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Is There A Genetic Paradox
of Biological Invasion?
Arnaud Estoup,1 Virginie Ravigné,2 Ruth Hufbauer,3
Renaud Vitalis,1 Mathieu Gautier,1 and Benoit Facon1,2
1
Unité Mixte de Recherche Centre de Biologie pour la Gestion des Populations,
Institut National de la Recherche Agronomique, 34988 Montferrier sur Lez, France;
email: [email protected]
2
Unité Mixte de Recherche Peuplements Végétaux et Bioagresseurs en Milieu Tropical,
Centre de Coopération Internationale en Recherche Agronomique pour le Développement,
97410 Saint-Pierre, Louisiana Réunion, France
3
Department of Bioagricultural Science and Pest Management, Colorado State University,
Fort Collins, Colorado 80523
Annu. Rev. Ecol. Evol. Syst. 2016. 47:51–72
Keywords
The Annual Review of Ecology, Evolution, and
Systematics is online at ecolsys.annualreviews.org
adaptation, bioinvasion, bottleneck, evolution, genetic diversity,
quantitative traits, selection
This article’s doi:
10.1146/annurev-ecolsys-121415–032116
c 2016 by Annual Reviews.
Copyright All rights reserved
Abstract
Bottlenecks in population size can reduce fitness and evolutionary potential,
yet introduced species often become invasive. This poses a dilemma referred
to as the genetic paradox of invasion. Three characteristics must hold true for
an introduced population to be considered paradoxical in this sense. First,
it must pass through a bottleneck that reduces genetic variation. Second,
despite the bottleneck, the introduced population must not succumb to the
many problems associated with low genetic variation. Third, it must adapt
to the novel environment. Some introduced populations are not paradoxical
as they do not combine these conditions. In some cases, an apparent paradox
is spurious, as seen in introduced populations with low diversity in neutral
markers that maintain high genetic variation in ecologically relevant traits.
Even when the genetic paradox is genuine, unique aspects of a species’ biology can allow a population to thrive. We propose research directions into
remaining paradoxical aspects of invasion genetics.
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1. INTRODUCTION
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Biological invasions are a component of global change, and their impact on the communities
and ecosystems they invade is substantial and complex (Simberloff 2013). Understanding both
the impacts and ecological and evolutionary processes that promote invasion is a key first step in
developing sound long-term approaches both to prevent future invasions and to manage existing
ones (Colautti & Lau 2015). From the earliest days of invasion biology, evolutionary biologists
postulated that evolution might play an important role in the success of invading species (e.g., Baker
& Stebbins 1965). In agreement, a growing number of studies show contemporary adaptations in
introduced populations (reviewed in Dlugosch & Parker 2008, Colautti & Lau 2015, Dlugosch
et al. 2015). In that context, biological invasions often seem paradoxical: How is it that exotic
organisms that are not initially adapted to their novel environment are able to establish and thrive,
often to such an extent that they outcompete native, presumably locally adapted, species (Sax
& Brown 2000, Facon et al. 2006)? Furthermore, the influence of genetic variation on invasion
success has long fascinated researchers (Baker & Stebbins 1965). The process of introduction
into a new location, as well as spatial expansion from the point of introduction, often imposes a
transitory reduction in population size (i.e., a demographic bottleneck), which has the potential to
reduce genetic variation (e.g., Dlugosch & Parker 2008, Edmonds et al. 2004, Peischl & Excoffier
2015). Small founding and expanding populations can lose much genetic variation via drift, and
inbreeding among members of small populations can lead to low fitness. Yet, rather than suffering
the fate of many species that have small populations and are currently at risk of extinction, many
introduced population grow and expand their range (Uller & Leimu 2011). That many presumably
genetically depauperate introduced populations are able to flourish and adapt is termed the genetic
paradox of invasions (Allendorf & Lundquist 2003). In this review, we first precisely define the
characteristics of introduced populations that determine whether they can or cannot be considered
as an example of a genetic paradox. We then discuss various invasion scenarios in more detail,
breaking down how it is that such a genetic paradox can be overcome.
Three characteristics must hold true for an introduced population to be considered a genetic
paradox. First, it must have lower genetic variation than the native source population at the onset
of the invasion (i.e., it went through a genetic bottleneck). Second, despite the bottleneck, the
introduced population does not succumb to the various deleterious consequences that low genetic
variation can have in the short term for population performance. Third, the introduced population
goes on to adapt successfully to the challenges presented by the novel abiotic and biotic features of
its new habitat. From these characteristics of the genetic paradox of invasion, introduced populations can be categorized broadly into those that simply do not count as paradoxical, as they do not
combine all three conditions, and those that do appear to be paradoxical. We discuss these situations in detail, presenting evidence that introduced populations can maintain high genetic diversity
at key parts of the genome, so that the genetic paradox is spurious. Even when the genetic paradox
is genuine, we explain how special biological features or conditions can enable species to overcome
low genetic diversity. Our approach to illuminating issues surrounding the concept of a genetic
paradox of invasions is summarized in Figure 1. Finally, we propose a nonexhaustive set of research
directions to gain further insights into some remaining paradoxical aspects of invasion genetics.
2. NO PARADOX
2.1. No Genetic Impoverishment in Invasive Populations Relative
to Native Ones
Comparisons of genetic diversity in native and invasive populations reveal that loss of genetic
diversity in invasive populations is less frequent and less intense than initially expected by invasion
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No loss of diversity: shallow bottleneck,
multiple introductions – Section 2.1
No paradox
No adaptive challenge: preadaptation,
including anthropogenically induced
adaptation to invade (AIAI) scenario
– Section 2.2
Diversity loss at neutral genetic markers
overestimates that of genetic variation at
ecologically relevant traits – Section 3.1
Spurious
paradox
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Diversity loss is a consequence of a successful
response to strong selection – Section 3.2
Bottleneck increases population fitness:
beneficial effect on particular traits, purge of
deleterious mutations, conversion of epistatic
to additive variance – Section 4.1
De novo mutations are frequent enough to
restore adaptive potential – Section 4.2
Adaptive phenotypic plasticity tempers
the adaptive challenge – Section 4.3
Genuine
paradox
Diversity loss is compensated for by
epigenetic processes – Section 4.4
Figure 1
Determinants used to evaluate whether an invasion does or does not pose a genetic paradox. The genetic
paradox appears when a bottlenecked introduced population becomes invasive. Three characteristics must
hold true for an introduced population to constitute such a genetic paradox. First, it must harbor lower
standing genetic variation than the native source population (i.e., it went through a genetic bottleneck).
