Review
Adaptive evolution in invasive species

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

Introduction

Biological invasions are defined as the introduction, establishment, and spread of species outside their native range ([1]; Figure 1]), and they are recognized as a major threat to the economy and environment worldwide [2]. By definition, introduced species are present in biogeographic regions where they did not evolve and to which they might be poorly adapted 1, 3, encountering a suite of novel stresses and selection pressures [4]. Consequently, introduced populations have considerable potential for rapid adaptation, and it has been proposed that this adaptation can explain why some introduced species establish, proliferate, and become invasive in new environments 1, 2, 3, 4, 5, 6, 7.

Evolutionary change was first recognized as an important process in biological invasions more than 30 years ago [8]. Nevertheless, most research in this area has been conducted in the past decade, and has concentrated on comparing genetic diversity between source and invasive populations [5]. Fewer studies have examined the role of rapid adaptive evolution in biological invasion 7, 9, and no study that we know of has attempted to identify the source of genetic and epigenetic variation underlying rapid adaptation in invasive species. The literature on non-invasive model or agronomic plant species, however, details a range of mechanisms that can influence rapid evolutionary change within 20 generations or fewer 10, 11, 12, 13. This includes a case in which heritable genomic change in Arabidopsis thaliana (thale cress) was caused by novel environmental stress [11], a mechanism not yet examined in the rapid evolution of invasive species. Given the potential that these mechanisms have for explaining invasiveness, the study of adaptive evolution in invasive species will fast become a very productive area of research.

In this review, we explore the role of rapid evolutionary change as a means of adaptation during plant invasions, and identify key research gaps. Our primary focus is to elucidate how different forms of genetic variation affect the likelihood of adaptive evolution during the introduction, establishment, and spread of invasive species (Figure 1). We examine the potential for adaptive evolution in invasive species provided by standing genetic variation compared to that from new mutations, and look at four types of evolutionary change that might promote rapid evolution in the introduced range: bottlenecks, hybridization, polyploidy, and stress-induced modification of the genome. Although adaptation from standing genetic variation and the four types of evolutionary change are not exclusive to plant invasions, the nature of many biological invasions predisposes invasive plants to these mechanisms 1, 3, 4. Moreover, recent biological invasions such as that of Hypericum canariense (Canary Island St. John's wort [14]), provide an ideal opportunity to investigate rapid adaptation [15]. We advocate the use of a combined quantitative trait locus (QTL) mapping and genome scan approach [16] to discover the underlying genetic changes associated with successful invasions and potentially to identify candidate genes that are involved in invasiveness.

Section snippets

Standing genetic variation compared with new mutation

Whether the genetic changes that allow species adapt to new environments arise from new mutation or standing genetic variation is currently a key question in evolutionary biology [17], and this question is equally important for understanding the rapid evolution of invasiveness. We predict that, during the invasion process, rapid adaptation, occurring over tens of generations or fewer [13], should mostly be due to alleles from standing genetic variation because favourable alleles are immediately

Bottlenecks

Genetic bottlenecks are commonly predicted to be associated with biological invasions [24], as introduced populations can be founded by a small number of individuals that are isolated from further gene flow [14]. Whether genetic bottlenecks constrain the speed of rapid adaptation is a question of great interest to invasion biologists 5, 13, 14. Traditionally, genetic bottlenecks were thought to decrease the potential for adaptive evolution [25] because of a reduction in the quantitative

Hybridization

Hybridization, both intra- and interspecific, has been suggested to stimulate invasiveness in plants [29]. Mounting evidence is becoming available to support this claim because many invading species, including Ambrosia artemisiifolia (Common ragweed) and Cytisus scoparius (Scotch broom), have multiple introductions. Other invading taxa, such as Helianthus annuus ssp. texanus (Weedy sunflower) are the by-products of inter-specific hybridization 5, 9, 14, 30, 31, 32, 33. In some cases, however,

Polyploidy

Polyploidy or genome doubling has been a pervasive force in plant evolution [43]. Interestingly, polyploids occur with greater frequency among invasive plants than among angiosperms in general 44, 45. In many cases where species consist of two or more ploidy levels in the native range, invasive populations often only contain individuals of the higher ploidy level, for example Fallopia japonica (Japanese knotweed) in Europe [46]. Alternatively, invasive populations can be neo-allopolyploids,

Stress-induced modification of the genome

Invasive species frequently encounter novel ecological contexts [4], both biotic (e.g. pathogens) and abiotic (i.e. UV exposure). Exposure to novel biotic or abiotic conditions can induce stress in some plants, and has been shown to affect genome stability in some cases 54, 55. This process is, on initial inspection, akin to the ideas of Lamarck, but a recent review distinguishes this area as stress-induced modification of the genome [12]. Stress-induced genome modification can be epigenetic

A genomic approach to studying adaptive evolution in invasive species

Understanding the genetic basis of traits that are involved in rapid adaptation to novel environmental conditions is a major goal in invasion biology. In particular, identifying the genes or genetic changes that underlie these traits will permit us to answer fundamental questions: how often does rapid adaptation result from standing genetic variation rather than new mutation in successful plant invasions? And are similar genes the targets of selection when the same species undergoes multiple

Acknowledgements

We thank three anonymous reviewers for insightful comments that greatly improved this manuscript and Ana Pavasovic for help with Figure 2. This work was supported in part by the ARC Discovery Grant (DP0664967) awarded to A.J.L. by the DST-NRF Centre of Excellence for Invasion Biology and the Working for Water Programme.

Glossary

Additive genetic variance
variance associated with the average outcome of substituting one allele with another.
Epigenetic
a factor that changes the phenotype of an organism that is not associated with a change in its DNA sequence.
Epistasis
the phenotypic consequence of interaction among alleles at multiple loci.
Founder effect
the difference in gene pools between an original population and a new population after colonization.
Genetic bottleneck
when population numbers are reduced to a level

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