Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions

Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long‐term. We then reviewed the literature on quantitative trait diversity and found that broad‐sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.     

Two colonisation stages generate two different patterns of genetic diversity within native and invasive ranges of Ulex europaeus

Genetic diversity and the way a species is introduced influence the capacity of populations of invasive species to persist in, and adapt to, their new environment. The diversity of introduced populations affects their evolutionary potential, which is particularly important for species that have invaded a wide range of habitats and climates, such as European gorse, Ulex europaeus. This species originated in the Iberian peninsula and colonised Europe in the Neolithic; over the course of the past two centuries it was introduced to, and has become invasive in, other continents. We characterised neutral genetic diversity and its structure in the native range and in invaded regions. By coupling these results with historical data, we have identified the way in which gorse populations were introduced and the consequences of introduction history on genetic diversity. Our study is based on the genotyping of individuals from 18 populations at six microsatellite loci. As U. europaeus is an allohexaploid species, we used recently developed tools that take into account genotypic ambiguity. Our results show that genetic diversity in gorse is very high and mainly contained within populations. We confirm that colonisation occurred in two stages. During the first stage, gorse spread out naturally from Spain towards northern Europe, losing some genetic diversity. During the second stage, gorse was introduced by humans into different regions of the world, from northern Europe. These introductions resulted in the loss of rare alleles but did not significantly reduce genetic diversity and thus the evolutionary potential of this invasive species.     

Potential limits to the benefits of admixture during biological invasion

Species introductions often bring together genetically divergent source populations, resulting in genetic admixture. This geographic reshuffling of diversity has the potential to generate favourable new genetic combinations, facilitating the establishment and invasive spread of introduced populations. Observational support for the superior performance of admixed introductions has been mixed, however, and the broad importance of admixture to invasion questioned. Under most underlying mechanisms, admixture's benefits should be expected to increase with greater divergence among and lower genetic diversity within source populations, though these effects have not been quantified in invaders. We experimentally crossed source populations differing in divergence in the invasive plant Centaurea solstitialis. Crosses resulted in many positive (heterotic) interactions, but fitness benefits declined and were ultimately negative at high source divergence, with patterns suggesting cytonuclear epistasis. We explored the literature to assess whether such negative epistatic interactions might be impeding admixture at high source population divergence. Admixed introductions reported for plants came from sources with a wide range of genetic variation, but were disproportionately absent where there was high genetic divergence among native populations. We conclude that while admixture is common in species introductions and often happens under conditions expected to be beneficial to invaders, these conditions may be constrained by predictable negative genetic interactions, potentially explaining conflicting evidence for admixture's benefits to invasion.     

Patterns of genetic diversity reveal multiple introductions and recurrent founder effects during range expansion in invasive populations of Geranium carolinianum (Geraniaceae)

Genetic diversity, and thus the adaptive potential of invasive populations, is largely based on three factors: patterns of genetic diversity in the species'' native range, the number and location of introductions and the number of founding individuals per introduction. Specifically, reductions in genetic diversity (‘founder effects'') should be stronger for species with low within-population diversity in their native range and few introductions of few individuals to the invasive range. We test these predictions with Geranium carolinianum, a winter annual herb native to North America and invasive in China. We measure the extent of founder effects using allozymes and microsatellites, and ask whether this is consistent with its colonization history and patterns of diversity in the native range. In the native range, genetic diversity is higher and structure is lower than expected based on life history traits. In China, our results provide evidence for multiple introductions near Nanjing, Jiangsu province, with subsequent range expansion to the west and south. Patterns of genetic diversity across China reveal weak founder effects that are driven largely by low-diversity populations at the expansion front, away from the introduction location. This suggests that reduced diversity in China has resulted from successive founder events during range expansion, and that the loss of genetic diversity in the Nanjing area was mitigated by multiple introductions from diverse source populations. This has implications for the future of G. carolinianum in China, as continued gene flow among populations should eventually increase genetic diversity within the more recently founded populations.     

