Adaptive evolution in invasive species.

Abstract

Many emerging invasive species display evidence of rapid adaptation. Contemporary genetic studies demonstrate that adaptation to novel environments can occur within 20 generations or less, indicating that evolutionary processes can influence invasiveness. However, the source of genetic or epigenetic variation underlying these changes remains uncharacterised. Here, we review the potential for rapid adaptation from standing genetic variation and from new mutations, and examine four types of evolutionary change that might promote or constrain rapid adaptation during the invasion process. Understanding the source of variation that contributes to adaptive evolution in invasive plants is important for predicting future invasion scenarios, identifying candidate genes involved in invasiveness, and, more generally, for understanding how populations can evolve rapidly in response to novel and changing environments.

Full text

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Adaptive evolution in invasive species
Peter J. Prentis1, John R.U. Wilson2, Eleanor E. Dormontt1, David M. Richardson2
and Andrew J. Lowe1,3
1Australian Centre for Evolutionary Biology and Biodiversity, School of Earth and Environmental Sciences, University of Adelaide,
North Terrace, South Australia 5005, Australia
2Centre for Invasion Biology, Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland, 7600,
South Africa
3State Herbarium and Bioknowledge South Australia, Hackney Road, Adelaide, South Australia 5005, Australia
Many emerging invasive species display evidence of
rapid adaptation. Contemporary genetic studies demon-
strate that adaptation to novel environments can occur
within 20 generations or less, indicating that evolution-
ary processes can influence invasiveness. However, the
source of genetic or epigenetic variation underlying
thesechangesremainsuncharacterised.Here,wereview
the potential for rapid adaptation from standing genetic
variation and from new mutations, and examine four
types of evolutionary change that might promote or
constrain rapid adaptation during the invasion process.
Understanding the source of variation that contributes
to adaptive evolution in invasive plants is important for
predicting future invasion scenarios, identifying candi-
date genes involved in invasiveness, and, more gener-
ally, for understanding how populations can evolve
rapidlyinresponsetonovelandchangingenvironments.
Introduction
Biological invasions are defined as the introduction, estab-
lishment, and spread of species outside their native range
([1];Figure1]),andtheyarerecognizedasamajorthreatto
theeconomyandenvironmentworldwide[2].Bydefinition,
introduced species are present in biogeographic regions
where they did not evolve and to which they might be
poorly adapted [1,3], encountering a suite of novel stresses
and selection pressures [4]. Consequently, introduced
populations have considerable potential for rapid adap-
tation, and it has been proposed that this adaptation can
explain why some introduced species establish, proliferate,
and become invasive in new environments [1–7].
Evolutionary change was first recognized as an import-
ant process in biological invasions more than 30 years ago
[8]. Nevertheless, most research in this area has been
conducted in the past decade, and has concentrated on
comparing genetic diversity between source and invasive
populations [5]. Fewer studies have examined the role of
rapid adaptive evolution in biological invasion [7,9], and no
study that we know of has attempted to identify the source
of genetic and epigenetic variation underlying rapid adap-
tation in invasive species. The literature on non-invasive
model or agronomic plant species, however, details a range
of mechanisms that can influence rapid evolutionary
change within 20 generations or fewer [10–13]. This
includes a case in which heritable genomic change in
Arabidopsis thaliana (thale cress) was caused by novel
environmental stress [11], a mechanism not yet examined
in the rapid evolution of invasive species. Given the poten-
tial that these mechanisms have for explaining invasive-
ness, the study of adaptive evolution in invasive species
will fast become a very productive area of research.
In this review, we explore the role of rapid evolutionary
change as a means of adaptation during plant invasions,
and identify key research gaps. Our primary focus is to
elucidate how different forms of genetic variation affect the
likelihood of adaptive evolution during the introduction,
establishment, and spread of invasive species (Figure 1).
We examine the potential for adaptive evolution in inva-
sive species provided by standing genetic variation com-
pared to that from new mutations, and look at four types of
evolutionary change that might promote rapid evolution in
the introduced range: bottlenecks, hybridization, poly-
ploidy, and stress-induced modification of the genome.