Second, despite this lower standing genetic variation, the introduced population does not succumb to
deleterious consequences of low genetic variation with respect to population dynamics. Third, the
introduced population goes on to adapt successfully to the challenges presented by the novel abiotic and
biotic features of its new habitat. The sections of the corresponding text are indicated.
biology pioneers (Bossdorf et al. 2005, Roman & Darling 2007, Dlugosch & Parker 2008, Uller
& Leimu 2011). Typical genetic markers used for this research are microsatellites, allozymes,
and/or selected mitochondrial or nuclear sequences that are generally presumed to be evolving
neutrally. Data from these markers show that many introduced populations possess comparable
or even greater genetic diversity than native source(s). This finding is seen in 69% of invasive
plants (Bossdorf et al. 2005) and 63% of aquatic invaders (Roman & Darling 2007). Situations
that do not count as paradoxical hence appear to correspond to a majority of invasive species and
populations, at least for some taxa (see also Uller & Leimu 2011). Dlugosch & Parker (2008) and
Uller & Leimu (2011) further reviewed studies of neutral genetic diversity in a large number of
species of animals, plants, and fungi and compared nuclear molecular diversity within introduced
and source populations. Overall they found that, in contrast to previous studies, a loss of variation
was the most frequent feature in invasive populations. However, reductions in genetic variation
were largely modest (e.g., average loss of 15.5% and 18.7% of allelic diversity and heterozygosity,
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respectively; Dlugosch & Parker 2008) and similar or higher levels of genetic diversity were also
found in some cases.
Genetic diversity is likely higher than previously expected due to the large numbers of individuals introduced into the new range (e.g., Simberloff 2009). The release of numerous individuals
increases the likelihood that an introduced population will retain representative genetic diversity
from the source population (Uller & Leimu 2011). Genetic diversity can also increase with the
number of introduction events. If additional introduction events are from the same or similar
native sources, they are essentially equivalent to increasing the numbers of individuals. In keeping
with this scenario, Dlugosch & Parker (2008) and Uller & Leimu (2011) detected a significant
albeit weak increase in neutral genetic variation in invasions in which multiple introductions had
occurred. If additional introduction events derive from genetically differentiated native or invasive
populations, they can substantially increase genetic diversity in introduced populations by transforming among-population variation in the native range into within-population variation in the
introduced range (Rius & Darling 2014). Introductions from multiple differentiated populations
of the native range have two consequences for adaptive process. First, as natural selection operates
at the within-population scale, such highly variable populations should be able to respond rapidly,
as suggested by a Cuban lizard introduced to Florida (Kolbe et al. 2004; see also Lavergne &
Molofsky 2007). Second, admixture may produce entirely novel genotypes, as demonstrated by
the freshwater snail Melanoides tuberculata (Facon et al. 2008). An important point is that admixture
may not always increase diversity at neutral genetic markers (see Section 5.1), but nonetheless it
can create novel variants. Novel genotypes might provide the opportunity for innovative responses
to the new local selection pressures of the nonnative environment and hence promote local spatial
expansion as well as colonization of novel habitats or geographical areas (Dlugosch & Parker 2008,
Rius & Darling 2014). It remains unclear, however, how often genetic admixture acts as a true
driver of invasion success (Uller & Leimu 2011, Rius & Darling 2014).
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2.2. Lower Genetic Diversity but No Adaptive Challenge in the Invasive Range
Some species do show lower genetic diversity in the introduced area as compared with the native
range, yet they do not face any significant adaptive challenge in the invaded habitat. No adaptive
challenge will occur when the environment is similar between the native and introduced ranges
(Sax & Brown 2000, Facon et al. 2006), and no adaptive challenge will occur if a trait in the
native range can be co-opted for a different use in the introduced range (i.e., a process termed
exaptation; box 1 in Hufbauer et al. 2012). Arriving already adapted to the environment found in
the introduced range can be facilitated by fluctuating and/or spatially heterogeneous environments
in the native range (Lee & Gelembiuk 2008), as such environments maintain high genetic diversity.
Demographic bottleneck events associated with long-distance introduction events may result in a
substantial decrease in genetic diversity, but such a decrease is expected to have a limited fitness
impact on preadapted invasive population.
Hufbauer et al. (2012) recently highlighted a specific mechanism termed anthropogenically
induced adaptation to invade (AIAI), by which preadaptation could contribute increasingly to
invasions and hence further resolve the genetic paradox. AIAI begins with contemporary local
adaptation to new human-altered habitats located within the native range of the species. The
potential for adaptive evolution is likely to be high because of greater effective population sizes and
genetic variation than might be expected in the introduced range. Owing to global environmental
homogenization, propagules from populations adapted to human-altered habitats in the native
range should then perform well within similarly human-altered habitats in the novel range. The
AIAI scenario is evolutionarily parsimonious because rather than requiring that rapid adaptive
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evolution occur multiple times when organisms are introduced to multiple different places around
the globe, the critical adaptations need to evolve only once.
3. SPURIOUS PARADOX
Some invasive populations combine all three conditions characterizing the genetic paradox of
invasion. However, because the proxy we use to characterize genetic variation is inadequate, the
genetic paradox is, in fact, spurious.
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3.1. Estimates of Diversity Loss Are Not Relevant
Molecular markers such as microsatellites, even though they are generally limited in number,
are useful for providing rough estimates of global genetic diversity (which is presumed to be
neutral) in a population. However, neutral genetic diversity measured with relatively few markers
is an imperfect predictor of the evolutionary potential of introduced populations (e.g., Lee et al.
