Abstract  

       

     Invasive species are known for their rapid evolutionary change and ability to modify community structure and ecosystems. They can displace native species, alter nutrient cycling and hydrology, and disrupt ecological interactions. Not only do they affect how the environment functions, these “natural pests” can also de detrimental to human health and conservation efforts. The hybrid mechanism to invasion has been studied extensively over the past several years and can explain numerous instances of invasion. Invasive plant evolution and establishment confers many patterns, of which include geographical isolation, multiple human introductions, and the lag time it takes for invasiveness to evolve. During this process, reproductive barriers, damaging alleles, and genetic bottlenecks could challenge new hybrid species. Introgression during hybridization and polyploidy speciation can mix up genetic material and create the conditions necessary for invasion. Once these are in place, the invasive plant’s success is dependent upon at least one of four pathways: fixed heterosis, increased genetic variation, evolutionary novelty, and a purged genetic load. These function to increase the invasive’s fitness and facilitate its spread.

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Introduction



     There has been much focus on invasive species over the last decade. Scientists have been attempting to answer questions from down to the genome level of what determines plant invasiveness to the ecological effects of invasion. Many non-mutually exclusive hypotheses have been proposed on how a species becomes invasive. These have included single gene mutations, competitive ability, occupation of an unfilled niche, and ecological release (Jain and Martins 1979) (Ellstrand and Schierenbeck 2000). A great deal of attention has been given to the enemy-release hypothesis, which states competition, predation, or parasitism may drive a species into a narrow niche in its native range, but when the species colonizes a new range, it is released from these constraints. These hypotheses assume that invasives are “born”, ready to colonize and invade without much genotypic change (Ellstrand and Schierenbeck 2000). However, these are not the only pathways to invasiveness. Invasives can also be “made”, evolving invasiveness after colonization. The idea of evolutionary change as a precursor to invasiveness was once controversial, but now it is well known and documented.

     During hybridization, two closely related interspecific or intraspecific plants mate to produce a genetic intermediate. This can generate novel phenotypes and increase the level of genetic variance- some of the potential requirements necessary for invasion. Interspecific hybridization has been shown to generate new stabilized plant species capable of spreading beyond their origin and colonizing a new range. For these reasons, it has been suggested that that hybridization, itself, can stimulate invasiveness.



Invasive evolution and establishment



     Hybridization between lineages and populations



     Invasiveness can evolve through a few different pathways, causing a rainbow of patterns to manifest in the invaders. Yet, there are many shared patterns among invasive lineages. Through knowing the patterns and processes, can invasiveness be predicted? For example, a general invasive predictor includes whether the organism has been invasive somewhere else (Ewel et al. 1999). If so, it is likely to display invasive traits in another range. Predicting invasive potential starts with asking which plants hybridize.

     Plants of the same genotype from different parts of the same geographic range have been shown to hybridize. This hybridization event can lead to stable hybrid zones, but will most likely not generate an invasive phenotype. To establish an invasive lineage, native taxa can either hybridize with introduced taxa or two introduced taxa of divergent lineages can hybridize with each other. It is more common for one native and one alien species to hybridize, because the establishment of the invasive hybrid only takes the introduction of one species, not two. A study of hybrids in Britain reinforces this concept. Eighty-seven hybrids were the result of one native and one alien taxa, while twenty-six hybrids originated from the mating of two non-native species (Abbott 2003).  However, two divergent non-native taxa may be settled together in the same time span from the same or different source locations. This was the case with Brachypodium sylvaticum, an invasive grass in the Pacific Northwest. The invasion of B. sylvaticum resulted from many alien introductions into the same range.



     Intraspecific hybridization



In addition to two interspecific taxa hybridizing, intraspecific hybridization, or hybridization between two populations of the same taxa, may occur. For intraspecific hybridization to play a role in invasion, three criteria must be met. The populations must exhibit some genetic differentiation, there must be multiple introductions into the range with more than one source population, and contact must be made between the natives (or non-natives) and non-natives, leading to novel traits with invasive behavior (Wolfe et al. 2007). After the colonization of B. sylvaticum, it underwent intraspecific hybridization between differentiated species and evolved novel genotypes. In this example, there are not any indications of the species undergoing interspecific hybridization after introduction. However, this is a rare case, as many invasive hybrids are the product of two interspecific populations (Rosenthal et al. 2008).