Although adaptation from standing genetic variation
and the four types of evolutionary change are not exclusive
to plant invasions, the nature of many biological invasions
predisposes invasive plants to these mechanisms [1,3,4].
Moreover, recent biological invasions such as that of
Hypericum canariense (Canary Island St. John’s wort
[14]),provideanideal opportunity
rapid adaptation [15]. We advocate the use of a combined
to investigate
Review
Glossary
Additive genetic variance: variance associated with the average outcome of
substituting one allele with another.
Epigenetic: a factor that changes the phenotype of an organism that is not
associated with a change in its DNA sequence.
Epistasis: the phenotypic consequence of interaction among alleles at multiple
loci.
Founder effect: the difference in gene pools between an original population
and a new population after colonization.
Genetic bottleneck: when population numbers are reduced to a level
insufficient to sustain the diversity in the population.
Introduced species (synonyms: alien, exotic, non-indigenous, non-native): a
species that is not native to a region and that was introduced to that region
through human activity.
Invasive species: an introduced species that has overcome dispersal barriers to
produce established self-perpetuating populations far from the initial introduc-
tion.
Polyploid: having more than two full copies of each chromosome.
Quantitative trait locus: the location on a chromosome of a gene(s) that affects
a quantitative trait.
Retrotransposon: a transposon copied from RNA with the use of reverse
transcriptase.
Standing genetic variation: the presence of more than one allele at a locus in a
natural population.
Corresponding author: Prentis, P.J. (peter.prentis@adelaide.edu.au).
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quantitative trait locus (QTL) mapping and genome scan
approach [16] to discover the underlying genetic changes
associated with successful invasions and potentially to
identify candidate genes that are involved in invasiveness.
Standing genetic variation compared with new
mutation
Whether the genetic changes that allow species adapt to
new environments arise from new mutation or standing
genetic variation is currently a key question in evolution-
ary biology [17], and this question is equally important for
understanding the rapid evolution of invasiveness. We
predictthat,duringtheinvasionprocess,rapidadaptation,
occurring over tens of generations or fewer [13], should
mostly be due to alleles from standing genetic variation
because favourable alleles are immediately available and
are usually found at a greater frequency in populations
relative to neutral or deleterious alleles [18]. Moreover,
because invasive populations frequently face new environ-
mental conditions, alleles that have neutral or even
deleterious effects in the native range can become advan-
tageous in the introduced range. Evidence supporting
our prediction comes from the natural invasion of the
Caribbean islands and Central America from Brazil by
Figure 1. Adaptive evolution during the stages of invasion. Key stages in plant invasions can be depicted with regard to the change in range size over time (centre), or with
reference to sequential barriers that the species must negotiate [66] (top). The barriers to invasion predispose plants to certain types of evolutionary change at different
points in the invasion process (bottom). Elucidation of these dynamics is crucial for understanding adaptive evolution in plant invasions. Rapid adaptation from standing
genetic variation is likely at all stages of invasion [18], but other evolutionary processes will be important at particular stages. Bottlenecks are likely to be particularly
prevalent during the introduction and establishment stages because of founder effects and population isolation after dispersal involving a long-distance jump [14,24].
Evolutionary change induced by new competitors, pathogens, natural enemies, or abiotic stressors, is most likely to occur during introduction and spread. Polyploidy can
benefit plants during early invasion if individuals with higher ploidy levels are stronger competitors or better colonizers than diploids [49,50]. Hybridisation can have
immediate impacts on invasive potential in neo-allopolyploids because of fixed heterosis [51], but might also be important in establishment and spread if adaptive
introgression and transgressive segregation aid the colonization of new environments [9,37]. Note, the success or sudden decline [67,68] of invasive plants can also be
caused by adaptive evolution in herbivores, pollinators, fungal symbionts or competing plants.
