Bridgehead Effect in the Worldwide Invasion of the Biocontrol Harlequin Ladybird

Recent studies of the routes of worldwide introductions of alien organisms suggest that many widespread invasions could have stemmed not from the native range, but from a particularly successful invasive population, which serves as the source of colonists for remote new territories. We call here this phenomenon the invasive bridgehead effect. Evaluating the likelihood of such a scenario is heuristically challenging. We solved this problem by using approximate Bayesian computation methods to quantitatively compare complex invasion scenarios based on the analysis of population genetics (microsatellite variation) and historical (first observation dates) data. We applied this approach to the Harlequin ladybird Harmonia axyridis (HA), a coccinellid native to Asia that was repeatedly introduced as a biocontrol agent without becoming established for decades. We show that the recent burst of worldwide invasions of HA followed a bridgehead scenario, in which an invasive population in eastern North America acted as the source of the colonists that invaded the European, South American and African continents, with some admixture with a biocontrol strain in Europe. This demonstration of a mechanism of invasion via a bridgehead has important implications both for invasion theory (i.e., a single evolutionary shift in the bridgehead population versus multiple changes in case of introduced populations becoming invasive independently) and for ongoing efforts to manage invasions by alien organisms (i.e., heightened vigilance against invasive bridgeheads).     

Deciphering the worldwide invasion of the Asian long‐horned beetle: A recurrent invasion process from the native area together with a bridgehead effect

Retracing introduction routes is crucial for understanding the evolutionary processes involved in an invasion, as well as for highlighting the invasion history of a species at the global scale. The Asian long‐horned beetle (ALB) Anoplophora glabripennis is a xylophagous pest native to Asia and invasive in North America and Europe. It is responsible for severe losses of urban trees, in both its native and invaded ranges. Based on historical and genetic data, several hypotheses have been formulated concerning its invasion history, including the possibility of multiple introductions from the native zone and secondary dispersal within the invaded areas, but none have been formally tested. In this study, we characterized the genetic structure of ALB in both its native and invaded ranges using microsatellites. In order to test different invasion scenarios, we used an approximate Bayesian “random forest” algorithm together with traditional population genetics approaches. The strong population differentiation observed in the native area was not geographically structured, suggesting complex migration events that were probably human‐mediated. Both native and invasive populations had low genetic diversity, but this characteristic did not prevent the success of the ALB invasions. Our results highlight the complexity of invasion pathways for insect pests. Specifically, our findings indicate that invasive species might be repeatedly introduced from their native range, and they emphasize the importance of multiple, human‐mediated introductions in successful invasions. Finally, our results demonstrate that invasive species can spread across continents following a bridgehead path, in which an invasive population may have acted as a source for another invasion.     

Genomic admixture increases fitness during a biological invasion

Abstract During biological invasions, multiple introductions can provide opportunities for admixture among genetically distinct lineages. Admixture is predicted to contribute to invasion success by directly increasing fitness through hybrid vigour or by enhancing evolutionary potential within populations . Here, we demonstrate genome‐wide admixture during an invasion that substantially boosted fitness in the cosmopolitan weed, Silene vulgaris. We identified three divergent demes in the native European range that expanded from glacial refugia and experienced historical admixture in a well‐known suture zone. During recent invasion of North America, multiple introductions created additional opportunities for admixture. In common garden experiments, recombinant genotypes from North America experienced a two‐fold increase in fitness relative to nonrecombinants, whereas recombinant genotypes from Europe showed no lasting fitness benefits. This contrast implicates hybrid vigour behind the boost in fitness and supports the hypothesis that admixture can lead to fitness increases that may catapult invasion into a new range.     