2007), because the correlation between assays of molecular marker diversity and quantitative trait
variation is weak (Pfrender et al. 2000, Reed & Frankham 2001). More specifically, meta-analyses
show that the loss of quantitative variation during invasion is generally smaller than the loss of
diversity at molecular markers (e.g., Dlugosch & Parker 2008).
There are two main reasons for this decoupling of patterns of variation at molecular markers
and additive variance at ecologically relevant traits (McKay & Latta 2002). The first reason is
natural selection. Genetic diversity at quantitative trait loci is predicted to correlate with diversity
at molecular markers only when selection is negligible or weak relative to genetic drift (Merilä
& Crnokrak 2001). Conversely, for fitness-related traits and in particular fecundity and mating
success, directional selection is expected to contribute significantly to shaping variation (Kingsolver
et al. 2012), in which case the relationship may be weaker or even absent. The second reason is
genetic architecture (number and effects of loci, and gene interactions). Molecular markers are
discrete traits with Mendelian inheritance, and population genetics theory predicts that when a
bottleneck occurs, alleles are lost to an extent that depends upon the duration and the strength of the
bottleneck (Nei et al. 1975). With some notable exceptions (e.g., antibiotic resistance genes, genefor-gene interactions between plants and pathogens), ecologically relevant traits are quantitative
traits that integrate across the effects of multiple genes. The additive variance for these traits, which
contributes to the response to selection, is therefore less affected by bottlenecks, because loss of
rare alleles has little effect on quantitative variation (Lande 1980, Barton & Charlesworth 1984).
Given all these factors, the low genetic variation measured at (relatively few) neutral markers does
not necessarily signal low additive genetic variance at ecologically relevant traits. The evolutionary
potential to become established might thus be preserved despite the observation of low genetic
diversity at neutral molecular markers (Dlugosch & Parker 2008, Bock et al. 2015, Dlugosch et al.
2015).
3.2. Diversity Loss Is a Consequence of the Response to Selection
Diversity is lost not only through bottleneck events and spatial expansion, but also through responses to natural selection. For example, selective sweeps tend to reduce the average molecular
diversity in the vicinity of a favorable mutation (Maynard Smith & Haigh 1974). Most importantly, there is another process that could lead to observing a general decrease in genetic variation
potentially at the whole genome scale, which is often overlooked. Robertson (1961) pointed out
that in a population responding to selection, the relatives of a selected individual are more likely to
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be selected for, in the current and subsequent generations, because relatives resemble each other.
Hence, selection tends to increase the variance in numbers of progeny, grand progeny, and so on,
which reduces effective size and therefore increases homozygosity, not only at loci involved in the
architecture of the character, but also at all loci in the genome. Robertson’s (1961) model was subsequently extended and generalized (e.g., Santiago & Caballero 1995). The so-called Robertson’s
effect is well-known in the field of animal breeding (Hill 2007) but is surprisingly rarely discussed
in invasion or conservation genetics. The low genetic variation observed in some invasive populations may be the consequence of successful adaptation to new environmental conditions affecting
evolutionary rescue (see Section 5.2), in which case there is no genetic paradox of invasion.
4. GENUINE PARADOX
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We now discuss situations of invasive populations for which the genetic paradox is genuine, but we
argue that in these cases some features of population dynamics or of the genetic (and nongenetic)
systems allow the population to overcome the various deleterious consequences of low genetic
variation.
4.1. Bottlenecks Increase Population Fitness
In some situations, a depletion of genetic diversity induced by bottleneck events or selection may
increase population fitness and boost invasiveness.
4.1.1. Bottlenecks can have beneficial effects on ecologically relevant traits. The most striking example corresponds to the loss of diversity at so-called greenbeard genes (Gardner & West
2010). Greenbeard genes can identify the presence of copies of themselves in other individuals
and cause their bearer to behave nepotistically toward those individuals. In the red imported fire
ant (Solenopsis invicta), the invasive populations show a loss of polymorphism, probably linked to
founder events, in a gene that encodes an odorant-binding protein used in recognition (Krieger &
Ross 2002). As a consequence, the introduced populations display less aggression to conspecifics
from other colonies compared with native populations. Without aggression between colonies,
colony density and population size increase relative to the native range. This pattern of a loss
of genetic variation triggering a decrease in the strength of colony boundaries in introduced areas compared with native ones has been documented in other ants and termites (Suarez et al.
2008, Helanterä et al. 2009, Leniaud et al. 2009). Examples of greenbeard genes have started to
accumulate but thus far are limited to social insects and microorganisms (Gardner & West 2010).
4.1.2. Bottlenecks may contribute to purging deleterious mutations. Theoretical models
demonstrate that bottleneck events can purge the deleterious alleles that cause inbreeding depression, at least under certain demographic conditions (i.e., reduction of population size of intermediate intensity) and genetic inheritance patterns (i.e., strongly deleterious and highly recessive
alleles) (Glémin 2003). Such purging has also been demonstrated empirically in artificially bottlenecked populations (Crnokrak & Barrett 2002, Avila et al. 2010). Moreover, several theoretical
and empirical studies have established that inbreeding can increase the efficiency of purging over
a broad range of population sizes and for less strongly recessive deleterious alleles (e.g., Barrett &
Charlesworth 1991, Glémin 2003).
Rather than posing a barrier to invasion, bottlenecks and inbreeding that occur during
introduction events and in the invasion front may therefore enhance invasion ability by purging
deleterious alleles so that even inbred individuals have high fitness. This process has been observed
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in the invasion of the harlequin ladybird (Harmonia axyridis) (Facon et al. 2011). The bottleneck
that invasive populations passed through upon introduction was of intermediate intensity, which
corresponds to the theoretical conditions required for purging. Experiments reveal that invasive
populations experience almost none of the inbreeding depression suffered by native populations,
suggesting that deleterious alleles were purged in the course of invasion. Additional evidence of
purging of deleterious alleles in introduced populations was recently found in two other invasive
species: the garlic mustard plant (Alliaria petiolata) (Mullarkey et al. 2013) and the bed bug (Cimex
lectularius) (Fountain et al. 2014). Gathering case studies through both phenotypic and genomic
approaches (see Sections 5.3 and 5.4) will reveal the frequency at which purging is involved in
invasion success. Theoretical work is also needed to gauge the range of magnitudes and durations
of bottlenecks that make purging more likely after introduction from a large equilibrium population as well as during spatial expansion from the introduction point. Thus far, theoretical studies
investigating the purging of recessive mutations have mainly focused on mutation–selection–drift
equilibrium populations (e.g., Glémin 2003; but see Kirkpatrick & Jarne 2000).
