
accessions to two groups unallied with japonica. Black-
hulled weedy rice and a few other accessions were almost
identical to domesticated O. sativa indica var. Aus; straw-
hulled weedy rice and a few other accessions were classified
with exoferal ancestry involving hybridization of O. sativa
indica and wild O. rufipogon. A single accession appeared to
be descended directly from the wild ancestor O. rufipogon.
Clearly, most of the US weedy rice populations evolved
from the cultivated species, but it is also clear that evolu-
tion did not occur in the United States. These data as well
as other historical data (Gealy 2005) suggest that US weedy
rice has an Asian origin.
Yet another pathway for the origin of weedy rice has
been described for its populations in Bhutan (Ishikawa
et al. 2005). In that country japonica rice cultivars pre-
dominate in the highlands while indica cultivars predomi-
nate in the lowlands. Ishikawa et al. (2005) compared
lowland cultivars, highland cultivars, and weedy popula-
tions with regards to nine isozyme loci, a chloroplast gen-
ome deletion, and four microsatellite loci. They found
clear genetic differentiation between japonica and indica
cultivars, and at the same time, they found that the weedy
populations had genotypes that had both combinations of
both japonica-specific alleles and indica-specific alleles.
They report that they did not detect any alleles specific to
wild relatives. Thus, their conclusion is that the weedy
populations are lineages descended from japonica x indica
hybrids. When Gressel (2005a) named the different evolu-
tionary pathways to ferality, he did not consider intercul-
tivar hybridization. Following his lead, we call this
particular pathway for Bhutanese weedy ricde ‘exo-endof-
erality’ because it is first a case of endoferality because all
ancestors are domesticates, but also ‘exo-’ because inter-
taxon hybridization is a critical evolutionary step.
All three of the above comprehensive studies present
strong evidence for the origin of the vast majority of the
weedy rice populations to be from cultivated rice. Inter-
estingly, the data collected reveals a polyphyletic origin
for weedy rice. Polyphylesis is now well-known to play a
role in the evolution of many invasive lineages (Novak
2007) but it is not clear whether it is the rule for domes-
ticate-derived pests.
For three of the four discovered pathways, involving
direct ancestry from indica and japonica, de-domestica-
tion likely occurred via the evolution of (at least) shatter-
ing due to either mutation or an epistatic recombination
event. The most parsimonious pathway for the remaining
exoferal lineage detected by Londo and Schaal (2007) is
for O. rufipogon to have provided the allele or alleles for
shattering.
Weedy rye in western North America
In terms of area planted, cereal rye (Secale cereale L.) is
one of the world’s top 10 grain crops. Volunteer rye has
occasionally been a serious agricultural weed problem
throughout North America for about 100 years. However,
by the early 1960s self-sustaining, naturalized weedy rye
populations were identified as increasingly problematic as
weeds of cultivated lands and invasives of uncultivated
lands in the US states of Washington, Oregon, Idaho, and
California. As a weed of cultivated rye, it was so bad that
‘farmers …abandoned efforts to grow cultivated rye for
human consumption’ (National Research Council 1989).
Subsequently, weedy rye has spread elsewhere in the wes-
tern United States and the Canadian province of British
Columbia (Burger and Ellstrand 2005).
Western North American weedy rye was originally
thought to be a hybrid derivative of cultivated rye and
the wild perennial mountain rye [S. strictum (C. Presl) C.
Presl.]. However, subsequent genetic analysis of several
populations of North American weedy rye with 14 allo-
zyme and three microsatellite loci failed to detect any
ancestry from S. strictum or any other wild Secale. Over-
all, the weedy populations are more similar to each other
than to any one cultivar. Nonetheless, the invasive popu-
lations share a single lineage that apparently evolved
directly from one or more cultivars of cereal rye (Burger
et al. 2006).
Just as in the case of rice, cultivated rye is nonshatter-
ing and has little dormancy, while its derivative has
evolved dispersal by shattering. De-domestication of the
nonshattering trait to shattering likely occurred via muta-
tion or perhaps an epistatic recombination event. Inter-
estingly, in this case, both the crop and the feral
Evolution of weeds and invasives from domesticates Ellstrand et al.