     Hybridization can occur between closely related populations or distantly related populations. If hybridization happens in closely related populations it may not lead to any significant evolutionary changes. This might be because sympatric species may have greater interbreeding barriers than species that are allopatric (Huxel 1999). Though any significant changes depend on many factors, one being relative geographic distance. Galloway and Etterson (2005) found that hybrids from nearby populations (less than 1.5 km) outperformed their parents. In the same study, they discovered that F1 hybrids between distant populations (more than 550km) had lower fitness compared to their parents. Only a handful of hybridization events will lead to progeny with superior fitness. Yet, these offspring may not become invasive if the biotic and/or abiotic environment does not allow for it.



     Human’s role in establishment



     Hybridization between related species of distant origin is usually perpetuated through the action of humans. Anderson and Stebbins (1954) suggested that humans are causing a breakdown in ecological isolation, bringing previously isolated species together and increasing the potential for hybridization and invasiveness. Anderson had previously described this process as ‘hybridization of the habitat’. The potential for hybridization, can be increased through habitat destruction, which opens niches for new lineages to thrive in, or through transportation.

     Many plant species were moved overseas during the last several centuries, when not much was known about the consequences of hybridization and invasive species. Several surveys of invasives point to the Mediterranean or Central Europe as the native range (Ellstrand and Schierenbeck 2000). The plants followed trading routes, and as trade grew, the number of invasives increased correspondingly. Currently, a disproportionate number of invasive plants are found in the new world and tropical areas. They are less likely to establish in temperate old world zones.



     Multiple Introductions

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     These across-population introductions are not always successful in establishing an invasive hybrid. Similar to the introduction of B. sylvaticum, a non-native plant species may require multiple introductions into the native range before it becomes invasive (Barrett and Husband 1990). At low population densities, the introduced species may not be able to survive and reproduce, but given a constant flow of introductions, the population will grow large enough for the species to maintain itself. Tamerix, a North American invasive that outcompetes native trees and salinizes the soil, is an example of a plant that was established through multiple introductions. Multiple introductions can also increase genetic diversity in the introduced range, though high genetic diversity may also occur through introgression after introduction and may be difficult to discriminate (Rosenthal et al. 2008). In sum, the frequent arrival of genetically distinct individuals into the foreign range may allow hybridization to take place and invasiveness to evolve.



     Lag time



     Usually correlated with geographical displacement and multiple introductions is the time involved that it takes for exotics to hybridize, evolve novel phenotypes, and become invasive. Rapid adaptation through evolutionary novelty or increased genetic variation may not always be the case in invasive evolution (Abbott 2003). The lag time associated with invasive behavior may be correlated with the selection processes that favor adapted genotypes from the recombinants (Kowarik 1995).  The lag time may occur over years, because it depends on the species life cycle, abundance, and other ecological factors. Kowarik (1995) looked at 184 invasive woody species and found, on average, it took 131 years for shrubs and 170 years for trees to become invasive. The results suggest that some species are not pre-adapted, but must evolve invasiveness after a long lag time.          

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Challenges during hybridization

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Apart from how invasive hybrids become established, they may also run into barriers along the way. Hybrid plant species can encounter reproductive barriers, lose advantageous alleles, or go through a genetic bottleneck, all of which can slow the rate of invasive establishment or affect the spread of invasive genotypes.



     Barriers

     

     Not all hybridization events will be successful, as many hybrids do not survive due to hybrid incompatibility or lethality of genes (Chen 2010). A

disadvantageous mating or lineage depends on the establishment of reproductive barriers and the relatedness between populations. Prezygotic and postzygotic barriers can evolve that keep lineages separate. Overcoming these barriers can be a challenge. Prezygotic barriers that can develop include habitat, temporal, and behavioral barriers (Rieseberg and Carney 1998). Post-zygotic barriers might include hybrid sterility or breakdown as well as hybrid weakness or inviability (Rieseberg and Carney 1998).