Bayesian inference of a complex invasion history revealed by nuclear and chloroplast genetic diversity in the colonizing plant,Silene latifolia

Species invading new ranges are subject to a series of demographic events that can strongly shape genetic diversity. Describing this demographic history is important for understanding where invasive species come from and how they spread, and is critical to testing hypotheses of postinvasion adaptation. Here, we analyse nuclear and chloroplast genetic diversity to study the invasion history of the widespread colonizing weed, Silene latifolia (Caryophyllaceae). Bayesian clustering and PCA revealed strong population structure in the native range of Europe, and although genotypes from multiple native sources were present in the introduced range of North America, the spatial distribution of genetic variance was dramatically reorganized. Using approximate Bayesian computation (ABC), we compared support for different invasion scenarios, including the number and size of independent introduction events and the amount of admixture occurring between sources of introduced genotypes. Our results supported independent introductions into eastern and western North America, with the latter forming a bridgehead for a secondary invasion into the Great Lakes region of central North America. Despite small estimated founder population sizes, the duration of the demographic bottleneck after the initial introduction appeared extremely short‐lived. This pattern of repeated colonization and rapid expansion has effectively eroded the strong population structure and cytonuclear associations present in Europe, but has retained overall high genetic diversity since invasion. Our results highlight the flexibility of the ABC approach for constructing a narrative of the demographic history of species invasions and provide baseline for future studies of evolutionary changes in introduced S. latifolia populations.     

Effects of admixture in native and invasive populations of <Emphasis Type="Italic">Lythrum salicaria</Emphasis>

Intraspecific hybridization between diverged populations can enhance fitness via various genetic mechanisms. The benefits of such admixture have been proposed to be particularly relevant in biological invasions, when invasive populations originating from different source populations are found sympatrically. However, it remains poorly understood if admixture is an important contributor to plant invasive success and how admixture effects compare between invasive and native ranges. Here, we used experimental crosses in Lythrum salicaria, a species with well-established history of multiple introductions to Eastern North America, to quantify and compare admixture effects in native European and invasive North American populations. We observed heterosis in between-population crosses both in native and invasive ranges. However, invasive-range heterosis was restricted to crosses between two different Eastern and Western invasion fronts, whereas heterosis was absent in geographically distant crosses within a single large invasion front. Our results suggest that multiple introductions have led to already-admixed invasion fronts, such that experimental crosses do not further increase performance, but that contact between different invasion fronts further enhances fitness after admixture. Thus, intra-continental movement of invasive plants in their introduced range has the potential to boost invasiveness even in well-established and successfully spreading invasive species.     

Population genomic analyses reveal a history of range expansion and trait evolution across the native and invaded range of yellow starthistle (Centaurea solstitialis)

Identifying sources of genetic variation and reconstructing invasion routes for non‐native introduced species is central to understanding the circumstances under which they may evolve increased invasiveness. In this study, we used genome‐wide single nucleotide polymorphisms to study the colonization history of Centaurea solstitialis in its native range in Eurasia and invasions into the Americas. We leveraged this information to pinpoint key evolutionary shifts in plant size, a focal trait associated with invasiveness in this species. Our analyses revealed clear population genomic structure of potential source populations in Eurasia, including deep differentiation of a lineage found in the southern Apennine and Balkan Peninsulas and divergence among populations in Asia, eastern Europe and western Europe. We found strongest support for an evolutionary scenario in which western European populations were derived from an ancient admixture event between populations from eastern Europe and Asia, and subsequently served as the main genetic ‘bridgehead’ for introductions to the Americas. Introductions to California appear to be from a single source region, and multiple, independent introductions of divergent genotypes likely occurred into the Pacific Northwest. Plant size has evolved significantly at three points during range expansion, including a large size increase in the lineage responsible for the aggressive invasion of the California interior. These results reveal a long history of colonization, admixture and trait evolution in C. solstitialis, and suggest routes for improving evidence‐based management decisions for one of the most ecologically and economically damaging invasive species in the western United States.     

The lack of genetic bottleneck in invasive Tansy ragwort populations suggests multiple source populations.