500 ª2010 Blackwell Publishing Ltd 3(2010) 494–504
populations have little seed dormancy. Other traits such
as smaller seed, smaller leaves, thinner culms, and delayed
flowering have rapidly evolved in this lineage (roughly 60
generations since original observations of volunteer popu-
lations) (Burger et al. 2007). It is not clear whether all of
these traits contribute to its evolution as a plant pest,
especially its invasiveness outside of agroecosystems.
However, evolution of a change in flowering time relative
to an ancestor can be a powerful reproductive isolating
mechanism. In this case, it might have evolved under
selection to frustrate maladaptive gene flow (‘reinforce-
ment’ of isolation) from the crop to the weedy lineage
(Levin 1978; see our relevant expanded discussion of evo-
lution of reproductive isolation below).
Wild radish in far western North America
Cultivated radish (R. sativus) is an important vegetable
whose root (botanically, the expanded hypocotyl) is con-
sumed worldwide. The wild jointed charlock (R. raphani-
strum L.; sometimes, confusingly called ‘wild radish’) is a
closely related species, separated from the cultigen by a
chromosomal translocation and a suite of morphological
characters. When the two co-occur in most of the world,
spontaneously hybridization occurs to a limited extent,
resulting in no more than highly localized hybrid swarms
(Snow and Campbell 2005).
In contrast, for almost 100 years, hybridization between
the two Raphanus taxa in California has been more exten-
sive (Frost 1923; Panetsos and Baker 1967). In the last
50 years, hybrid-derived wild Raphanus has invaded
coastal plains and disturbed inland valleys along the Paci-
fic edge of North America from the US state of Oregon
south through California to the Mexican state of Baja
California (Whitson 2006). It has also become a trouble-
some weed for agronomic crops.
Experimental work on what is now known as ‘Califor-
nia wild radish’ has confirmed it to be a lineage des-
cended from hybrids of R. sativus and R. raphanistrum.
Hegde et al. (2006) compared California wild radish
populations with cultivars of R. sativus and populations
of R. raphanistrum. They used 10 allozyme loci as well as
common garden experiments to characterize the three
types. The allozyme data revealed that California wild
radish populations were in Hardy-Weinberg equilibrium;
that is, there was no evidence that pure individuals of the
parental taxa had persisted in significant frequencies.
STRUCTURE analysis of the allozyme dataset confirmed
that conclusion. STRUCTURE assigned the cultivated
radish to one group and the jointed charlock individuals
to another group. The individuals from the California
wild radish populations were assigned at various levels of
hybrid ancestry involving the first two groups. Multivari-
ate analysis of morphological characters measured in their
common garden experiments revealed that the standard
phenotype of California wild radish is significantly differ-
ent from both of its progenitors. Interestingly, its bolting
date, flowering date, and hypocotyl width are intermedi-
ate to its progenitors; its fruit diameter and fruit length
are the same as the cultigen; and its fruit weight trans-
gresses both parents! A subsequent common garden
experiment showed that in several, contrasting California
environments, the hybrid lineage produced both more
fruits per plant and more seeds per plant than either pro-
genitor (Ridley and Ellstrand 2009), including specific
source cultivars and R. raphanistrum populations as
determined from cpDNA analysis (Ridley et al. 2008).
Is there something special about California that permit-
ted this rapid adaptive evolution to proceed in light of
the fact that Raphanus hybrids elsewhere have proven to
be evolutionary deadends? Another common garden
experiment has given a tantalizing result. Synthetic, F
4
generation hybrid lineages and their R. raphanistrum pro-
genitors were grown in the field in Michigan and Califor-
nia. The hybrid lineages’ fitness was slightly inferior to
R. raphanistrum in Michigan but in California they exhib-
ited 22% greater survival and 270% greater lifetime
fecundity (Campbell et al. 2006; see also Campbell and
Snow 2009).