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Eichhornia paniculata (Brazilian water hyacinth). In this
species, recessive modifier genes that promote selfing often
occur at low frequencies in outcrossing Brazilian popu-
lations but fail to spread, possibly as reliable pollination
services are available and because of genetic costs associ-
ated with inbreeding depression [19,20]. Self-fertilization
has evolved, however, in the Caribbean islands where the
recessive modifier genes have increased in frequency [21],
possibly because of unreliable pollinator services in this
new environment. Adaptation from standing genetic vari-
ation should also dominate rapid evolution during range
expansion, particularly when invasive species are exposed
to ecogeographic variation. Geographical clines in life-
history traits that have been found in many invasive
plants, including California poppies (Eschscholzia califor-
nica) and Purple loosestrife (Lythrum salicaria), provide
compelling evidence of local adaptation to environmental
conditions [20,22]. Clines observed in E. californica and L.
salicaria mirror similar clines observed in the native range
of these plants, indicating that this adaptation possibly
arose from standing genetic variation.
Recent advances in population genetic theory [17,18,23]
are making it possible to distinguish between adaptation
from standing genetic variation and adaptation from new
mutation, as they leave different molecular signatures in
the genome. By applying this theory in conjunction with
genome scans, it will become possible to decipher whether
rapid evolution in invasive species is mainly through selec-
tion on standing genetic variation.
Bottlenecks
Genetic bottlenecks are commonly predicted to be associ-
ated with biological invasions [24], as introduced popu-
lations can be founded by a small number of individuals
that are isolated from further gene flow [14]. Whether
geneticbottlenecks constrainthe speed of rapid adaptation
is a question of great interest to invasion biologists
[5,13,14]. Traditionally, genetic bottlenecks were thought
to decrease the potential for adaptive evolution [25]
because of a reduction in the quantitative variation within
a population. Recent theoretical research, however, has
suggested that bottlenecks can lead to increased genetic
variance in founding populations because of the conversion
of epistatic to additive variance [26], and hence, bottle-
necks could promote rapid adaptive evolution. Conversely,
Turelli and Barton [27] argue that biologically realistic
models do not predict large conversions of epistatic to
additive variance following a bottleneck. They argue that
epistatic components of variance for most traits tend to be
small [28] and that an increase in variance is appreciable
only under extreme levels of inbreeding. In view of these
arguments, we predict that bottlenecks restrict the speed
of rapid adaptive evolution during most introductions, but
have the potential to promote rapid adaptation under
special conditions.
A particularly interesting example of rapid adaptive
evolution after a strong genetic bottleneck is provided by
H. canariense, Canary Island St. John’s wort. Three iso-
lated invasive populations showed evidence of a strong
genetic bottleneck (expected heterozygosity was 45% lower
thanthatofnativepopulations).Despitethislossofgenetic
variation, the three introduced populations had higher
growthratesthansourcepopulations,andaclineinflower-
ing time has developed among locations, indicating adap-
tation to local environmental conditions in less than 50
years. It is not known, however, whether adaptation would
have been quicker had there been no bottleneck.
Hybridization
Hybridization, both intra- and interspecific, has been
suggested to stimulate invasiveness in plants [29]. Mount-
ing evidence is becoming available to support this claim
because many invading species, including Ambrosia arte-
misiifolia (Common ragweed) and Cytisus scoparius
(Scotch broom), have multiple introductions. Other invad-
ing taxa, such as Helianthus annuus ssp. texanus (Weedy
sunflower) are the by-products of inter-specific hybridiz-
ation [5,9,14,30–33]. In some cases, however, multiple
invasion events can lead to a mosaic of maladaptation,
where trait values from one population might be better
suited in another population, a pattern observed for Ver-
bascum thapsus (Common mullein) [14].
Invasion biologists are exceptionally interested in find-
ing out what types of hybridisation provide the genetic
novelty for rapid adaptation. A hybrid might have
increased fitness due to heterosis or later-generation
recombination of parental genotypes [34]. First-generation
hybrids often exhibit heterosis, and are larger and have
increased yield compared to parental lines [35]. With the
exception of asexual species and allopolyploids [36], how-
ever, the benefits of heterosis diminish in later-generation
hybrids because of recombination and reduction in hetero-
zygosity. Because heterosis can be transient, we predict
that recombination is more important in the rapid evol-
ution of invasive species.