Jacobaea vulgaris (Asteraceae) is a species of Eurasian origin that has become a serious non-indigenous weed in Australia, New Zealand, and North America. We used neutral molecular markers to (1) test for genetic bottlenecks in invasive populations and (2) to investigate the invasion pathways. It is for the first time that molecular markers were used to unravel the process of introduction in this species.The genetic variation of 15 native populations from Europe and 16 invasive populations from Australia, New Zealand and North America were compared using the amplified fragment length polymorphisms (AFLP's). An analysis of molecular variance showed that a significant part (10%) of the total genetic variations between all individuals could be explained by native or invasive origin.Significant among-population differentiation was detected only in the native range, whereas populations from the invasive areas did not significantly differ from each other; nor did the Australian, New Zealand and North American regions differ within the invasive range. The result that native populations differed significantly from each other and that the amount of genetic variation, measured as the number of polymorphic bands, did not differ between the native and invasive area, strongly suggests that introductions from multiple source populations have occurred. The lack of differentiation between invasive regions suggests that either introductions may have occurred from the same native sources in all invasive regions or subsequent introductions took place from one into another invasive region and the same mix of genotypes was subsequently introduced into all invasive regions.An assignment test showed that European populations from Ireland, the Netherlands and the United Kingdom most resembled the invasive populations.     

Recent admixture generates heterozygosity–fitness correlations during the range expansion of an invading species

Admixture, the mixing of historically isolated gene pools, can have immediate consequences for the genetic architecture of fitness traits. Admixture may be especially important for newly colonized populations, such as during range expansion and species invasions, by generating heterozygosity that can boost fitness through heterosis. Despite widespread evidence for admixture during species invasions, few studies have examined the demographic history leading to admixture, how admixture affects the heterozygosity and fitness of invasive genotypes, and whether such fitness effects are maintained through time. We address these questions using the invasive plant Silene vulgaris, which shows evidence of admixture in both its native Europe and in North America where it has invaded. Using multilocus genotype data in conjunction with approximate Bayesian computation analysis of demographic history, we showed that admixture during the invasion of North America was independent from and much younger than admixture in the native range of Europe. We tested for fitness consequences of admixture in each range and detected a significant positive heterozygosity–fitness correlation (HFC) in North America; in contrast, no HFC was present in Europe. The lack of HFC in Europe may reflect the longer time since admixture in the native range, dissipating associations between heterozygosity at markers and fitness loci. Our results support a key short‐term role for admixture during the early stages of invasion by generating HFCs that carry populations past the threat of extinction from inbreeding and demographic stochasticity.     

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.     

Secondary Contact and Admixture between Independently Invading Populations of the Western Corn Rootworm,Diabrotica virgifera virgifera in Europe

The western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae), is one of the most destructive pests of corn in North America and is currently invading Europe. The two major invasive outbreaks of rootworm in Europe have occurred, in North-West Italy and in Central and South-Eastern Europe. These two outbreaks originated from independent introductions from North America. Secondary contact probably occurred in North Italy between these two outbreaks, in 2008. We used 13 microsatellite markers to conduct a population genetics study, to demonstrate that this geographic contact resulted in a zone of admixture in the Italian region of Veneto. We show that i) genetic variation is greater in the contact zone than in the parental outbreaks; ii) several signs of admixture were detected in some Venetian samples, in a Bayesian analysis of the population structure and in an approximate Bayesian computation analysis of historical scenarios and, finally, iii) allelic frequency clines were observed at microsatellite loci. The contact between the invasive outbreaks in North-West Italy and Central and South-Eastern Europe resulted in a zone of admixture, with particular characteristics. The evolutionary implications of the existence of a zone of admixture in Northern Italy and their possible impact on the invasion success of the western corn rootworm are discussed.     