Invasion success and genetic diversity of introduced populations of guppies Poecilia reticulata in Australia

High genetic diversity is thought to characterize successful invasive species, as the potential to adapt to new environments is enhanced and inbreeding is reduced. In the last century, guppies, Poecilia reticulata, repeatedly invaded streams in Australia and elsewhere. Quantitative genetic studies of one Australian guppy population have demonstrated high additive genetic variation for autosomal and Y-linked morphological traits. The combination of colonization success, high heritability of morphological traits, and the possibility of multiple introductions to Australia raised the prediction that neutral genetic diversity is high in introduced populations of guppies. In this study we examine genetic diversity at nine microsatellite and one mitochondrial locus for seven Australian populations. We used mtDNA haplotypes from the natural range of guppies and from domesticated varieties to identify source populations. There were a minimum of two introductions, but there was no haplotype diversity within Australian populations, suggesting a founder effect. This was supported by microsatellite markers, as allelic diversity and heterozygosity were severely reduced compared to one wild source population, and evidence of recent bottlenecks was found. Between Australian populations little differentiation of microsatellite allele frequencies was detected, suggesting that population admixture has occurred historically, perhaps due to male-biased gene flow followed by bottlenecks. Thus success of invasion of Australia and high additive genetic variance in Australian guppies are not associated with high levels of diversity at molecular loci. This finding is consistent with the release of additive genetic variation by dominance and epistasis following inbreeding, and with disruptive and negative frequency-dependent selection on fitness traits.     

Population genetics of introduced bullfrogs, Rana (Lithobates) catesbeianus, in the Willamette Valley, Oregon, USA

The American bullfrog, Rana (Lithobates) catesbeianus, is endemic to eastern North America, but has been introduced to approximately 40 countries on four continents and is considered one of the hundred worst invasive alien species in the world. Here, we investigated the genetics of invasive bullfrogs in the Willamette Valley, Oregon, USA, where bullfrogs are widespread and abundant to determine: (1) the minimum number of bullfrog introductions; (2) the native source population(s); and (3) whether genetic variation is reduced compared to source populations. To answer these questions, we analyzed partial sequences of the mitochondrial cytochrome b gene for 251 bullfrogs from the Willamette Valley and the native range. We found that bullfrogs from the Mississippi River basin and Great Lakes region were introduced at least once to the Willamette Valley. Genetic variation measured as haplotype diversity (h) and nucleotide diversity (?? _n ) was not significantly different between Willamette Valley and source populations. Our results were in contrast to a recent genetic analysis of invasive bullfrog populations in Europe, which found that genetic variation in European bullfrog populations was much lower than in source populations. European bullfrogs also originated from different source populations than Willamette Valley bullfrogs. The difference in genetic composition between Willamette Valley and European bullfrogs is likely due to differences in their invasion histories and may have implications for the potential of bullfrogs in these different regions to adapt and expand.     

Genetic structure of invasive earthworms Dendrobaena octaedra in the boreal forest of Alberta: insights into introduction mechanisms

Population genetic studies can help to determine whether invasive species are established via single vs. multiple introduction events and also to distinguish among various colonization scenarios. We used this approach to investigate the introduction of Dendrobaena octaedra , a non-native earthworm species, to the boreal forest of northern Alberta. The spread of non-native earthworms in forested systems is not well understood, although bait abandonment and vehicular transport are believed to be important. Mitochondrial DNA sequencing revealed that multiple introductions of this species have occurred in northern Alberta, although individual populations may have been established by either single or multiple invaders introduced on one or more occasions. There was no relationship between genetic distances and either geographical distances or distances along road networks, suggesting that human-mediated jump dispersal is more common than diffusive spread via road networks or via active dispersal. As well, genetic diversity was significantly greater at boat launches than roads, indicating that multiple introductions may be more likely to occur at those locations. Focusing management efforts on areas where multiple introductions are likely to occur may help to reduce invasive species' potential for adaptive evolution and subsequent rapid spread.     

High genetic variance in life-history strategies within invasive populations by way of multiple introductions

Biological invasions represent major threats to biodiversity as well as large-scale evolutionary experiments. Invasive populations have provided some of the best known examples of contemporary evolution [3-6], challenging the classical view that invasive species are genetically depauperate because of founder effects. Yet the origin of trait genetic variance in invasive populations largely remains a mystery, precluding a clear understanding of how evolution proceeds. In particular, despite the emerging molecular evidence that multiple introductions commonly occur in the same place, their contribution to the evolutionary potential of invasives remains unclear. Here, by using a long-term field survey, mtDNA sequences, and a large-scale quantitative genetic experiment on freshwater snails, we document how a spectacular adaptive potential for key ecological traits can be accumulated in invasive populations. We provide the first direct evidence that multiple introductions are primarily responsible for such an accumulation and that sexual reproduction amplifies this effect by generating novel trait combinations. Thus bioinvasions, destructive as they may be, are not synonyms of genetic uniformity and can be hotspots of evolutionary novelty.     