Avenues for future research
Evolutionary studies on weedy and/or invasive plants that
have domesticated ancestors have been useful for detailing
the phylogenetic history of such plants. More examples
might exist. While accumulating our examples for
Table 1, we encountered some cases for which the current
evidence is too weak at this time to convincingly support
or refute a crop origin for an invasive lineage. These are
enumerated in Table 2. Likewise, we encountered exam-
ples of domesticated taxa that have become plant pests,
but it is not clear whether these have evolved to become
pests or are simply ecological opportunists (Table 3).
Consider the case of strawberry guava (Psidium cattleia-
num Sabine). The free-living version of this domesticated
plant is considered by some to be one of the world’s
worst invasive species (Lowe et al. 2000), but no studies
have examined whether the invasive strawberry guava
populations are substantially genetically different from
their domesticated progenitor.
The majority of our entries in Table 1 are examples of
remarkably rapid evolution, at least six of our problem-
atic lineages evolved in less than a century. The compari-
son of progenitors and their wild descendants grown in a
common environment reveals differences that may
account for the success of the latter.
Ellstrand et al. Evolution of weeds and invasives from domesticates
ª2010 Blackwell Publishing Ltd 3(2010) 494–504 501
Nonetheless, research on such systems has barely
exploited their utility for evolutionary study in compari-
son with certain other plant pests, such as the large
body of integrated ecological, physiological and genetic
study employed to understand evolution of invasiveness
in North American reed canarygrass (Phalaris arundina-
cea L.) by Molofsky and colleagues (Lavergne and Mol-
ofsky 2004) (For some other examples of rapid
evolution in invasive plant species see Xu et al. (2010)
and references therein). In particular, invasives and
weeds descended from domesticated plants are ripe for
approaches to tease out the evolutionary pathway to
their new lifestyle. How do they differ from their pro-
genitors with respect to their ecological relationships
with biotic enemies, that is, herbivores and disease-caus-
ing organisms? Are there any differences in their chemi-
cal or physical defenses?
Genetic and genomic approaches, often used in concert
with ethnobotanical data, have been successful in illumi-
nating the evolution of crops from wild species under
domestication (Purugganan and Fuller 2009). These
approaches may prove to be equally powerful in investi-
gating evolution in the other direction, the evolution of
sustainable feral populations from domesticated species.
Let’s consider some of these approaches.
Refined cytogenetic tools for studying chromosomal
evolution under domestication have expanded to include
not only traditional chromosome banding, but also tech-
niques using fluorescent in situ hybridization (FISH)
(e.g., Zhang et al. 2002) and genomic in situ hybridization
(GISH) (e.g., Stace and Bailey 1999). Despite the fact that
many major crops are cytogenetically well-characterized,
we are not aware of any studies that address whether
and how chromosomal evolution has occurred under
de-domestication.
Even if a crop species hasn’t had its genome sequenced,
it is likely to be well-mapped. Quantitative trait locus
(QTL) mapping has proven a powerful way to study the
domestication-related genes (Paterson 2002) by examining
the co-segregation of a trait with markers to determining
the number of loci, their chromosomal location, and their
relative influence on the expression of that trait. For
example, the first maize ‘domestication gene’, teosinte
branched1 (tb1), was identified by QTL mapping (Doeb-
ley et al. 1995). In the same way, crosses between plant
pests and their crop progenitors can be made to examine
the genetic basis of key ecological traits that correlate with
invasive success (Prentis et al. 2008).
Evolutionary genomic approaches have proven particu-
larly fruitful for identifying the genomic and genetic cor-
relates of crop domestication, in particular, potential
adaptive changes (e.g., Ross-Ibarra et al. 2007). For
domesticated taxa that have had their genome sequenced,
such as rice and sorghum, comparative evolutionary eco-
genomic approaches with their descendants will be able
to provide a sweeping view of what genomic changes have
occurred in the evolution of invasives and/or weeds rela-
tive to their crop ancestor. As genome sequencing become
both less expensive and easier to conduct (http://
genome10k.soe.ucsc.edu/), such approaches will become
available for more species, but the descendants of domes-
ticated taxa will still have the advantage of centuries of
study.