Invasion history of North American Canada thistle,Cirsium arvense

Aim Canada thistle (Cirsium arvense– Cardueae, Asteraceae) is one of the worst invasive plants world‐wide. Native to Eurasia, its unintentional introduction into North America now threatens the native flora and is responsible for enormous agricultural losses. The goals of this study are to: (1) reconstruct the evolutionary history of C. arvense and estimate how often it may have colonized North America, (2) compare the genetic diversity between European and North American populations to detect signs of demographic bottlenecks and/or patterns of population admixture, and (3) conduct bioclimatic comparisons to infer eventual niche shifts following this species’ introduction into North America. Location Europe and North America. Methods A total of 1522 individuals from 58 populations were investigated with six microsatellite markers. Estimates of heterozygosity (H_E) and allelic richness (R_S) were quantified for each population, and population structure was inferred via analyses of molecular variance (AMOVAs), principal components analyses (PCAs), Mantel tests and Bayesian clustering analyses. Climatic niche spaces were based on 19 bioclimatic variables extracted from approximately 32,000 locations covering the entire range, and compared using PCA and hierarchical cluster analysis. Results Although there is evidence of multiple introductions from divergent European lineages, North American populations of C. arvense exhibited significantly lower levels of genetic diversity than their putative ancestors. Bioclimatic comparisons pointed to a high degree of niche conservatism during invasion, but indicated that genotypes from the former USSR and Central European mountain chains were probably best adapted to invade North America upon entry into the continent. Main conclusions Genetic and historical data suggest that C. arvense first entered North America from Western Europe with the first European settlers, and was later introduced from Eastern Europe into the prairie states during the agricultural boom. The species went through a significant bottleneck following its introduction into the New World, but the level of genetic diversity remained high owing to admixture between genetically differentiated lineages and to a highly efficient outcrossing breeding system.     

Tracking invasion histories in the sea: facing complex scenarios using multilocus data

In recent years, new analytical tools have allowed researchers to extract historical information contained in molecular data, which has fundamentally transformed our understanding of processes ruling biological invasions. However, the use of these new analytical tools has been largely restricted to studies of terrestrial organisms despite the growing recognition that the sea contains ecosystems that are amongst the most heavily affected by biological invasions, and that marine invasion histories are often remarkably complex. Here, we studied the routes of invasion and colonisation histories of an invasive marine invertebrate Microcosmus squamiger (Ascidiacea) using microsatellite loci, mitochondrial DNA sequence data and 11 worldwide populations. Discriminant analysis of principal components, clustering methods and approximate bayesian computation (ABC) methods showed that the most likely source of the introduced populations was a single admixture event that involved populations from two genetically differentiated ancestral regions--the western and eastern coasts of Australia. The ABC analyses revealed that colonisation of the introduced range of M. squamiger consisted of a series of non-independent introductions along the coastlines of Africa, North America and Europe. Furthermore, we inferred that the sequence of colonisation across continents was in line with historical taxonomic records--first the Mediterranean Sea and South Africa from an unsampled ancestral population, followed by sequential introductions in California and, more recently, the NE Atlantic Ocean. We revealed the most likely invasion history for world populations of M. squamiger, which is broadly characterized by the presence of multiple ancestral sources and non-independent introductions within the introduced range. The results presented here illustrate the complexity of marine invasion routes and identify a cause-effect relationship between human-mediated transport and the success of widespread marine non-indigenous species, which benefit from stepping-stone invasions and admixture processes involving different sources for the spread and expansion of their range.     

Nuclear and chloroplast microsatellites show multiple introductions in the worldwide invasion history of common ragweed, Ambrosia artemisiifolia

Background

Ambrosia artemisiifolia is a North American native that has become one of the most problematic invasive plants in Europe and Asia. We studied its worldwide population genetic structure, using both nuclear and chloroplast microsatellite markers and an unprecedented large population sampling. Our goals were (i) to identify the sources of the invasive populations; (ii) to assess whether all invasive populations were founded by multiple introductions, as previously found in France; (iii) to examine how the introductions have affected the amount and structure of genetic variation in Europe; (iv) to document how the colonization of Europe proceeded; (v) to check whether populations exhibit significant heterozygote deficiencies, as previously observed.