     Outbreeding between two populations increases genetic diversity, but gene flow between populations too far apart may lead to a or breakup of co-adapted gene complexes (Wolfe et al. 2007). Distant mating might result in a loss of local adaptation and eventually lowered fitness (Lippman and Zamir 2007) (Wolfe et al. 2007). If an individual mates with another individual in the same population, deleterious recessive alleles can be brought together and inbreeding depression might result. However, species may not be subject to the above barriers and it is possible for a hybrid zone to develop. The species still might not be able to hybridize successfully as new barriers are able to develop that inhibit hybridization.



     Bottlenecks



     A species that has recently colonized a new range and hybridized with a native species may find itself in a genetic bottleneck. The newly formed hybrid is likely to be cut off from the founding population, leading to lowered genetic diversity and heterozygosity in the invasive populations compared to the native population (Rosenthal et al. 2008).

     The evidence of a bottleneck due to founder effects in the introduced range is seen in B. sylvaticum. When two species of non-native B. sylvaticum hybridized in the introduced range, only a small fraction of the total genetic diversity in the species was represented, with no gene flow detected between the ranges (Rosenthal et al. 2008). Still, the evidence of a bottleneck can be difficult to identify, as it may be possible that the evidence of one was erased by gene flow via wind. The consequences for a lack of gene flow during invasion may not be that great considering the low genetic diversity found in some extremely successful invasive hybrids. However, in many instances, a diverse genome does contribute to the establishment of hybrid invasives and deserves consideration.



Introgression and polyploidy



     The establishment of and challenges encountered in invasive plant hybrids has revealed some common patterns. Not yet addressed are some of the hybridization mechanisms that can lead to a plant’s invasive qualities. As we will see, stable, invasive hybrid species can result from introgression or polyploidy.



Introgression



     Defined, introgression is the repeated backcrossing of genes between the hybrid and parental generation. It is a common source of genetic variation that can have important effects on the evolution of a species and the establishment of an invasive species. Introgression is a powerful force that can dictate the success of an invasive hybrid lineage. Much of the genome appears to be permeable to introgression, despite linkage, because reproductive barriers are under genetic control (Rieseberg and Carney 1998). However, too much recombination between populations may reduce viability and fertility, while too little recombination may stop introgression.

     The uncovering of introgressed phenotypes reveals some interesting trends.  For example, rare genotypes can become common and increase when they backcross with non-native taxa. Additionally, introgressed individuals may adapt more efficiently and colonize new habitats through range expansion (Abbott 2003). A hybrid swarm might form in the process, and as the frequency of native genotypes decreases and the invader’s genotype increases, displacement of the native species is likely through increased assimilation or environmental stochasticity (Huxel 1999). Invasive populations only contain a small portion of the total genetic diversity found in the native range. In the case of introgression, the admixture between populations and continued backcrossing would increase the total genetic variation, allowing natural selection to act on the hybrid.

     The invasive behavior of Spartina alterniflora demonstrates the influence of introgression on a native species (Anttila et al. 1998). S. alterniflora is a rare invader to the San Francisco Bay salt marshes. The plant produces twenty-one times the amount of viable pollen compared to the native Spartina foliosa. Twenty-eight per cent (1.5 times the rate) of S. alterniflora’s pollen germinates on the native’s stigmas, increasing the seed set of the native plants. The native’s pollen was found not to increase the invader’s seed set. The invaders flower was twice as tall as the native’s, allowing better pollen dispersal by the wind.

     The hybrid of the two species prefers a habitat similar to the invaders, growing in low intertidal zones covering the open mud. Their choice of habitat is vital to that of birds and marine life, which are under threat due to the introgression between the S. alterniflora and S. foliosa. The allelic diversity of S. foliosa is also being compromised. Genetic simulation, genetic dilution, and extinction are long-term threats to the native species.



     Polyploidy 


     Aside from introgression, polyploidy can play a significant role in invasion. New lineages that are isolated from the parental generation can display invasive qualities through an increase in genetic variation (Saad et al. 2011). Polyploidy also confers other fitness advantages in hybrids not seen in the parental generation, such as a faster time to reproduction, increased biomass, photosynthetic activity, and behavioral flexibility (Pandit et al. 2011). Polyploidy is extremely common in plants. Twenty-five per cent of plant species hybridize and within those hybrid events forty-seven per cent of angiosperms are polyploid (Chen 2010).