Founder events predict changes in genetic diversity during human‐mediated range expansions

Intentional or accidental introduction of species to new locations is predicted to result in loss of genetic variation and increase the likelihood of inbreeding, thus reducing population viability and evolutionary potential. However, multiple introductions and large founder numbers can prevent loss of genetic diversity and may therefore facilitate establishment success and range expansion. Based on a meta‐analysis of 119 introductions of 85 species of plants and animals, we here show a quantitative effect of founding history on genetic diversity in introduced populations. Both introduction of large number of individuals and multiple introduction events significantly contribute to maintaining or even increasing genetic diversity in introduced populations. The most consistent loss of genetic diversity is seen in insects and mammals, whereas introduced plant populations tend to have higher genetic variation than native populations. However, loss or gain of genetic diversity does not explain variation in the extent to which plant or animal populations become invasive outside of their native range. These results provide strong support for predictions from population genetics theory with respect to patterns of genetic diversity in introduced populations, but suggest that invasiveness is not limited by genetic bottlenecks.     

High genetic diversity is not essential for successful introduction

Some introduced populations thrive and evolve despite the presumed loss of diversity at introduction. We aimed to quantify the amount of genetic diversity retained at introduction in species that have shown evidence of adaptation to their introduced environments. Samples were taken from native and introduced ranges of Arctotheca populifolia and Petrorhagia nanteuilii. Using microsatellite data, we identified the source for each introduction, estimated genetic diversity in native and introduced populations, and calculated the amount of diversity retained in introduced populations. These values were compared to those from a literature review of diversity in native, confamilial populations and to estimates of genetic diversity retained at introduction. Gene diversity in the native range of both species was significantly lower than for confamilials. We found that, on average, introduced populations showing evidence of adaptation to their new environments retained 81% of the genetic diversity from the native range. Introduced populations of P. nanteuilii had higher genetic diversity than found in the native source populations, whereas introduced populations of A. populifolia retained only 14% of its native diversity in one introduction and 1% in another. Our literature review has shown that most introductions demonstrating adaptive ability have lost diversity upon introduction. The two species studied here had exceptionally low native range genetic diversity. Further, the two introductions of A. populifolia represent the largest percentage loss of genetic diversity in a species showing evidence of substantial morphological change in the introduced range. While high genetic diversity may increase the likelihood of invasion success, the species examined here adapted to their new environments with very little neutral genetic diversity. This finding suggests that even introductions founded by small numbers of individuals have the potential to become invasive.     

Post-colonization temporal genetic variation of an introduced fly, Rhagoletis completa

Evolutionary biologists have been puzzled by the success of introduced species: despite founder effects that reduce genetic variability, invasive species are still successful at colonizing new environments. It is possible that the evolutionary processes during the post-colonization period may increase the genetic diversity and gene flow among invasive populations over time, facilitating their long-term success. Therefore, genetic diversity and population structure would be expected to show greater temporal variation for successful introduced populations than for native populations. We studied the population genetics of the walnut husk fly, Rhagoletis completa, which was introduced into California from the Midwestern US in the early 1900s. We used microsatellites and allozymes to genotype current and historic fly populations, providing a rare perspective on temporal variability in population genetic parameters. We found that introduced populations showed greater temporal fluctuations in allele frequencies than native populations. Some introduced populations also showed an increase in genetic diversity over time, indicating multiple introductions had occurred. Population genetic structure decreased in both native and introduced populations over time. Our study demonstrates that introduced species are not at equilibrium and post-colonization processes may be important in ameliorating the loss of genetic diversity associated with biological invasions.     

Low genetic and morphological differentiation between an introduced population of dunnocks in New Zealand and an ancestral population in England

Species invasions and exotic species introductions can be considered as ??unplanned experiments??, which help us to understand the evolution of organisms. In this study, we investigated whether an exotic bird species, the dunnock (Prunella modularis), has diverged genetically and morphologically from its native source population (Cambridge, England) after introduction into a new environment (Dunedin, South Island of New Zealand; exotic population). We used a set of microsatellite markers and three morphological traits to quantify the divergence between these two populations. We quantified neutral genotypic differentiation between the populations, and also used an individual-based Bayesian clustering method to assess genetic structure. We compared morphological divergence using univariate and principal components analyses. We found that individuals from the Dunedin population are genetically distinct from the Cambridge population, but levels of differentiation are very low. Overall within-population levels of genetic diversity are low compared to other bird species, and effective population sizes are small; indicating that the native population probably has a historically low level of genetic diversity, and that the introduced population retained most of that diversity after its introduction into New Zealand. We found little evidence of morphological divergence, and the evolutionary rate of change in these traits is below the average for other taxa. Our study adds support to the growing literature showing that invasive species maintain most of their initial genetic diversity after multiple founder events, even when population size is severely reduced. Moreover, our morphological data indicate slow evolutionary rates in species introduced to similar habitats.     