Principal Findings

We found evidence for multiple introductions of A. artemisiifolia, within regions but also within populations in most parts of its invasive range, leading to high levels of diversity. In Europe, introductions probably stem from two different regions of the native area: populations established in Central Europe appear to have originated from eastern North America, and Eastern European populations from more western North America. This may result from differential commercial exchanges between these geographic regions. Our results indicate that the expansion in Europe mostly occurred through long-distance dispersal, explaining the absence of isolation by distance and the weak influence of geography on the genetic structure in this area in contrast to the native range. Last, we detected significant heterozygote deficiencies in most populations. This may be explained by partial selfing, biparental inbreeding and/or a Wahlund effect and further investigation is warranted.

Conclusions

This insight into the sources and pathways of common ragweed expansion may help to better understand its invasion success and provides baseline data for future studies on the evolutionary processes involved during range expansion in novel environments.     

A few north Appalachian populations are the source of European black locust

The role of evolution in biological invasion studies is often overlooked. In order to evaluate the evolutionary mechanisms behind invasiveness, it is crucial to identify the source populations of the introduction. Studies in population genetics were carried out on Robinia pseudoacacia L., a North American tree which is now one of the worst invasive tree species in Europe. We realized large‐scale sampling in both the invasive and native ranges: 63 populations were sampled and 818 individuals were genotyped using 113 SNPs. We identified clonal genotypes in each population and analyzed between and within range population structure, and then, we compared genetic diversity between ranges, enlarging the number of SNPs to mitigate the ascertainment bias. First, we demonstrated that European black locust was introduced from just a limited number of populations located in the Appalachian Mountains, which is in agreement with the historical documents briefly reviewed in this study. Within America, population structure reflected the effects of long‐term processes, whereas in Europe it was largely impacted by human activities. Second, we showed that there is a genetic bottleneck between the ranges with a decrease in allelic richness and total number of alleles in Europe. Lastly, we found more clonality within European populations. Black locust became invasive in Europe despite being introduced from a reduced part of its native distribution. Our results suggest that human activity, such as breeding programs in Europe and the seed trade throughout the introduced range, had a major role in promoting invasion; therefore, the introduction of the missing American genetic cluster to Europe should be avoided.     

The invasion route for an insect pest species: the tobacco aphid in the New World

Biological invasions are rapid evolutionary events in which populations are usually subject to a founder event during introduction followed by rapid adaptation to the new environment. Molecular tools and Bayesian approaches have shown their utility in exploring different evolutionary scenarios regarding the invasion routes of introduced species. We examined the situation for the tobacco aphid, Myzus persicae nicotianae, a recently introduced aphid species in Chile. Using seven microsatellite loci and approximate Bayesian computation, we studied populations of the tobacco aphid sampled from several American and European countries, identifying the most likely source populations and tracking the route of introduction to Chile. Our population genetic data are consistent with available historical information, pointing to an introduction route of the tobacco aphid from Europe and/or from other putative populations (e.g. Asia) with subsequent introduction through North America to South America. Evidence of multiple introductions to North America from different genetic pools, with successive loss of genetic diversity from Europe towards North America and a strong bottleneck during the southward introduction to South America, was also found. Additionally, we examined the special case of a widespread multilocus genotype that was found in all American countries examined. This case provides further evidence for the existence of highly successful genotypes or 'superclones' in asexually reproducing organisms.     

Evidence for multiple introductions of Phragmites australis to North America: detection of a new non-native haplotype

We found a new non-native haplotype of Phragmites australis in North America that provides convincing evidence for multiple introductions of this highly invasive reed from Europe. Prior to our detection of this new non-native haplotype, invasion of North America by this reed grass was thought to be limited to a single cp-DNA haplotype–haplotype M. However, we found two sites colonized by haplotype L1 in Quebec, Canada, a haplotype native to northern Europe, Great Britain and Romania. Because the invasion of North America by P. australis is ongoing, and because there is evidence for intra- and inter-specific hybridization and increased fecundity resulting from outcrossing, more attention should be paid to genetic differences and associated vigor of populations of introduced Phragmites across North America.     