4.1.3. Bottlenecks may increase additive genetic variance at ecologically relevant traits.
Both empirical and theoretical studies suggest that bottlenecks can contribute to the conversion
of nonadditive genetic effects (i.e., epistatic and, to a lesser extent, dominance effects) into additive
genetic variance on which selection can act (Turelli & Barton 2006, Van Heerwaarden et al. 2008;
see also references reviewed in Neiman & Linksvayer 2006, Dlugosch & Parker 2008). Researchers
have long been interested in this process, because it might explain how additive variation (but
not total genetic variation) might paradoxically increase after a bottleneck (Goodnight 1988).
Theoretical studies show that the conditions under which such conversion may occur are relatively
narrow (Turelli & Barton 2006). An increase in additive variation has sometimes been observed in
laboratory experiments, at least transiently, particularly for life history traits that are expected to
have many nonadditive genetic components (Neiman & Linksvayer 2006). However, whether this
increase has a significant impact on evolutionary potential remains unclear (Van Heerwaarden et al.
2008). A pattern of loss of global variation and gain of additive genetic variation during bottlenecks
has rarely been documented in natural systems. Two notable exceptions are high levels of additive
variation coupled with evidence of a bottleneck in island populations of the moor frog (Rana
arvalis) (Knopp et al. 2007) and a similar pattern seen in pitcher-plant mosquito (Wyeomyia smithii )
populations that have expanded their geographical range northward (Armbruster et al. 1998).
4.2. De Novo Mutations Are Frequent Enough to Restore Adaptive Potential
Generally, rapid adaptation stems from standing genetic variation (Barrett & Schluter 2008). This
assertion is thought to hold true for introduced populations, particularly given the timescale of
invasions. Mutations occur relatively rarely and, when they do occur, are initially at low frequency.
Thus, existing beneficial variants typically have higher initial frequencies than novel mutations,
increasing both the probability and the speed of their fixation (Barrett & Schluter 2008, Dlugosch
et al. 2015). However, recent studies suggest that mutation may in fact be common enough
to contribute to the genetic variation available for adaptation, even in the relatively short time
frame of an invasion (Lynch & Conery 2000, Ossowski et al. 2010). Furthermore, mutation
accumulation experiments frequently find evidence of beneficial mutations (Heilbron et al. 2014).
The ability of mutation to contribute meaningfully to variation on which selection acts is increased
by the polygenic basis of many traits linked to fitness. With multiple loci involved, there are
more opportunities for mutations to occur and thus increase adaptive potential after a bottleneck
(Lande 2015). Three main factors can increase the likelihood of adaptation being facilitated by
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new mutations during invasions. First, mutations that are neutral or even deleterious in the native
range may prove to be advantageous in the novel abiotic and biotic environment experienced in the
introduced range (Barrett & Schluter 2008). Second, at least at some point in the invasive process,
invasive populations display high growth rates that provide better opportunities for fixation of new
mutations (e.g., Otto & Whitlock 1997, Hallatschek & Nelson 2010). Third, for invasive species
with short generation times, opportunities for mutation are non-negligible even during the short
time frame of an invasion (Dlugosch et al. 2015).
The development of genomic technologies has already provided insight into two types of
mutations that might significantly contribute to adaptive processes during invasion. One type is
copy number variation (CNV) (Lynch & Conery 2000), which occurs at nearly the same rate
as point mutations but seems to result more frequently in beneficial phenotypes (Hirase et al.
2014). Although their impact in rapid adaptation remains unclear (but see Gaines et al. 2010),
CNV could potentially restore adaptive potential in genetically depauperate invasive populations
(Dlugosch et al. 2015). The second type is transposable elements, which are known to contribute
to adaptation (e.g., Casacuberta & González 2013, Stapley et al. 2015). Transposable elements
can be activated by biotic and abiotic stress (e.g., Walbot 1999, Capy et al. 2000), a situation
frequently encountered by invasive populations experiencing a new habitat. Higher activity of
transposable elements may in turn produce genetic variation and therefore increase the rate of
introduction of potentially beneficial alleles (Stapley et al. 2015). The best experimental evidence
of an adaptive role of transposable elements during invasion comes from Drosophila species. For
instance, several transposable elements seem to have been selected for during the invasion of North
America by Drosophila melanogaster less than 200 years ago (González et al. 2008). Similarly, invasive
populations of D. buzzatii and D. subobscura display high frequencies of transposable elements
compared with native populations (Garcı́a Guerreiro et al. 2008, Garcı́a Guerreiro & Fontdevila
2011).
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4.3. Adaptive Phenotypic Plasticity Tempers the Adaptive Challenge
Adaptive plasticity can enable populations to move toward a new adaptive optimum in an introduced area despite potentially lower genetic variation (Richards et al. 2006, Davidson et al. 2011).
Adaptive plasticity encompasses three different strategies (Bock et al. 2015): (a) It may allow fitness
of an invader to be maintained across several unfavorable environments (termed the Jack-of-alltrades strategy), (b) it can increase the fitness of an invader under some favorable conditions
(the master-of-some strategy), and (c) invaders are able to combine both abilities (i.e., the Jackand-master strategy). Milberg et al. (1999) compared five Asteraceae plant species introduced to
Australia with five native species across a nutrient gradient. They showed that the invasive species
could increase their biomass more at high nutrient levels than native species could, suggesting
a master-of-some strategy may be common in invasive species. In animals, Yeh & Price (2004)
showed that a plastic response in the length of the breeding season increased the invasiveness of
the dark-eyed Junco ( Junco hyemalis).