Recombination can generate novel gene combinations
upon which natural selection acts to produce a phenotype
that is better suited to colonise novel environments [37].
Senecio squalidus (Oxford ragwort) provides a classic
example of this. S. squalidus, a recombinant hybrid be-
tween Senecio aethensis and Senecio chrysanthemumifo-
lius, was originally brought from Mount Etna in Sicily to
Oxford Botanical Garden, England. Both parental species
are absent from the wild in the UK, but the hybrid species
became invasive and is now widespread [38].
Enhanced invasiveness as the result of recombination
can occur by two main mechanisms. First, hybrids can
exhibit traits that are novel or extreme relative to those
of either parental line, a common feature of plant hybrids
in particular [39,40]. Such extreme phenotypes are often
the outcome of transgressive segregation, where alleles
from both parents combine to produce extreme traits that
exceed parental phenotypic values in either a negative or
positive direction [34]. In a recent study of gene expression
usinganon-invasive hybridspecies, Helianthus deserticola
(Desert sunflower), and its parental species, 2% of genes
exhibited transgressive expression profiles [41]. H. deser-
ticola has colonized a novel habitat type not inhabited by
either parent, indicating that transgressive segregation
associated with interspecific hybridization can aid the
colonization of novel environments. In some cases, trans-
gressive gene expression in interspecific hybrids results in
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changes to patterns of parental gene expression that are so
extensive that it has been termed ‘transcriptome shock’
[42].
Second, hybridization can cause adaptive trait intro-
gression, in which alleles that could potentially increase
fitness or fecundity are transferred from one species to
another [9]. Adaptive trait introgression has conferred
herbivore-resistanttraits
Helianthus debilis, into common sunflower, Helianthus
annuus ssp. annuus. This introgression has allowed a
stabilized hybrid lineage of this species, H. annuus ssp.
texanus, to colonize new environments in central and
southern Texas [9]. In two uniform environment exper-
iments located in southern Texas, H. annuus ssp. texanus
exhibited 55% higher fitness than H. annuus ssp. annuus
and was more resistant to herbivores.
from Beach sunflower,
Polyploidy
Polyploidy or genome doubling has been a pervasive force
in plant evolution [43]. Interestingly, polyploids occur with
greater frequency among invasive plants than among
angiosperms in general [44,45]. In many cases where
species consist of two or more ploidy levels in the native
range, invasive populations often only contain individuals
of the higher ploidy level, for example Fallopia japonica
(Japanese knotweed) in Europe [46]. Alternatively, inva-
sive populations can be neo-allopolyploids, such as Trago-
pogon mirus (remarkable Goat’s beard) [47], formed from
recent hybridization between two species and subsequent
genome doubling. Why polyploids are overrepresented on
listsofinvasivespeciesiscurrentlyunknown,anddifferent
explanations probably apply for neo-allopolyploids and
other polyploids. One reason for the greater incidence of
invasiveness among taxa that have higher ploidy levels is
that there might be fitness or competitive difference(s)
between populations with different ploidy levels in some
species complexes. For example, Flegrova and Krahulec
[48] found, using reciprocal transplant experiments, that
tetraploid Anthoxanthum odoratum (Sweet vernal grass)
had higher fitness than diploid Anthoxanthum alpinum
(Alpine sweet vernal grass) in both habitats. Another
reason for the high incidence of invasiveness among poly-
ploids could be that they are better colonizers than
diploids, a pattern that has received some support [49],
particularly in the Artic flora [50].
Neo-allopolyploids are probably successful invaders
because of fixed heterosis that results from the fixing of
divergentparentalgenomesinallopolyploids.Theenforced
pairing of homologous chromosomes in allopolyploids pre-
vents intergenomic recombination, and hence the benefits
of heterosis are not diminished in later generations of
allopolyploid hybrids [51]. Fixed heterosis is probably
the major reason for the success of neo-allopolyploids that
reproduce asexually. Neo-allopolyploids that reproduce
sexually, however, often pass through strong fertility bot-
tlenecks associated with difficulties in meiosis [52,53],
which might slow adaptation.