We end with a few intriguing questions based on the
simple observation that crops and weeds often have a lot
in common ecologically. First, with regard to crops and
their weedy derivatives, we note that both grow in exactly
the same location, but they are subjected to different selec-
tion regimes. How do weedy crop derivatives end up per-
ceiving different selection pressures so that diverge in
sympatry? Furthermore, how do they diverge given that
they are likely to be swamped by gene flow from the
initially more abundant crop? With regards to the latter
Table 2. Invasives (I) or weeds (W) with too little evidence to determine whether they are descended from domesticated plants.
Common name of
plant pest Possible crop progenitor (s) Citations
I Fennel Fennel, Foeniculum vulgare Bell et al. (2008)
I Sunflower Cultivated sunflower, Helianthus annuus Berville
´et al. (2005)
I Jerusalem artichoke Jerusalem artichoke, Helianthus tuberosus* Berville
´et al. (2005); Kowarik (2005)
W Green bristlegrass Foxtail millet, Setaria italica Darmency (2005)
W Shattercane Grain sorghum, Sorghum bicolor Ejeta and Grenier (2005)
Table 3. Invasives (I) or weeds (W) that are descended from domesti-
cated plants but whether they have evolved is not known.
Name of plant pest and its progenitor Citations
I Strawberry guava (Psidium cattleianum) Lowe et al. (2000)
I,W Callery pear (Pyrus calleryana) Culley and
Hardiman (2009)
I Arabica coffee (Coffea arabica) Joshi et al. (2009)
I Robusta coffee (Coffea canephora) Joshi et al. (2009)
Evolution of weeds and invasives from domesticates Ellstrand et al.
502 ª2010 Blackwell Publishing Ltd 3(2010) 494–504
question, it is clear that reproductive isolating barriers
must evolve rapidly, perhaps explaining why our list of
examples is short (that is, evolution of sustainable feral
populations is difficult). And, at the same time, that would
explain why phenological divergence has been noted for all
of our examples descended from an outcrossing crop
ancestor (artichoke, radish, rye, beet) which would be sub-
ject to a rain of cross-compatible pollen, but not for all of
those descended from a highly selfing crop ancestor
(wheat, finger millet, sorghum, rice) for which relatively
short distances should afford reproductive isolation.
Second, both crops and weeds are often selected for a
life in a disturbed habitat. Both characteristically grow
densely in simple communities or even monocultures. If
humans select crops that grow densely in monospecific
stands, are those plants only a few allele changes away
from becoming invasives or weeds (de Wet and Harlan
1975)? If such is the case, careful and thorough evaluation
should accompany the development of new crops designed
to answer pressing societal needs, including new bioenergy
feedstocks created with the goal of providing a stable
domestic energy supply (Barney and DiTomaso 2008).
Acknowledgements
Our initial manuscript benefited from the ideas of Profes-
sor Jeffrey Ross-Ibarra and his Graduate Genetics Group
at the University of California at Davis. The authors
thank Bao Doan, Baorong Lu, Jeffrey Ross-Ibarra, Allison
Snow, and two anonymous reviewers for their ideas and/
or insightful contributions to subsequent versions of this
manuscript. This work was supported by NSF DEB-
0409984 and NRI-CSREES-USDA 2003-35320 grants to
N.C.E. as well as a US Environmental Protection Agency
(EPA) Science to Achieve Results (STAR) Graduate Fel-
lowship to C.E.R. EPA has not officially endorsed this
publication, and the views expressed herein might not
reflect the views of EPA.
Literature cited
Andersson, M. S., and M. C. de Vicente. 2010. Gene Flow between Crops and
Their Wild Relatives. Johns Hopkins University Press, Baltimore, MD.
Arnold, M. L. 2006. Evolution through Genetic Exchange. Oxford University
Press, Oxford, UK.
Ayal, S., and A. A. Levy. 2005. Wheat domestication and de-domestication –
What are the odds? In J. Gressel, ed. Crop Ferality and Volunteerism,
pp. 167–173. CRC Press, Boca Raton, FL.