The genetic mechanisms responsible for plasticity are not yet well understood. Plasticity was
initially associated with autogamy, apomixis, vegetative reproduction, hybridization, and polyploidy (Baker & Stebbins 1965). More recently, several plasticity genes, such as loci with environmentally sensitive alleles and regulatory loci that modify gene expression levels across different
environments, have been characterized (Des Marais et al. 2013). Finally, evidence that epigenetic modifications such as DNA methylation and chromatin modification play a role in adaptive
plasticity has also been found (Bastow et al. 2004; see also Section 4.4).
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Thus far, how often and to what extent adaptive plasticity drives invasion success remains unclear. A common idea is that invasive species generally display more adaptive plasticity allowing
them to cope better with new environments in introduced areas (Richards et al. 2006). However, recent meta-analyses have reached opposite conclusions indicating that adaptive plasticity is
not necessarily advantageous in the context of invasion (Davidson et al. 2011, Palacio-López &
Gianoli 2011). These conflicting results might be reconciled by consideration of the transient
nature of plasticity (Lande 2009). After an initial benefit from plasticity, an invader may lose its
ability to express different phenotypes in favor of the expression of a locally adapted fixed phenotype through genetic assimilation (Lande 2015). Theory indicates that a correlation of colonization
with increased plasticity depends on the difference in the optimal phenotype between ancestral and
colonized environments; the difference in mean, variance, and predictability of the environments;
the cost of plasticity; and the time elapsed since colonization (Lande 2015). Theoretical studies
also show that the frequency of environmental fluctuations determines whether we can expect an
adaptive response through local adaptation (if the fluctuations are rare) or through phenotypic
plasticity (if the fluctuations are frequent compared with the generation time). Disturbance occurring on rapid timescales would tend to select for adaptive plasticity that may increase organismal
flexibility (Meyers et al. 2005).
4.4. Diversity Loss Is Compensated for by Epigenetic Processes
Empirical evidence that phenotypic variation can be transmitted independently from DNA polymorphism inheritance is growing (reviewed in Danchin et al. 2011). Such epigenetic phenomena
provide an information layer above the DNA sequence level and can contribute to variation in
gene expression and phenotype via multiple molecular mechanisms including DNA methylation,
histone modifications, small RNAs, and noncoding RNA (Kinoshita & Jacobsen 2012). The evolutionary significance of these nongenetic mechanisms of inheritance is under animated debate
that divides scientists (Bonduriansky & Day 2009, Mesoudi et al. 2013).
Some epigenetic modifications may be heightened by abiotic and biotic factors, allowing organisms to respond quickly to a new environment (Dowen et al. 2012, Schrey et al. 2012). Thus,
epigenetic variation has been suggested to provide a source for the phenotypic diversity found in
recently introduced populations and be an important mechanism by which invasive populations
succeed in novel environments. More specifically, epigenetic modification of gene expression
might weaken the deleterious effects of bottlenecks by allowing organisms to adjust their phenotypes to match novel environments (Bock et al. 2015). Additionally, the process of invasion
itself may increase epigenetic variation through increased contact with environmental stressors
( Jablonka 2013) and exposure to population bottlenecks (Rapp & Wendel 2005). Examples of a
role for epigenetic shifts in compensating for losses in genetic variability are accumulating (Liebl
& Martin 2012, Bock et al. 2015, Rollins et al. 2015). In keeping with this trend, studies on
different invasive house sparrow (Passer domesticus) populations have found a significant negative
relationship between genetic and epigenetic (DNA methylation) diversity and also between levels
of DNA methylation and age of introduction in invasive house sparrows (Schrey et al. 2012, Liebl
et al. 2013).
5. THE PATH TO NEW INSIGHTS INTO THE GENETIC PARADOX
OF INVASIONS
We now propose a nonexhaustive set of possible research directions to gain further insights into
some remaining paradoxical aspects of invasion genetics.
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5.1. Using Data from Standard Neutral Genetic Markers More Effectively
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The characterization of relatively few neutral genetic markers is clearly insufficient to decipher
the role of selection in invasion success (Dlugosch et al. 2015). However, neutral genetic markers
remain informative for identifying key evolutionary events such as bottlenecks and/or admixture
that shape genetic variation in introduced populations. Because different metrics of genetic variation at molecular markers reveal different aspects of the potentially complex story of an invasive
population (e.g., Estoup & Guillemaud 2010), the choice of the statistics used to summarize genetic diversity is crucial. Both Dlugosch & Parker (2008) and Uller & Leimu (2011) found that
allelic diversity and/or heterozygosity of nuclear markers were the most commonly used metrics
of diversity. Given this finding, they limited their review to studies that reported these values for
introduced and source populations. Similar choices were made in other reviews of this type (e.g.,
Bossdorf et al. 2005, Roman & Darling 2007). Unfortunately, these traditional metrics of genetic
diversity are poor at detecting genetic admixture, which is hypothesized to play an important
role in invasions, especially when such admixture occurs concomitantly with intense bottleneck
events. A better summary statistic to detect admixture is allele size variance at microsatellite loci
(the most frequently used marker type to date). We illustrate this issue using computer-simulated
data sets presented in the Supplemental Material (follow the Supplemental Material link from
the Annual Reviews home page at http://www.annualreviews.org).
Most importantly, to thoroughly study changes in genetic diversity as well as adaptation or
other processes that may occur during and after introductions, it is crucial to identify the original
source(s) of the introductions. The source region(s) provide the benchmark against which genetic
and evolutionary changes are assessed; thus, identifying source region(s) is crucial to evaluating
whether apparent evolutionary changes are valid or simply reflect regional differences (i.e., local
adaptation, drift, and evolutionary history) between the true source population and the area sampled for study (Dlugosch & Parker 2008, Keller & Taylor 2008). This important question has
motivated the development of recent statistical methods in population genetics for reconstructing the routes of invasion even from relatively few neutral genetic markers genotyped in native
and invasive populations of a species (Estoup & Guillemaud 2010, Cristescu 2015). In particular,
approximate Bayesian computation (ABC) methods provide useful quantitative inferences in the
complex evolutionary scenarios typically encountered in invasive species (Estoup & Guillemaud
2010). ABC methods should be preferentially envisaged for optimal use of the information provided by a large set of summary statistics, which may describe most of the molecular information
at neutral genetic markers within and between populations.