Allopolyploids can also undergo extensive alterations to
their genome and transcriptome, including some that arise
with the onset of genome doubling [43]. Novel phenotypes
are known to emerge from these changes, including some
with high visibility to selection [43], and these changes
might promote invasiveness in some neo-allopolyploids.
Recent studies demonstrate, however, that hybridization
has a greater effect than chromosome doubling on genomic
changesinallopolyploids [42].Thus,hybridizationcouldbe
more important for the success of allopolyploid invaders
than is genome doubling.
Stress-induced modification of the genome
Invasive species frequently encounter novel ecological con-
texts [4], both biotic (e.g. pathogens) and abiotic (i.e. UV
exposure). Exposure to novel biotic or abiotic conditions
can induce stress in some plants, and has been shown to
affect genome stability in some cases [54,55]. This process
is, on initial inspection, akin to the ideas of Lamarck, but a
recent review distinguishes this area as stress-induced
modification of the genome [12]. Stress-induced genome
modification can be epigenetic [11]; alternatively, it can
occur when retrotransposons activate and reinsert into the
genome [56] and in some instances are stably inherited
[54,57].
Stress-induced genomic effects have been implicated in
rapidgenomicorphenotypicchangeinseveralwell-studied
plant species, including Arabidopsis and flax (Linum usi-
tatissimum) [10,11,55]. For example, elevated UV-C
exposure and pathogen attack increased rates of homolo-
gous recombination in Arabidopsis for at least four gener-
ations in the progeny of treated plants [11]. Abiotic stress
has also been shown to activate retrotransposons in Tri-
ticum (wheat), resulting in the silencing of genes adjacent
to the insertion sites of the retrotransposons and altering
the expression patterns of these genes [56]. A particularly
interesting example of phenotypic change promoted by
novel environmental stress occurs in L. usitatissimum,
in which growth under different fertilizer treatments
resulted in large-scale genomic changes in one generation
(see Figure 2 for a detailed description of this process).
These examples show that a decrease in genome stability,
in response to environmental stimuli, can cause modifi-
cations to the genome and transcriptome, resulting in new
phenotypic variation that is then exposed to selection
[12,55]. Although stress-induced modification of the gen-
ome has only recently emerged as a mechanism that can
create genetic novelty, we predict that it will explain some
instances of rapid adaptation in invasive species.
A genomic approach to studying adaptive evolution
in invasive species
Understanding the genetic basis of traits that are involved
in rapid adaptation to novel environmental conditions is a
major goal in invasion biology. In particular, identifying
the genes or genetic changes that underlie these traits will
permit us to answer fundamental questions: how often
does rapid adaptation result from standing genetic vari-
ation rather than new mutation in successful plant inva-
sions? And are similar genes the targets of selection when
the same species undergoes multiple independent inva-
sions? To answer these questions, and to identify genes
underlyinginvasivetraits, werecommendanapproachput
forward recently by Stinchcombe and Hoekstra [16]. This
powerfulapproachusesagenomescanincombinationwith
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QTL mapping to identify chromosomal regions and genes
within these regions that are involved in adaptive evol-
ution in invasive plants.
Genome scans involve genotyping numerous
throughout the genome of many individuals in several
populations [58] to detect ‘outlier’ loci that show unusually
high levels of differentiation. This makes it possible to
distinguish between evolutionary forces that affect the
whole genome (e.g. bottlenecks) and those that affect
particular loci (i.e. selection) [59]. For non-model species
whose genomes have not been sequenced, which include
most invasive plants, the most effective genome scan
approach to identify ‘outliers’ utilizes microsatellites in
the untranslated regions of expressed sequence tags
[60]. This approach makes use of close linkage between
a polymorphic marker and a transcribed gene to detect
candidatelocithatmightbeinvolvedinadaptiveevolution.