Bagavathiannan, M. V., B. Julier, P. Barre, R. H. Gulden, and R. C. Van
Acker. 2010. Genetic diversity of feral alfalfa (Medicago sativa L.) popula-
tions occurring in Manitoba, Canada and comparison with alfalfa cultivars:
an analysis using SSR markers and phenotypic traits. Euphytica 173:419–
432.
Baker, H. G. 1974. The evolution of weeds. Annual Review of Ecology 5:1–24.
Baker, H. G., and G. L. Stebbins. 1965. The Genetics of Colonizing Species.
Academic Press, New York, NY.
Barney, J. N., and J. M. DiTomaso. 2008. Nonnative species and bioenergy: are
we cultivating the next invader? BioScience 58:64–70.
Barrett, S. H. 1983. Crop mimicry in weeds. Economic Botany 37:255–282.
Bell, C. E., T. Easely, and K. R. Goodman. 2008. Effective fennel (Foeniculum
vulgare) control with herbicides in natural habitats in California. Invasive
Plant Science and Management 1:66–72.
Berville
´, A., M.-H. Muller, B. Poinso, and H. Serieys. 2005. Risks of gene flow
between sunflower and other Helianthus species. In J. Gressel, ed. Crop
Ferality and Volunteerism, pp. 209–230. CRC Press, Boca Raton, FL.
Blossey, B., and R. No
¨tzold. 1995. Evolution of increased competitive ability in
invasive nonindigenous plants: a hypothesis. Journal of Ecology 83:887–889.
Bossdorf, O., H. Auge, L. Lafuma, W. E. Rogers, E. Siemann, and D. Prati. 2005.
Phenotypic and genetic differentiation between native and introduced plant
populations. Oecologia 144:1–11.
Brodersen, C., S. Lavergne, and J. Molofsky. 2008. Genetic variation in
photosynthetic characteristics among invasive and native populations of reed
canarygrass (Phalaris arundinacea). Biological Invasions 10:1317–1325.
Burger, J. C., and N. C. Ellstrand. 2005. Feral rye – evolutionary origins of a
weed. In J. Gressel, ed. Crop Ferality and Volunteerism, pp. 175–192. CRC
Press, Boca Raton, FL.
Burger, J. C., S. Lee, and N. C. Ellstrand. 2006. Origin and genetic structure of
feral rye in the western United States. Molecular Ecology 15:2527–2539.
Burger, J. C., J. S. Holt, and N. C. Ellstrand. 2007. Rapid phenotypic divergence
of feral rye from domesticated cereal rye. Weed Science 55:204–271.
Campbell, L. G., and A. A. Snow. 2009. Can feral weeds evolve from cultivated rad-
ish (Raphanus sativus, Brassicaceae)? American Journal of Botany 96:498–506.
Campbell, L. G., A. A. Snow, and C. E. Ridley. 2006. Weed evolution after crop
gene introgression: greater survival and fecundity of hybrids in a new environ-
ment. Ecology Letters 11:1198–1209.
Cao, Q., B.-R. Lu, H. Xia, J. Rong, F. Sala, A. Spada, and F. Grassi. 2006. Genetic
diversity and origin of weedy rice (Oryza sativa f. spontanea) populations
found in North-eastern China revealed by simple sequence repeat (SSR)
markers. Annals of Botany 98:1241–1252.
Colautti, R. I., J. L. Maron, and S. C. H. Barrett. 2009. Common garden compar-
isons of native and introduced plant populations: latitudinal clines can obscure
evolutionary inferences. Evolutionary Applications 2:187–199.
Culley, T. M., and N. A. Hardiman. 2009. The role of intraspecific hybridization
in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus
calleryana. Biological Invasions 11:1107–1120.
Darmency, H. 2005. Incestuous relations of foxtail millet (Setaria italica) with
its parents and cousins. In J. Gressel, ed. Crop Ferality and Volunteerism,
pp. 81–96. CRC Press, Boca Raton, FL.