Complex patterns of global spread in invasive insects: eco-evolutionary and management consequences

The advent of simple and affordable tools for molecular identification of novel insect invaders and assessment of population diversity has changed the face of invasion biology in recent years. The widespread application of these tools has brought with it an emerging understanding that patterns in biogeography, introduction history and subsequent movement and spread of many invasive alien insects are far more complex than previously thought. We reviewed the literature and found that for a number of invasive insects, there is strong and growing evidence that multiple introductions, complex global movement, and population admixture in the invaded range are commonplace. Additionally, historical paradigms related to species and strain identities and origins of common invaders are in many cases being challenged. This has major consequences for our understanding of basic biology and ecology of invasive insects and impacts quarantine, management and biocontrol programs. In addition, we found that founder effects rarely limit fitness in invasive insects and may benefit populations (by purging harmful alleles or increasing additive genetic variance). Also, while phenotypic plasticity appears important post-establishment, genetic diversity in invasive insects is often higher than expected and increases over time via multiple introductions. Further, connectivity among disjunct regions of global invasive ranges is generally far higher than expected and is often asymmetric, with some populations contributing disproportionately to global spread. We argue that the role of connectivity in driving the ecology and evolution of introduced species with multiple invasive ranges has been historically underestimated and that such species are often best understood in a global context.     

BIODIVERSITY RESEARCH: Genetic diversity in two introduced biofouling amphipods (Ampithoe valida & Jassa marmorata) along the Pacific North American coast: investigation into molecular identification and cryptic diversity

Aim We investigated patterns of genetic diversity among invasive populations of Ampithoe valida and Jassa marmorata from the Pacific North American coast to assess the accuracy of morphological identification and determine whether or not cryptic diversity and multiple introductions contribute to the contemporary distribution of these species in the region. Location Native range: Atlantic North American coast; Invaded range: Pacific North American coast. Methods We assessed indices of genetic diversity based on DNA sequence data from the mitochondrial cytochrome c oxidase subunit I (COI) gene, determined the distribution of COI haplotypes among populations in both the invasive and putative native ranges of A. valida and J. marmorata and reconstructed phylogenetic relationships among COI haplotypes using both maximum parsimony and Bayesian approaches. Results Phylogenetic inference indicates that inaccurate species‐level identifications by morphological criteria are common among Jassa specimens. In addition, our data reveal the presence of three well supported but previously unrecognized clades of A. valida among specimens in the north‐eastern Pacific. Different species of Jassa and different genetic lineages of Ampithoe exhibit striking disparity in geographic distribution across the region as well as substantial differences in genetic diversity indices. Main conclusions Molecular genetic methods greatly improve the accuracy and resolution of identifications for invasive benthic marine amphipods at the species level and below. Our data suggest that multiple cryptic introductions of Ampithoe have occurred in the north‐eastern Pacific and highlight uncertainty regarding the origin and invasion histories of both Jassa and Ampithoe species. Additional morphological and genetic analyses are necessary to clarify the taxonomy and native biogeography of both amphipod genera.     

Unravelling the invasion history of the Asian tiger mosquito in Europe

Multiple introductions are key features for the establishment and persistence of introduced species. However, little is known about the contribution of genetic admixture to the invasive potential of populations. To address this issue, we studied the recent invasion of the Asian tiger mosquito (Aedes albopictus) in Europe. Combining genome‐wide single nucleotide polymorphisms and historical knowledge using an approximate Bayesian computation framework, we reconstruct the colonization routes and establish the demographic dynamics of invasion. The colonization of Europe involved at least three independent introductions in Albania, North Italy and Central Italy that subsequently acted as dispersal centres throughout Europe. We show that the topology of human transportation networks shaped demographic histories with North Italy and Central Italy being the main dispersal centres in Europe. Introduction modalities conditioned the levels of genetic diversity in invading populations, and genetically diverse and admixed populations promoted more secondary introductions and have spread farther than single‐source invasions. This genomic study provides further crucial insights into a general understanding of the role of genetic diversity promoted by modern trade in driving biological invasions.     