5.2. More Theoretical Studies to Characterize the Factors Influencing
the Dynamics of Adaptation During Invasions
A growing body of theory investigates the role of evolution during invasions. To understand the
role of evolution requires modeling complex population dynamics and its interplay with evolutionary forces (mutation, migration, drift, and selection) and presents considerable theoretical
and methodological challenges. More specifically, a better characterization of the effects of strong
demographic disequilibrium induced by bottlenecks and/or admixture on genetic variation at
quantitative traits is required, particularly when the underlying genetic architecture is complex.
Thus far, most theoretical studies of the determinants of invasion success have been simulation
models with explicit genetic architecture of the traits under selection and demographic stochasticity (e.g., Holt et al. 2003). Few studies have explicitly taken into account spatial aspects as well
(e.g., Travis et al. 2005, Peischl & Excoffier 2015).
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a
N0
c
Fitness
Population size
Environmental change
Minimum viable
population size
b
Recurrent migration into
a novel environment
High risk of extinction
Time
Population growth
Growth rate
Fitness
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Trait
Adaptation
0
Population decline
Previous
optimum
New
optimum
Trait
Time
Figure 2
The most commonly modeled scenarios of evolutionary rescue and potential links to biological invasion. Evolutionary rescue is
adaptation to a challenging environment that increases intrinsic fitness and enables a population to escape from extinction. Biological
invasions can be considered special cases of evolutionary rescue, in which the environmental change is sudden and caused by an
introduction into a novel environment. Most current models of evolutionary rescue assume either (a) that a population at demogenetic
equilibrium experiences an abrupt or gradual change of environment or (b) that a new environment is colonized by the recurrent
migration of individuals from a source population. An important feature absent from most evolutionary rescue models is consideration
of how the introduction process itself (bottleneck, multiple introductions from potentially genetically differentiated sources, etc.) affects
the kind of genetic variation available right after introduction. A typical evolutionary rescue scenario is detailed in panel c. A population
experiences an environment where it suffers from severe maladaptation. The population size first decreases so that extinction is
unavoidable in the absence of evolution. N0 indicates the initial population size just after environmental change.
Biological invasions may, to some extent, be considered special cases of evolutionary rescue.
Evolutionary rescue occurs when a population that is expected to go extinct in a given environment
nonetheless persists because evolution by natural selection increases fitness rapidly enough to
prevent extinction (e.g., Gonzalez et al. 2013). Most models of evolutionary rescue study the
persistence of populations for which the environment changes more or less gradually (Figure 2).
Most theoretical studies agree that evolutionary rescue and thus invasion success are facilitated by
large initial population sizes, large initial genetic variation, high mutation rates, and phenotypic
plasticity. Yet, these studies also show that genetic variation expressed during different points in
the life cycle (birth rates, reproductive values, survival) can have different effects on the probability
of rescue (e.g., Gandon et al. 2013, Martin et al. 2013). The models generally predict that invasion
is facilitated when ecologically relevant traits are encoded by few loci. Furthermore, with complex
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quantitative genetic architectures, and when loci contribute unequally to fitness, both the pace of
adaptation and the vulnerability to extinction depend in complex ways on gene interactions and
on the initial genetic structure of the introduced population (Gomulkiewicz et al. 2010).
Though in many ways the concept of evolutionary rescue is relevant to invasions, most models
include neither a bottleneck nor admixture. Thus, the genetic variance on which selection operates
is that of an entire population at equilibrium, not that of a small propagule or a mix of propagules. Only a small fraction of evolutionary rescue models specifically deal with invasion into a
novel environment (i.e., with an explicit introduction step into a new area) (Holt et al. 2005). The
new environment may be homogeneous and constant, or heterogeneous and temporally variable.
Although spatial heterogeneity may have contrasting effects on invasion success, temporal variability tends to facilitate invasion (Holt et al. 2005). These studies, however, generally consider
recurrent migration from a single source population into the novel environment rather than the
one-time introduction of a small propagule (Travis et al. 2005). One important conclusion of these
studies is that, as foreseen in models of niche evolution (e.g., Ronce & Kirkpatrick 2001), high
recurrent migration rates may hamper invasion by introducing maladapted genes.
Overall, theoreticians have made significant progress during the last few years integrating
complex genetic architecture of fitness traits and demographic disequilibrium into their models.
Still, an important feature of invasion biology remains absent from the present theoretical literature: how the introduction pattern itself affects the kind of genetic variation available right after
introduction. As suggested by Gomulkiewicz et al. (2010), genetic architecture and the genetic
composition of the introduced population (diversity, linkage, and substructure) may interact to
determine the likelihood of invasion success. Moreover, the genetic composition of the introduced
population depends on the details of the introduction: Rare alleles can be lost, novel genotypes
can emerge, and gene interactions may be modified (Dlugosch et al. 2015). How these features
affect invasion success remains to be explored.
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5.3. More Experimental Studies to Test Theoretical Expectations
Our understanding of the frequency with which low genetic variation prevents adaptation to a
novel environment is limited by our inability to know how many introductions fail to establish and
the reasons for those failures. There are two main ways to address this lacuna in our knowledge.
