Estimation of the number of founders of an invasive pest insect population: the fire ant Solenopsis invicta in the USA

Determination of the number of founders responsible for the establishment of invasive populations is important for developing biologically based management practices, predicting the invasive potential of species, and making inferences about ecological and evolutionary processes. The fire ant Solenopsis invicta is a major invasive pest insect first introduced into the USA from its native South American range in the mid-1930s. We use data from diverse genetic markers surveyed in the source population and the USA to estimate the number of founders of this introduced population. Data from different classes of nuclear markers (microsatellites, allozymes, sex-determination locus) and mitochondrial DNA are largely congruent in suggesting that 9-20 unrelated mated queens comprised the initial founder group to colonize the USA at Mobile, Alabama. Estimates of founder group size based on expanded samples from throughout the southern USA were marginally higher than this, consistent with the hypothesis of one or more secondary introductions of the ant into the USA. The rapid spread and massive population build-up of introduced S. invicta occurred despite the loss of substantial genetic variation associated with the relatively small invasive propagule size, a pattern especially surprising in light of the substantial genetic load imposed by the loss of variation at the sex-determination locus.     

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.     

Population genetics reveals origin and number of founders in a biological invasion

Propagule pressure is considered the main determinant of success of biological invasions: when a large number of individuals are introduced into an area, the species is more likely to establish and become invasive. Nevertheless, precise data on propagule pressure exist only for a small sample of invasive species, usually voluntarily introduced. We studied the invasion of the American bullfrog, Rana catesbeiana, into Europe, a species that is considered a major cause of decline for native amphibians. For this major invader with scarce historical data, we used population genetics data (a partial sequence of the mitochondrial cytochrome b gene) to infer the invasion history and to estimate the number of founders of non-native populations. Based on differences between populations, at least six independent introductions from the native range occurred in Europe, followed by secondary translocations. Genetic diversity was strongly reduced in non-native populations, indicating a very strong bottleneck during colonization. We used simulations to estimate the precise number of founders and found that most non-native populations derive from less than six females. This capability of invasion from a very small number of propagules challenges usual management strategies; species with such ability should be identified at an early stage of introduction.     

Local-scale invasion pathways and small founder numbers in introduced Sacramento pikeminnow (Ptychocheilus grandis)

Given the general pattern of invasions with severe ecological consequences commonly resulting from multiple introductions of large numbers of individuals on the intercontinental scale, we explored an example of a highly successful, ecologically significant invader introduced over a short distance, possibly via minimal propagule pressure. The Sacramento pikeminnow (Ptychocheilus grandis) has been introduced to two coastal rivers in northern California where it poses a risk to threatened and endangered fishes. We assayed variation in seven microsatellite loci and one mitochondrial DNA gene to identify the source populations and estimate founder numbers for these introductions. Our analysis suggests that successful invasion of the Eel River was likely the result of a single transfer of 3–4 effective founders from nearby within the species’ native range: Clear Lake or its outflow Cache Creek. The other introduced population (Elk River), known from only seven individuals, likely represents secondary expansion from the introduced Eel River population. Our findings highlight the threat posed by close-range invaders and the ability of some fishes to rapidly invade ecologically suitable areas despite small effective founding numbers.     

Population genetics of an invasive species,Heracleum mantegazzianum: implications for the role of life history,demographics and independent introductions

The population genetic structure of an invasive, nonindigenous riparian weed (Heracleum mantegazzianum) in the northeast of England was investigated using microsatellite DNA markers. Data were used to assess the size and frequency of introductions into three catchments and the subsequent spread. We sampled 13 populations, including a remote population (Perivale, London) for comparison. Five loci were screened and considerable variation was found. Results revealed greater overall variation between populations from different catchments than those in the same catchment, and suggested the generation of population structure in the relatively short time since the initial introduction. Between-catchment variation may reflect population structure generated by local founders as the species spread and may indicate a large initial founder population at the time of the introduction into Britain, or multiple introductions. Within-catchment variation was consistent with expectations based on the water-borne dispersal of seeds in this species, and the relatively small dispersal range of likely pollinators. Independent introductions stand out in some cases as exceptions to the general pattern. Taken together the results are consistent with a relatively large initial founder population, and the subsequent spread of the species in local founder populations, followed by some level of inbreeding within local populations and novel introductions in some localities.     