Darwin, C. 1859. On the Origin of Species by Means of Natural Selection. John
Murray, London, UK.
Darwin, C. 1868. The Variation of Animals and Plants under Domestication.
John Murray, London, UK.
van Dijk, H. 2004. Gene exchange between wild and crop in Beta vulgaris: how
easy is hybridization and what will happen in later generations? In H. C. M.
den Nijs, D. Bartsch, and J. Sweet, eds. Introgression from Genetically Modi-
fied Plants into Wild Relatives, pp. 53–61. CABI Publishing, Wallingford, UK.
Dlugosch, K. M., and I. M. Parker. 2008a. Founding events in species invasions:
genetic variation, adaptive evolution, and the role of multiple introductions.
Molecular Ecology 17:431–449.
Dlugosch, K. M., and I. M. Parker. 2008b. Invading populations of an orna-
mental shrub show rapid life history evolution despite genetic bottlenecks.
Ecology Letters 11:701–709.
Doebley, J., A. Stec, and C. Gustus. 1995. Teosinte branched1 and the origin of
maize: evidence for epistasis and the evolution of dominance. Genetics
141:333–346.
Ehara, K., and S. Abe. 1950. Classification of the forms of Japanese barnyard
millet. Proceedings of the Crop Science Society of Japan 20:245–246.
Ejeta, G., and C. Grenier. 2005. Sorghum and its weedy hybrids. In J. Gressel, ed.
Crop Ferality and Volunteerism, pp. 123–136. CRC Press, Boca Raton, FL.
Ellstrand, N. C., and K. Schierenbeck. 2000. Hybridization as a stimulus for the
evolution of invasiveness in plants? Proceedings of the National Academy of
Sciences USA 97:7043–7050.
Ellstrand et al. Evolution of weeds and invasives from domesticates
ª2010 Blackwell Publishing Ltd 3(2010) 494–504 503
Frost, H. G. 1923. Heterosis and dominance of size factors in Raphanus. Genetics
8:116–153.
Gealy, D. R. 2005. Gene movement between rice (Oryza sativa) and weedy rice
(Oryza sativa) – a U.S. temperate rice perspective. In J. Gressel, ed. Crop
Ferality and Volunteerism, pp. 323–354. CRC Press, Boca Raton, FL.
Gepts, P. 2004. Crop domestication as a long-term selection experiment. Plant
Breeding Reviews 24:1–44.
Gressel, J. 2005a. Introduction – the challenges of ferality. In J. Gressel, ed. Crop
Ferality and Volunteerism, pp. 1–7. CRC Press, Boca Raton, FL.
Gressel, J. 2005b. Crop Ferality and Volunteerism. CRC Press, Boca Raton, FL.
Hegde, S. G., J. D. Nason, J. Clegg, and N. C. Ellstrand. 2006. The evolution of
California’s wild radish has resulted in the extinction of its progenitors.
Evolution 60:1187–1197.
Hierro, J. L., J. M. Marron, and R. M. Callaway. 2005. A biogeographical
approach to plant invasions: the importance of studying exotics in their
introduced and native range. Journal of Ecology 93:5–15.
Hilu, K., J. M. J. de Wet, and D. Seigler. 1978. Flavonoid patterns and systematics
in Eleusine. Biochemical Systematics and Ecology 6:247–249.
Holm, L. G., D. L. Plucknett, J. V. Pancho, and J. P. Herberger. 1977. The
World’s Worst Weeds: Distribution and Biology. University Press of Hawaii,
Honolulu.
Holm, L., J. Doll, E. Holm, J. Pancho, and J. Herberger. 1997. World Weeds:
Natural Histories and Distribution. John Wiley & Sons, New York, NY.
Ishikawa, R., N. Toki, K. Imai, Y. I. Sato, H. Yamagishi, Y. Shimamoto, K. Ueno
et al. 2005. Origin of weedy rice grown in Bhutan and the force of genetic
diversity. Genetic Resources and Crop Evolution 52:395–403.