遗传多样性与外来物种的成功入侵: 现状和展望

遗传多样性被认为是影响外来种入侵成功的重要因素之一。研究表明, 尽管外来种在入侵过程中可能受到奠基者效应的影响, 但是多次引种、种内或种间杂交等过程使得许多外来种在引入地的遗传多样性水平未必会显著低于原产地, 从而使得外来种可能通过快速进化来适应引入地的新生境。然而, 高水平的遗传多样性并非成功入侵的必要条件, 遗传变异的匮乏对一些外来种的入侵能力没有明显的影响, 甚至在一些生物入侵案例中, 遗传多样性的降低反而促进了入侵成功。针对遗传多样性与入侵成功之间的复杂关系, 本文在评述外来种遗传多样性的研究现状的基础上, 分析了遗传多样性对外来种的短期入侵成功和长期进化的影响机制, 从方法角度探讨了目前研究中存在的若干问题, 并对如何推进入侵生态学研究提出了一些看法。正如一些学者提出的, 入侵生态学需要与生态学其他分支整合起来, 才能加深对生物入侵及其相关的生态和进化过程的理解。     

No evolutionary shift in the mating system of north American Ambrosia artemisiifolia (Asteraceae) following its introduction to China

The mating system plays a key role during the process of plant invasion. Contemporary evolution of uniparental reproduction (selfing or asexuality) can relieve the challenges of mate limitation in colonizing populations by providing reproductive assurance. Here we examined aspects of the genetics of colonization in Ambrosia artemisiifolia, a North American native that is invasive in China. This species has been found to possess a strong self-incompatibility system and have high outcrossing rates in North America and we examined whether there has been an evolutionary shift towards the dependence on selfing in the introduced range. Specifically, we estimated outcrossing rates in one native and five invasive populations and compared levels of genetic diversity between North America and China. Based on six microsatellite loci we found that, like the native North American population, all five Chinese populations possessed a completely outcrossing mating system. The estimates of paternity correlations were low, ranging from 0.028-0.122, which suggests that populations possessed ~8-36 pollen donor parents contributing to each maternal plant in the invasive populations. High levels of genetic diversity for both native and invasive populations were found with the unbiased estimate of gene diversity ranging from 0.262-0.289 for both geographic ranges based on AFLP markers. Our results demonstrate that there has been no evolutionary shift from outcrossing to selfing during A. artemisiifolia's invasion of China. Furthermore, high levels of genetic variation in North America and China indicate that there has been no erosion of genetic variance due to a bottleneck during the introduction process. We suggest that the successful invasion of A. artemisiifolia into Asia was facilitated by repeated introductions from multiple source populations in the native range creating a diverse gene pool within Chinese populations.     

Highly diverse and highly successful: invasive Australian acacias have not experienced genetic bottlenecks globally

Background and AimsInvasive species may undergo rapid evolution despite very limited standing genetic diversity. This so-called genetic paradox of biological invasions assumes that an invasive species has experienced (and survived) a genetic bottleneck and then underwent local adaptation in the new range. In this study, we test how often Australian acacias (genus Acacia), one of the world’s most problematic invasive tree groups, have experienced genetic bottlenecks and inbreeding.MethodsWe collated genetic data from 51 different genetic studies on Acacia species to compare genetic diversity between native and invasive populations. These studies analysed 37 different Acacia species, with genetic data from the invasive ranges of 11 species, and data from the native range for 36 species (14 of these 36 species are known to be invasive somewhere in the world, and the other 22 are not known to be invasive).Key ResultsLevels of genetic diversity are similar in native and invasive populations, and there is little evidence of invasive populations being extensively inbred. Levels of genetic diversity in native range populations also did not differ significantly between species that have and that do not have invasive populations.ConclusionWe attribute our findings to the impressive movement, introduction effort and human usage of Australian acacias around the world.     

Evidence for multiple introductions of Centaurea stoebe micranthos (spotted knapweed,Asteraceae) to North America

Invasive species’ success may depend strongly on the genetic resources they maintain through the invasion process. We ask how many introductions have occurred in the North American weed Centaurea stoebe micranthos (Asteraceae), and explore whether genetic diversity and population structure have changed as a result of introduction. We surveyed individuals from 15 European native range sites and 11 North American introduced range sites at six polymorphic microsatellite loci. No significant difference existed in the total number of alleles or in the number of private alleles found in each range. Shannon–Weaver diversity of phenotype frequencies was also not significantly different between the ranges, while expected heterozygosity was significantly higher in the invasive range. Population structure was similar between the native range and the invasive range, and isolation by distance was not significant in either range. Traditional assignment methods did not allocate any North American individuals to the sampled European populations, while Bayesian assignment methods grouped individuals into nine genetic clusters, with three of them shared between North America and Europe. Invasive individuals tended to have genetically admixed profiles, while natives tended to assign more strongly to a single cluster. Many North American individuals share assignment with Romania and Bulgaria, suggesting two separate invasions that have undergone gene flow in North America. Samples from three other invasive range sites were genetically distinct, possibly representing three other unique introductions. Multiple introductions and the maintenance of high genetic diversity through the introduction process may be partially responsible for the invasive success of C. stoebe micranthos.