     There are two types of polyploidy: autopolyploidy and allopolyploidy. Autopolyploidy is the multiplication of the same chromosome set within an organism. There is not an apparent increase in heterosis in autopolyploid hybrids. Allopolyploidy is the product of the addition of two different chromosome sets between two organisms. This usually happens when chromosome doubling or the fusion of unreduced gametes follows hybridization. Hybrid species can be formed instantaneously through this duplication process. It is also possible for polyploid hybrids to arise independently at different locations (Soltis and Soltis 1993). Tragopogon is an allopolyploid formed in Western North America and is taking over local environments. At least thirteen different origins of polyploid formation have been documented in this invasive hybrid.

     What affect does polyploidy have on the likelihood of a plant becoming invasive? Pandit et al. (2011) compiled the largest data set yet to test the association between ploidy and invasiveness. An assessment of chromosome numbers for 81 invasive angiosperms and 2356 of their congeners was completed. They found that invasives are likely to have high chromosome counts and be polyploid. Being invasive is twelve per cent more likely as chromosome number doubles, one per cent more likely as ploidy level doubles, and twenty per cent more likely for polyploids compared with diploid.

     Centaurea maculosa, or spotted knapweed, an invasive to Western North America, demonstrates that polyploidy does play a role in invasiveness (Treier et al. 2009). There were both diploid and tetraploid individuals introduced, but now the population is almost exclusively tetraploid. However, it is unclear if the tetraploids in this case are better adapted or a selective advantage was present.

     Polyploidy can also be one way of overcoming deceased heterozygosity through generations. When mating is limited or disadvantageous, self-fertilization or asexual reproduction may allow a selective advantage. Selfing in hybrids can lead to a ninety-four percent rate of heterozygosity in the next generation due to the rise in tetraploid combinations, while selfing in diploids only leads to a fifty per rate of heterozygosity. An intermittent period of apomixis may confer an advantage when mates are not available. It can also be an alternative reproductive strategy that could fix heterosis due to copying of genetic material (Chen 2010).
         

     In the case of Spartina angelica, which became invasive through a chromosome doubling, heterozygosity was found at many loci, but hardly any variation existed in the population (Thompson 1991). It is unknown exactly how polyploidy increased the fitness of S. angelica; it may have been a result of fixed heterosis, a novel genotype, or both.



Stabilizing the hybrid

     

     Introgression and polyploidy can set the stage for invasiveness by mixing up the genome and creating novel variation. How these mechanisms make an invasive plant so successful can be investigated by looking into the fitness advantages displayed by invasive plant species that allow stabilization and colonization of new habitats.



     Fixed Heterosis



     The increased fitness in hybrids itself can play the lead role in invasiveness.
Heterosis, or hybrid vigor, refers to the increased qualities of hybrid offspring. When heterosis is fixed through mechanisms such as allopolyploidy, this may bring about invasiveness. In plants, this might include a fixed increase in biomass, height, rate of growth, or fertility. Heterosis is widespread in natural systems, but rarely assumed to be fixed in hybrids as it may shift in different stages of growth (Ellstrand and Schierenbeck 2000).

     The outstanding vigor is hidden in parents and only seen in the hybrid progeny because of the events that take place after mating. This concept may be demonstrated by the ability to rapidly colonize areas unavailable to parents (Abbott 2003).
In most cases, early hybrids exceed that of the parents. An example of early success (one of many examples) is found in Artemisia hybrids that show higher seed germination and growth rates (Rieseberg and Carney 1998). Sometimes, early hybrid generations are less fit than the parental generation, but after a few generations the hybrid will outperform one or both parents. Increased fertility and viability are likely to wash away lethal gene combinations during the process.

