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ES47CH03-Estoup ARI V I E W 7:18 Review in Advance first posted online on August 4, 2016. (Changes may still occur before final publication online and in print.) A N I N C E S R E 9 July 2016 D V A Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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. 51 Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 1. INTRODUCTION Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 52 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 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 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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, www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 53 ARI 9 July 2016 7:18 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). Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup 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 54 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 55 ES47CH03-Estoup ARI 9 July 2016 7:18 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 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 56 Estoup et al. Changes may still occur before final publication online and in print Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup ARI 9 July 2016 7:18 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 www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 57 ARI 9 July 2016 7:18 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). Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup 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). 58 Estoup et al. Changes may still occur before final publication online and in print Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup ARI 9 July 2016 7:18 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. www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 59 ES47CH03-Estoup ARI 9 July 2016 7:18 5.1. Using Data from Standard Neutral Genetic Markers More Effectively Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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). 60 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 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 Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 61 ARI 9 July 2016 7:18 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup 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 62 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 63 ARI 9 July 2016 7:18 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. ES47CH03-Estoup 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. 64 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI a 9 July 2016 7:18 No genetic paradox Native range Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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). www.annualreviews.org • Genetic Paradox in Invasion Changes may still occur before final publication online and in print 65 ES47CH03-Estoup ARI 9 July 2016 7:18 c Genuine genetic paradox Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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 66 Estoup et al. Changes may still occur before final publication online and in print ES47CH03-Estoup ARI 9 July 2016 7:18 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. Annu. Rev. Ecol. Evol. Syst. 2016.47. Downloaded from www.annualreviews.org Access provided by Northern Illinois University on 08/25/16. For personal use only. 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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