Experimental island invasion of house mice

The ability of invasive species to recurrently establish populations from small numbers of founders, while threatened species struggle at the same low population sizes, is a paradox in conservation biology. Little is known about the mechanisms contributing to the post-arrival success of low density invasive populations as most invasive species research focuses on established, high density populations. Experimental studies are powerful, but generally limited to laboratory or invertebrate experiments. Here, we experimentally demonstrate that vertebrate mammal invasion from a very small (n = 2) number of founders follows relatively simple deterministic predictions. An intentional island invasion of introduced house mice (Mus musculus Linnaeus) from one founding pair closely tracked the density dependent logistic growth curve and reached the seasonal carrying capacity of a previously extant population in only 5 months. Carrying capacity reflected both density dependent and independent processes. In contrast to the previously incumbent population, the invading population retained a marked genetic signal of its recent founder event, but the populations were otherwise demographically indistinguishable. Stochastic events such as individual variability, supplemental immigration and ecological release, but not Allee effects, played important roles during colonisation, but following establishment dynamics rapidly became deterministic, with little demographic impact of reduced genetic diversity. The small population paradigm appears to have little influence on the population dynamics of highly successful invasive species.     

Molecular evidence for a founder effect in invasive house finch (Carpodacus mexicanus) populations experiencing an emergent disease epidemic

The impact of founder events on levels of genetic variation in natural populations remains a topic of significant interest. Well-documented introductions provide a valuable opportunity to examine how founder events influence genetic diversity in invasive species. House finches (Carpodacus mexicanus) are passerine birds native to western North America, with the large eastern North American population derived from a small number of captive individuals released in the 1940s. Previous comparisons using amplified fragment length polymorphism (AFLP) markers found equivalent levels of diversity in eastern and western populations, suggesting that any genetic effects of the founder event were ameliorated by the rapid growth of the newly established population. We used an alternative marker system, 10 highly polymorphic microsatellites, to compare levels of genetic diversity between four native and five introduced house finch populations. In contrast to the AFLP comparisons, we found significantly lower allelic richness and heterozygosity in introduced populations across all loci. Three out of five introduced populations showed significant reductions in the ratio of the number of alleles to the allele size range, a within-population characteristic of recent bottlenecks. Finally, native and introduced populations showed significant pairwise differences in allele frequencies in every case, with stronger isolation by distance within the introduced than native range. Overall, our results provide compelling molecular evidence for a founder effect during the introduction of eastern house finches that reduced diversity levels at polymorphic microsatellite loci and may have contributed to the emergence of the Mycoplasma epidemic which recently swept the eastern range of this species.     

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.     

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.     

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.     

Can genetic data confirm or refute historical records? The island invasion of the small Indian mongoose (Herpestes auropunctatus)

Many studies aimed at reconstructing the invasion history of a species rely, in part, on inferences based on patterns of genetic variation. These inferences warrant careful interpretation, however. In particular, given the time scale of most invasions, the typical demography of invasive species in their invaded range, and the available molecular tools, the underlying assumptions of population genetic models will often be violated. Given this fact, we examined the potential of population genetic data for reconstructing the history of serial introductions of the small Indian mongoose, Herpestes auropunctatus. We used simulations to test the power of existing microsatellite data for testing the credibility of historical introduction records. Although our results are generally consistent with most historical records for H. auropunctatus, the existing data have low power to reject alternative historical hypotheses. Simulations of a wide range of founder population sizes show broadly overlapping results, making rather different historical scenarios of introductions difficult to rule out with typical datasets. We advocate caution in the use of molecular population genetics to infer the history of invasive species, and we suggest extensive simulations as a tool to evaluate, in advance, this approach for addressing important research questions.     

Population genetic structure and the effect of founder events on the genetic variability of moose, Alces alces, in Canada

Moose, Alces alces, occur naturally throughout most of Canada but successful introductions of known numbers of animals have been made to the islands of Newfoundland and Cape Breton. Five microsatellite loci were used to investigate the population genetic structure and any change in genetic variability due to founder events of moose in Canada. Comparisons of allele frequencies for moose from 11 regions of the country suggested that there are at least seven genetically distinct populations (P < 0.05) in North America, namely Alberta, eastern Ontario, New Brunswick, Cape Breton, Labrador, western Newfoundland, and the Avalon Peninsula of Newfoundland. The average population heterozygosity was approximately 33% (range from 22 to 41%). UPGMA analysis of Nei's genetic distances produced phenograms similar to what would be expected when geographical location and population history are considered. The loss of heterozygosity due to a single founder event (n = 3; two introductions and a natural colonization) ranged from 14 to 30%, and the cumulative loss of heterozygosity due to two successive founder events (an introduction followed by a natural colonization) was 46%. In these examples loss of genetic variability has not been associated with any known phenotypic deviances, suggesting that populations may be established from a small number of founders. However, the viability of these founded populations over evolutionary timescales cannot be determined and is highly dependent upon chance.     