Joshi, A. A., D. Mudappa, and T. R. S. Raman. 2009. Brewing trouble: coffee
invasion in relation to edges and forest structure in tropical rainforest frag-
ments of the Western Ghats, India. Biological Invasions 11:2387–2400.
Kaus, A., and A. Go
´mez Pompa. 1992. Taming the wilderness myth. BioScience
42:271–279.
Keller, S. R., D. R. Sowell, M. Neiman, L. M. Wolfe, and D. R. Taylor. 2009.
Adaptation and colonization history affect the evolution of clines in two
introduced species. New Phytologist 183:678–690.
Kowarik, I. 2005. Urban ornamentals escaped from cultivation. In J. Gressel, ed.
Crop Ferality and Volunteerism, pp. 97–121. CRC Press, Boca Raton, FL.
Lavergne, S., and J. Molofsky. 2004. Reed canary grass (Phalaris arundinacea)asa
biological model in the study of plant invasions. Critical Reviews in Plant
Sciences 23:415–429.
Leak-Garcia, J. A. 2009. Genetic origins and the evolution of invasiveness of
Cynara cardunculus in California. PhD dissertation in Genetics, Genomics, and
Bioinformatics. University of California, Riverside, California, USA.
Levin, D. A. 1978. The origin of isolating mechanisms in flowering plants.
Evolutionary Biology 11:185–317.
Londo, J. P., and B. A. Schaal. 2007. Origins and population genetics of weedy
red rice in the USA. Molecular Ecology 16:4523–4535.
Lowe, S., M. Browne, S. Boudjelas, and M. De Poorter. 2000. 100 of the World’s
Worst Invasive Alien Species: A Selection from the Global Invasive Species Data-
base. The Invasive Species Specialist Group (ISSG) a specialist group of the Spe-
cies Survival Commission (SSC) of the World Conservation Union (IUCN).
Moloney, K. A., C. Holzapfel, K. Tielbo
¨rger, F. Jeltsch, and F. M. Schurr. 2009.
Rethinking the common garden in invasion research. Perspectives in Plant
Ecology, Evolution and Systematics 11:311–320.
Morrell, P. L., T. D. Williams-Coplin, A. L. Lattu, J. E. Bowers, J. M. Chandler,
and A. H. Paterson. 2005. Crop-to-weed introgression has impacted allelic
composition of johnsongrass populations with and without recent exposure to
cultivated sorghum. Molecular Ecology 14:2143–2154.
Mu
¨cher, T., P. Hesse, M. Pohl-Orf, N. C. Ellstrand, and D. Bartsch. 2000. Char-
acterization of weed beet in Germany and Italy. Journal of Sugar Beet Research
37:19–38.
National Research Council. 1989. Field Testing Genetically Modified Organisms:
Framework for Decisions. National Academy Press, Washington.
Novak, S. J. 2007. The role of evolution in the invasion process. Proceedings of
the National Academy of Sciences USA 104:3671–3672.
Panetsos, C. A., and H. G. Baker. 1967. The origin of variation in ‘‘wild’’ Raph-
anus sativus (Cruciferae) in California. Genetica 38:243–274.
Paterson, A. H. 2002. What has QTL mapping taught us about plant domestica-
tion? New Phytologist 154:591–608.
Paterson, A. H., K. F. Schertz, Y. R. Lin, S.-C. Liu, and Y.-L. Chang. 1995. The
weediness of wild plants: molecular analysis of genes influencing dispersal and
persistence of johnsongrass, Sorghum halepense (L.) Pers. Proceedings of the
National Academy of Sciences USA 92:6127–6131.
Prentis, P. J., J. R. U. Wilson, E. E. Dormontt, D. M. Richardson, and A. J. Lowe.
2008. Adaptive evolution in invasive species. Trends in Plant Sciences 13:288–
294.
Pritchard, J. K., M. Stephens, and P. Donnelly. 2000. Inference of population
structure using multilocus genotypic data. Genetics 155:945–959.
Purugganan, M. D., and D. Q. Fuller. 2009. The nature of selection under plant
domestication. Nature 457:843–848.