First, using mesocosms and microcosms, the role of genetic diversity in successful founding and
adaptation can be tested experimentally. A growing body of literature exists on this front (reviewed
in Szucs et al. 2014). Much of this research, however, stops with initial establishment, and the
role of genetic diversity over multiple generations in staving off extinction and facilitating adaptation remains an area ripe for experimental research. Second, we can capitalize on introduction
scenarios for which we have data on both successes and failures: namely, populations that humans
have purposefully introduced into new ranges. This includes organisms used in classical biological
control (Fauvergue et al. 2012) and species introduced as sources of food or for other human endeavors (fish, foxes, many birds; e.g., Duggan et al. 2006). The challenge with these introduction
scenarios is that although the numbers of individuals released is typically known, their genetic
background is not. Moreover, evidence has been found that mass rearing of biological control
agents in the laboratory induces genetic changes of life history traits that may subsequently translate into maladaptation to natural habitat and hence affect successful establishment in the wild
(e.g., Leider et al. 1990, Tayeh et al. 2012). Nevertheless, experimental evidence indicates that
invasion success increases with the number of individuals released (e.g., Simberloff 2009, Uller &
Leimu 2011). However, the degree to which this pattern is driven by demographic effects and the
degree to which it is driven by genetic effects remain unclear. The few experimental studies that
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attempt to disentangle demographic and genetic mechanisms certainly suggest that both mechanisms are involved (Hufbauer et al. 2013, Szucs et al. 2014). Future purposeful introductions
(e.g., for biological control or reintroductions of species during conservation efforts) should include the collection of tissue for genetic analyses. Ideally, such introductions would also be done
in an experimental context, with different levels of genetic diversity as a treatment in replicated
introductions. Such studies are not feasible for many purposeful introductions but should be for
biological control, in which the organisms (typically insects) are often biologically suitable for
creation of groups with different genetic backgrounds, and replicated releases.
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5.4. New Insights from High-Throughput Sequencing
and Genotyping Technologies
The advent of high-throughput sequencing and genotyping methods and their application to
nonmodel species have provided new opportunities to address key issues regarding the genetics
of invasive species. More particularly, cost-effective molecular approaches, such as genotyping
by sequencing (GBS) (Elshire et al. 2011), allow genotyping of a reasonably large number of
individuals at several thousands of markers, even in the absence of a reference assembly genome
for the species of interest. Similarly, the sequencing of pools of individual DNA (an experimental
process termed Pool-seq; Schlötterer et al. 2014), allows efficient characterization of the pattern
of genetic diversity within and across populations on a genome-wide basis, leading to a further
reduction of sequencing costs while maintaining and sometimes increasing precision in allele
frequency estimation (Gautier et al. 2013).
The resulting large data sets can be quite informative about the demographic history of the genomically characterized populations. For instance, such data make it possible to assess the multiple
origins of an invasive population even if potential sources are only weakly genetically differentiated.
Admixture between weakly differentiated populations is predicted to facilitate invasion (Dlugosch
et al. 2015). Thus far, testing this prediction has been difficult, owing to the lack of resolution
provided by standard genetic markers. Tests based on the F-statistics as defined in Patterson et al.
(2012) make it possible to test explicitly for admixture events (F3 -statistic) and to estimate admixture proportions (ratio of F4 -statistics) from allele frequency data obtained from high-throughput
sequencing and genotyping methods. Interestingly, such tests are powerful when only proxies of
the source populations are sampled. Several recently developed methods relying on the observed
site frequency spectrum (Guntenkunst et al. 2009, Excoffier et al. 2013) appear particularly well
suited to characterize the complex evolutionary history of invasive populations accurately, including delimiting the intensity of possible bottlenecks (e.g., Alcala et al. 2016). Finally, ABC methods
(Cornuet et al. 2014), especially recently developed ones (e.g., ABC random forest; Pudlo et al.
2016), are also well suited to analysis of large SNP data sets and can distinguish among complex
evolutionary scenarios.
In addition to demographic inference, population (and quantitative) genomics approaches based
on high-throughput sequencing and genotyping technologies are quite promising for studying the
evolution of phenotypic traits in natural populations (Wray 2013). Specifically, they can be used
to better understand the genetic architecture of traits underlying invasion success (Bock et al.
2015). Genetic differentiation of invasive populations from native source populations via scanning
along the genome for adaptive differentiation will provide powerful insights into recent invasions
even if overall differentiation is low. A wide range of statistical approaches have already been
proposed and thoroughly evaluated in different contexts (e.g., Vitti et al. 2013, Lotterhos &
Whitlock, 2014, Vitalis et al. 2014). Among these, a promising approach is treating the historical
origin of populations (i.e. invasive versus native) as a categorical trait in analyses characterizing
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the association of ecological variables with genetic differentiation along the genome (e.g., Gautier
2015). A limitation of such indirect (or bottom-up) approaches lies in the biological interpretation
of the footprints of selection: Explaining differences is prone to telling “just so” stories (Pavlidis
et al. 2012). In any case, a detailed annotated genome for the species of interest or a closely related
model species is a minimal requirement to identify relevant candidate physiological pathways (e.g.,
Flori et al. 2009) and hence candidate traits associated with invasion. Such candidate traits can
be subsequently studied in more detail in either experimental or natural populations following a
reverse ecology framework (Li et al. 2008).
If a measurable trait is available, standard quantitative genetics approaches can be used to
map quantitative trait loci in experimental populations (e.g., crosses between invasive and source
populations) or outbred populations (i.e., genome-wide association studies) to identify relevant
candidate genes. The effort required in terms of sampling may constitute a serious limitation
for nonmodel species. In this case, using evolve and resequence approaches to investigating the
genomic responses to selection during experimental evolution is an attractive alternative (e.g.,
Schlötterer et al. 2015).
The characterization of the genetic architecture of traits involved in invasiveness is expected
to provide multiple useful insights. For example, (a) the number and effect of genes involved;
(b) the relative influence of large-scale variants such as the so-called supergenes in situations of
major adaptive shifts (i.e., clusters of tightly linked loci; Schwander et al. 2014); (c) the relative
importance of selection on de novo mutation versus standing variation (Peter et al. 2012); and
(d ) the assessment of purging of deleterious variants or expansion load, for example, by comparing the relative proportion of synonymous and nonsynonymous coding variants (or other kinds
of functional variants) within the selective sweeps detected in the genome of an invasive population. Such new genomic investigations will certainly contribute to a better understanding of the
remaining spurious and genuine situations of genetic paradox in invasive species.