By scanning the genomes of populations from the native
and introduced range of invasive species, we will be able to
determine both the severity of bottlenecks at population
founding and potential candidate loci that have been the
target of selection. It is important to note, however, that
genome scans have a major limitation when used in iso-
lation: it is often unclear which ‘outlier’ loci underlie
phenotypic traits of interest.
QTL mapping uses statistical analyses of both molecu-
lar markers that are distributed throughout the genome
and traits measured in the progeny of controlled crosses to
identify stretches of DNA that are closely linked to genes
that underlie the trait in question [16]. Thus, QTL studies
have been useful for estimating the complexity of the
genetic architecture that underlies phenotypic traits in
many plant species, from Quercus robur and Quercus
petraea (a closely related oak species) to Arabidopsis
loci
[61,62]. Using a QTL approach on a mapping population
generated from a cross between the native and introduced
range of an invasive species, it should be possible to
identify the position and number of genes that control
traits that are important to successful invasions [63].
QTL approaches provide insight into the nature of adap-
tation to different environmental conditions, but they sel-
dom lead to the genes underlying particular traits because
a given QTL typically contains many genes. Nevertheless,
there are exceptions in which specific genes that are linked
to a particular trait have been identified [64].
Combining a genome scan with QTL mapping has
advantages over either approach taken in isolation. For
instance, outlier loci identified from genome scans can be
integrated onto linkage maps to determine if they map to
chromosomal regions underlying traits of interest. This
approach has been used with success in Zea mays ssp.
mays (maize) and its wild progenitor Z. mays ssp. parvi-
glumis (Teosinte) to identify genes that were possible
targets of selection during domestication [65]. In this
study, two outlier loci were found to map close to a chro-
mosomal region controlling two traits that differ signifi-
cantly between maize and teosinte. We predict that
utilizing this combined approach can move the field of
invasion biology forward by allowing researchers to deter-
mine the genetic basis of invasiveness, and in some
instances, to identify candidate genes or mutations that
are involved in the rapid evolution of invasiveness.
Acknowledgements
We thank three anonymous reviewers for insightful comments that
greatly improved this manuscript and Ana Pavasovic for help with
Figure 2. This work was supported in part by the ARC Discovery Grant
(DP0664967) awarded to A.J.L. by the DST-NRF Centre of Excellence for
Invasion Biology and the Working for Water Programme.
Figure 2. Environmentally induced heritable change observed in flax. In Linum usitatissimum (flax), growth on different fertilizer treatments (with or without environmental
stress) can result in large-scale genomic alterations within a single generation [57]. Specifically, in the presence of an inducing stress, genome-wide insertions and rapid
genotypic and phenotypic changes occur that can be stably inherited in the subsequent absence of the inducing stress, but only under particular temperature regimes
(general conditions) [55]. Without the general conditions, the phenotypes and genotypes of subsequent generations can be unstable. Interestingly, this instability can be
stopped at any point by resuming the presence of general conditions during early growth. Recent work has identified a specific sequence (LIS-1) that is consistently inserted
into the genome at the same site and at the same growth stage when flax is subjected to the initial inducing stress; this is thought to involve a complex set of insertions and
rearrangements and is probably typical of similar changes occurring throughout the flax genome [57].
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Plant Science Conferences in 2008
18th International Plant Lipid Symposium
20–25 July 2008
Bordeaux, France
http://www.ispl2008-bordeaux.cnrs.fr
Banff Conference on Plant Metabolism
2008 July 30 – August 3, 2008
Banff, Alberta, Canada
http://www.ucalgary.ca/plantmetabolism
XVI Congress of the Federation of European Societies of Plant Biology (FESPB 2008)
17–22 August 2008
Tampere, Finland
http://www.fespb2008.org/
Gordon Research Conference
CO2 Assimilation in Plants: Genome to Biome
17–22 August 2008
University of New England
Biddeford, Maine
www.grc.uri.edu/programs/2008/co2.htm
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