Ridley, C. E., and N. C. Ellstrand. 2009. Evolution of enhanced reproduction in
the hybrid-derived invasive, California wild radish (Raphanus sativus). Biologi-
cal Invasions 11:2251–2264.
Ridley, C. E., S.-C. Kim, and N. C. Ellstrand. 2008. Bidirectional history of
hybridization in California wild radish, Raphanus sativus (Brassicaceae), as
revealed by chloroplast DNA. American Journal of Botany 95:1437–1442.
Ross-Ibarra, J., P. L. Morrell, and B. S. Gaut. 2007. Plant domestication, a unique
opportunity to identify the genetic basis of adaptation. Proceedings of the
National Academy of Sciences USA 104:8641–8648.
Schierenbeck, K. A., and N. C. Ellstrand. 2009. Hybridization and the evolution
of invasiveness in plants and other organisms. Biological Invasions 11:1093–
1105.
Sharma, G. P., A. S. Raghubanshi, and J. S. Singh. 2005. Lantana invasion: an
overview. Weed Biology and Management 5:157–165.
Smartt, J., and N. W. Simmonds. 1995. Evolution of Crop Plants, 2nd edn.
Longman, Harlow, UK.
Snow, A. A., and L. G. Campbell. 2005. Can feral radishes become weeds? In J.
Gressel, ed. Crop Ferality and Volunteerism, pp. 193–208. CRC Press, Boca
Raton, FL.
Stace, C. A., and J. P. Bailey. 1999. The value of genomic in situ hybridization
(GISH) in plant taxonomic and evolutionary studies. In P. M. Hollingsworth,
R. M. Bateman, and R. J. Gornall, eds. Molecular Systematics and Plant
Evolution, pp. 199–210. Taylor & Francis, London, UK.
Sun, Q., Z. Ni, Z. Liu, J. Gao, and T. Huang. 1998. Genetic relationships and
diversity among Tibetan wheat, common wheat and European spelt wheat
revealed by RAPD markers. Euphytica 99:205–211.
Suneson, C. A., K. O. Rachie, and G. S. Khush. 1969. A dynamic population of
weedy rye. Crop Science 9:121–124.
Valverde, B. E. 2005. The damage by weedy rice – can feral rice remain unde-
tected? In J. Gressel, ed. Crop Ferality and Volunteerism, pp. 279–294. CRC
Press, Boca Raton, FL.
Vaughan, D. A., P. L. Sanchez, J. Ushiki, A. Kaga, and N. Tomooka. 2005. Asian
rice and weedy rice – evolutionary perspectives. In J. Gressel, ed. Crop Ferality
and Volunteerism, pp. 257–277. CRC Press, Boca Raton, FL.
Venable, D. L. 2007. Bet hedging in a guild of desert annuals. Ecology 88:1086–
1090.
de Wet, J. M. J. 1995. Finger millet. In J. Smartt, and N. W. Simmonds, eds. Evo-
lution of Crop Plants, 2nd edn, pp. 137–140. Longman, Harlow, UK.
de Wet, J. M. J., and J. R. Harlan. 1975. Weeds and domesticates: evolution in
the man-made habitat. Economic Botany 29:99–107.
de Wet, J. M. J., K. E. Prasada Rao, D. E. Brink, and M. H. Mengesha. 1984. Sys-
tematics and evolution of Eleusine coracana (gramineae). American Journal of
Botany 71:550–557.
Whitson, T. 2006. Weeds of the West. Western Society of Weed Science, Newark,
CA.
Xu, C.-Y., M. H. Julien, M. Fatemi, C. Girod, R. D. Van Klinken, C. L. Gross,
and S. J. Novak. 2010. Phenotypic divergence during the invasion of Phyla
canescens in Australia and France: evidence for selection-driven evolution.
Ecology Letters 13:32–44.
Zhang, L., A. S. Peek, D. Dunams, and B. S. Gaut. 2002. Population genetics
of duplicated disease defense genes, hm1 and hm2, in maize (Zea mays ssp.
mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics
162:851–860.
Evolution of weeds and invasives from domesticates Ellstrand et al.
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