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6. CONCLUSIONS
In this review, we attempt to shed new light on the dilemma in invasion biology referred to as
the genetic paradox of invasions. That is, how bottlenecked invasive populations, which typically
have low genetic diversity and hence are believed to have low evolutionary potential and/or low
reproductive fitness, can become invasive. Our main findings are succinctly displayed in Figure 3.
We argue that, though the notion of a genetic paradox of invasion is intuitive and possible in
theory, it is to a large extent overrated. Instead, many invaders either have genetic diversity similar to or even greater than natives or do not face significant adaptive challenges in the invaded
area. Some invasive populations do seem to combine all the conditions of a genetic paradox but,
because the proxy used to characterize genetic variation is inadequate, the paradox is in fact spurious. More specifically, in this situation, the diversity loss at a small set of neutral genetic markers
is not reflected in genetic variation of ecologically relevant traits. Alternatively, genetic variation
at neutral loci and ecologically relevant traits can be low owing to successful adaptation to new
environmental conditions. In some invasions, however, the genetic paradox is genuine. We argue
that in these cases a diverse array of mechanisms allows the invasive population to overcome the
various deleterious consequences of low genetic variation and adapt to its novel environment.
Such mechanisms include an increase in population fitness promoted by demographic bottleneck
event(s) (via beneficial effects on particular traits, purge of deleterious mutations, and/or conversion of epistatic to additive variance) and compensation for the loss in genetic diversity by adaptive
phenotypic plasticity or epigenetic changes.
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No genetic paradox
Native range
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VG-N
Introduced range
VG-N
VG-A
VG-A
VG-N
VG-N
Introduced populations show
comparable or greater
genetic diversity relative to
native populations, owing to
multiple introductions. They
have adapted to the novel
environment (represented by
match of adaptive variation to
the new background color)
Introduced populations may
have lower genetic diversity
than the native range, but
there is no adaptive challenge
owing to prior adaptations
including AIAI effects*
VG-A
Genetic variation at
neutral loci
Genetic variation at
VG-A ecologically relevant
adaptive traits
b
Spurious genetic paradox
Native range
VG-N
Introduced range
VG-N
VG-A
Loss in diversity at neutral loci is
not reflected in adaptive traits.
The loss of quantitative variation
during invasion is generally
smaller than the loss of diversity
at neutral markers
VG-A
VG-N
VG-A
Global loss in diversity is a
consequence of successful
response to strong
selection pressures**
Figure 3
Schematic recapitulation of the different situations corresponding to (a) no genetic paradox, (b) spurious
genetic paradox, or (c) genuine genetic paradox, showing the different mechanisms used by invaders to
escape genetic constraints and adapt to their novel environment, hence resolving the apparent genetic
paradox in panel c. (∗ ) Fundamentally, anthropogenically induced adaptation to invade (AIAI) (Hufbauer
et al. 2012) begins with contemporary local preadaptation; however, rather than adapting to the native
habitat, species adapt to new human-altered habitats located within the species’ native range. (∗∗ ) A strong
selective process, owing to successful adaptation, may cause a general decrease in genetic variation at the
whole genome scale. (∗∗∗ ) A striking example is the case of introduced populations of the eusocial invasive
fire ant (Solenopsis invicta), which show a loss of polymorphism, probably linked to founder events, in a
recognition gene. As a consequence, the introduced populations display less aggression to conspecifics so
that colony density and population size become higher than in the native range (Krieger & Ross 2002).
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c
Genuine genetic paradox
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Native range
VG-N
VG-A
VG-N
VG-A
VG-N
VG-A
VG-N
VG-A
Plasticity
VG-N
VG-N
VG-A
Genetic variation
at neutral loci
Introduced range
VG-A
A particular life
history makes reduced
variation at some traits
advantageous***
VG-N
VG-A
Conversion of epistatic
variation to additive
genetic variation
VG-N
VG-A
The bottleneck imposed
upon introduction
increased fitness via purge
of deleterious mutations
VG-A
Diversity loss is compensated
for by (increased) adaptive
phenotypic plasticity
VG-N
VG-N
Plasticity
VG-N
VG-A
Genetic variation at
VG-A ecologically relevant
adaptive traits
Diversity loss is compensated
for by epigenetic processes
Deleterious
mutations
Epigenetic
changes (e.g.,
methylation)
Figure 3
(Continued )
Like any paradox in science, there is only one solution: To definitively resolve the genetic
paradox of invasion, we need more science. To this end, we propose a nonexhaustive set of possible
research directions to gain further insights into some remaining paradoxical aspects of invasion
genetics. Fruitful research approaches include more rigorous analyses of standard data sets of neutral genetic markers, more theoretical studies to characterize the factors influencing the complex
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dynamics of adaptation during invasions, more experimental studies to test theoretical expectations, and the application of high-throughput sequencing and genotyping methods to invasive
species.
DISCLOSURE STATEMENT
The authors are not aware of any affiliations, memberships, funding, or financial holdings that
might be perceived as affecting the objectivity of this review.
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ACKNOWLEDGMENTS
All authors thank Daniel Simberloff for inviting and motivating us to write this review.
A.E., B.F., and M.G. acknowledge financial support by the national funder ANR (France)
through the European Union program ERA-Net BiodivERsA (project EXOTIC), the Languedoc
Roussillon region (France) through the European Union program FEDER FSE IEJ 2014–2020
(project CEPADROL), and the INRA scientific department SPE (AAP-SPE 2016). V.R. acknowledges financial support by the European Union regional development fund (ERDF), the Conseil
Départemental de la Réunion, the Région Réunion, and the French Agropolis Fondation (Labex
Agro–Montpellier, E-SPACE project number 1504-004). R.H. acknowledges support from the
National Science Foundation (DEB-0949619), USDA Agriculture and Food Research Initiative award (2014-67013-21594), and the French Agropolis Fondation (Labex Agro–Montpellier)
through the AAP “International Mobility” (CfP 2015-02).
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