The chestnut blight fungus world tour: successive introduction events from diverse origins in an invasive plant fungal pathogen

Clonal expansion has been observed in several invasive fungal plant pathogens colonizing new areas, raising the question of the origin of clonal lineages. Using microsatellite markers, we retraced the evolutionary history of introduction of the chestnut blight fungus, Cryphonectria parasitica, in North America and western Europe. Combining discriminant analysis of principal components and approximate Bayesian computation analysis, we showed that several introduction events from genetically differentiated source populations have occurred in both invaded areas. In addition, a low signal of genetic recombination among different source populations was suggested in North America. Finally, two genetic lineages were present in both invaded areas as well as in the native areas, suggesting the existence of genetic lineages with a high capacity to establish in diverse environments and host species. This study confirmed the importance of multiple introductions, but questioned the role of genetic admixture in the success of introduction of a fungal plant pathogen.     

Genetic Bottlenecks in Time and Space: Reconstructing Invasions from Contemporary and Historical Collections

Herbarium accession data offer a useful historical botanical perspective and have been used to track the spread of plant invasions through time and space. Nevertheless, few studies have utilised this resource for genetic analysis to reconstruct a more complete picture of historical invasion dynamics, including the occurrence of separate introduction events. In this study, we combined nuclear and chloroplast microsatellite analyses of contemporary and historical collections of Senecio madagascariensis, a globally invasive weed first introduced to Australia c. 1918 from its native South Africa. Analysis of nuclear microsatellites, together with temporal spread data and simulations of herbarium voucher sampling, revealed distinct introductions to south-eastern Australia and mid-eastern Australia. Genetic diversity of the south-eastern invasive population was lower than in the native range, but higher than in the mid-eastern invasion. In the invasive range, despite its low resolution, our chloroplast microsatellite data revealed the occurrence of new haplotypes over time, probably as the result of subsequent introduction(s) to Australia from the native range during the latter half of the 20^th century. Our work demonstrates how molecular studies of contemporary and historical field collections can be combined to reconstruct a more complete picture of the invasion history of introduced taxa. Further, our study indicates that a survey of contemporary samples only (as undertaken for the majority of invasive species studies) would be insufficient to identify potential source populations and occurrence of multiple introductions.     

Inferring the origin of populations introduced from a genetically structured native range by approximate Bayesian computation: case study of the invasive ladybird Harmonia axyridis

Correct identification of the source population of an invasive species is a prerequisite for testing hypotheses concerning the factors responsible for biological invasions. The native area of invasive species may be large, poorly known and/or genetically structured. Because the actual source population may not have been sampled, studies based on molecular markers may generate incorrect conclusions about the origin of introduced populations. In this study, we characterized the genetic structure of the invasive ladybird Harmonia axyridis in its native area using various population genetic statistics and methods. We found that native area of H. axyridis most probably consisted of two geographically distinct genetic clusters located in eastern and western Asia. We then performed approximate Bayesian computation (ABC) analyses on controlled simulated microsatellite data sets to evaluate (i) the risk of selecting incorrect introduction scenarios, including admixture between sources, when the populations of the native area are genetically structured and sampling is incomplete and (ii) the ability of ABC analysis to minimize such risks by explicitly including unsampled populations in the scenarios compared. Finally, we performed additional ABC analyses on real microsatellite data sets to retrace the origin of biocontrol and invasive populations of H. axyridis, taking into account the possibility that the structured native area may have been incompletely sampled. We found that the invasive population in eastern North America, which has served as the bridgehead for worldwide invasion by H. axyridis, was probably formed by an admixture between the eastern and western native clusters. This admixture may have facilitated adaptation of the bridgehead population.