     Three genetic models may explain the situation of heterosis: dominance, overdominance (ODO), and pseudodominance. In the dominance model, deleterious alleles are complemented by a good allele, increasing the fitness of the hybrid compared to the inbred parents (Chen 2010). In the ODO model, innovative interactions occurring in each of the many loci lead to superior the function of the hybrid over the inbred parent. Typically, the fitness advantage in hybrids is short lived due to recombination leading to hybrid breakdown. However, loci with ODO effects can persist by increasing reproductive fitness and therefore continue their own survival into the following generations (Lippman and Zamir 2007). This is the favored model, because it is the combinations of genes that set the level of heterosis. Together, dominance and ODO QTLs are key contributors to heterosis. The last model of heterosis is the pseudodominance model, an intermediate between the previous two models. It is a simple case of dominance complementation, but also resembles ODO because of linkage. Here, the complementation of dominant and recessive alleles acts in repulsion (Chen 2010) (Lippman and Zamir 2007). Unfortunate to the hybrids, this can breakup in selfers due to recombination.

In sum, hybridizing can increase heterozygosity and cause genome wide changes and interactions between alleles. Some invasive lineages may display fixed heterosis, which may stimulate invasiveness through better adaptations to the environment.



     Increased genetic variation

              

     An increase in genetic variation can also be responsible for the success of an invasive lineage. It is the recombination between genes that leads to the variation and novelty seen in invasives. In general, early successional plants and late successional plants have the same amount of genetic variation. But some hybrids have more genetic variation than their parents as a result of ‘coalescent complexes’ (Ellstrand and Schierenbeck 2000). Schierenbeck and Ellstrand (2007) found that twelve out of the thirty-eight cases of invasive plants formed through hybridization involved stabilization through ‘coalescent complexes’.
          
     Evolutionary Novelty
          
     Evolutionary novelty refers to the formation of exceptional genotypes during hybridization. The creation of unique genotypes is currently the “most common hypothesis for hybridization’s role in adaptive evolution” (Arnold 1997). The main idea of novelty is that recombination in hybrids will lead to a mixture of genotypes, some being less adapted, others being more adapted to certain environments. The better-adapted ones are a result of the recombination process leading to novel genotypes not seen in the parental populations. Invasive plants have been found that exhibit novelty resulting from intermediate traits, a combination of traits, or traits that exceed those of the parents (Ellstrand and Schierenbeck 2000).



     Purging genetic load



     Hybridization can also raise fitness through purging of genetic load, though this is not conclusive (Abbott 2003). Isolated populations may build up many deleterious recessive alleles, that when fixed, may reduce the total fitness of the population. However, if that population hybridizes with another population, recombination between individuals will increase genetic diversity and reduce load. Hybrids have been shown to have higher fecundity and viability compared to the parental generation. The dumping of genetic load in hybrids is a new idea and no apparent studies have been done to experimentally test it, because it would be difficult to compare the load of the hybrid with that of the parent.



Conclusion



     Though many mechanisms have been described that can lead to a plant’s invasiveness, the patterns seen in hybridization as a stimulus for invasion have been explained here. I have shown that plants establish an invasive lineage through the mating of a native plant with a non-native plant or two non-native plants. Mating between populations and the effects of the relative distance between populations was also discussed. Humans have greatly accelerated the rate of hybridization by bringing together isolated related species and by creating new niches for hybrids. Yet, evolution of an invasive hybrid lineage does not occur instantaneously. Multiple introductions and a long lag time are usually associated with the establishment and success of an invasive plant species.

     There are several obstacles a plant must potentially overcome on the path to invasiveness. These include reproductive barriers, harmful alleles or a break-up of successful alleles, and genetic bottlenecks.



     Introgression may allow adaptation and increase fitness during hybridization, while polyploidy will reproductively isolate the species and bring together alleles that have superior function compared to the parental generation. Hybridization can confer fitness advantages in the stable hybrid, including fixed heterosis, increased genetic variation, evolutionary novelty, and a purged genetic load.

     As invasives spread, they can wipe out entire species and/or change the way an ecosystem functions. If we want to manage invasive plants, we must understand why they have become invasive in the first place and the ecological and evolutionary consequences of that status (Lippman and Zamir 2007). Much more is to be known about hybridization as a stimulus for invasion and further studies are needed on the interactions between genetic, environmental, and anthropogenic phenomena responsible for spread of hybrid invasives.