Genetic evidence for multiple introduction events of raccoons (Procyon lotor) in Spain

The common raccoon (Procyon lotor) is endemic to Central and North America, although non-native populations have become established around the world. In Spain, growing evidence of the introduction of raccoons has been reported across the country in the last decade, especially in Central Spain where the largest population is thought to occur. We used mitochondrial and microsatellite DNA data to investigate the genetics of invasive raccoons in Central Spain and to infer: the number of introduction events, the number of founders and the genetic variability of the introduced populations compared to a native population. We found that at least two introduction events have occurred along the Jarama and Henares Rivers in Central Spain, which currently constitute two genetically differentiated subpopulations. In both localities the number of effective founders from a native population was estimated as 2–4 individuals. These newly founded populations have expanded and show evidence of incipient contact and reproduction between them. This may allow for an increase in the genetic variability and adaptive potential of the population(s), possibly increasing the difficulty of controlling this invasive species. Our results reveal the ability to longitudinally monitor the genetics of the raccoon range expansion and emphasize the urgent need to control the pet trade of potentially invasive species.     

Limited mitochondrial DNA diversity is indicative of a small number of founders of the German raccoon (Procyon lotor) population

The raccoon (Procyon lotor) has successfully invaded central Europe, despite the population apparently having been founded by a small number of individuals in two distinct populations in Germany. The ecological success of the invasion has been explained by raccoons being an adaptable, truly omnivorous species. However, the German raccoon population might have a larger number of founders and be more genetically diverse than assumed, as accidental or deliberate releases of household pets or individuals from zoos are relatively common. In the present study, we sequenced a 550-base-pair long fragment of the mitochondrial control region in 193 raccoons from Germany and neighbouring countries. We only identified six different haplotypes; of which, five were limited to Germany. Our results support the notions that the population was founded by a small number of females and that the German raccoons originate from two separate release events in central and eastern Germany. Additionally, however, we provide evidence for the presence of a distinct population in Saxony, eastern Germany. Further studies using different genetic markers are necessary to gain additional information on genetic diversity and population genetic structure.     

Paradox lost: genetic diversity and the success of aquatic invasions

There is mounting evidence that reduced genetic diversity in invasive populations is not as commonplace as expected. Recent studies indicate that high propagule vectors, such as ballast water and shellfish transplantations, and multiple introductions contribute to the elimination of founder effects in the majority of successful aquatic invasions. Multiple introductions, in particular, can promote range expansion of introduced populations through both genetic and demographic mechanisms. Closely related to vectors and corridors of introduction, propagule pressure can play an important role in determining the genetic outcome of introduction events. Even low-diversity introductions have numerous means of avoiding the negative impact of diversity loss. The interaction of high propagule vectors and multiple introductions reveal important patterns associated with invasion success and deserve closer scrutiny.     

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.     

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.     

Genetic population structure of the masked palm civet Paguma larvata, (Carnivora: Viverridae) in Japan, revealed from analysis of newly identified compound microsatellites

The masked palm civet Paguma larvata (Carnivora: Viverridae) in Japan has been phylogeographically considered an introduced species from Taiwan. To reveal the population structures and relationships among the P. larvata populations in Japan, seven compound microsatellite loci were isolated from the genome and genotyped for 287 individuals collected from the field. STRUCTURE analysis and factorial correspondence analysis of genotyping data revealed that animals from Japan were divided into four genetic clusters. Geographic distribution of the genetic clusters partly referred to sampling areas, indicating multiple introductions into distinct areas of Japan or independent founding events leading to the generation of different genetic clusters within introduced populations in Japan. The large genetic differentiation of populations in the Shikoku District from those in other areas within Japan suggests that there were at least two introduction routes into Japan, and a possibility that some founders from areas other than Taiwan were also involved in the introduction into Japan. The genetic variation within Japanese populations were not markedly reduced compared with that of Taiwan. The results indicated that the Japanese populations of P. larvata could have retained moderate genetic diversity during founding events, because of multiple introductions, or a large number or high genetic diversity of founders. Although some individuals in Japan showed a sign of admixture between different clusters, there is no evidence that such an admixture markedly increased the genetic diversity within Japanese populations.     

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.     

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.