Genetic structure and invasion history of the house mouse (Mus musculus domesticus) in Senegal, West Africa: a legacy of colonial and contemporary times.

Knowledge of the genetic make-up and demographic history of invasive populations is critical to understand invasion mechanisms. Commensal rodents are ideal models to study whether complex invasion histories are typical of introductions involving human activities. The house mouse Mus musculus domesticus is a major invasive synanthropic rodent originating from South-West Asia. It has been largely studied in Europe and on several remote islands, but the genetic structure and invasion history of this taxon have been little investigated in several continental areas, including West Africa. In this study, we focussed on invasive populations of M. m. domesticus in Senegal. In this focal area for European settlers, the distribution area and invasion spread of the house mouse is documented by decades of data on commensal rodent communities. Genetic variation at one mitochondrial locus and 16 nuclear microsatellite markers was analysed from individuals sampled in 36 sites distributed across the country. A combination of phylogeographic and population genetics methods showed that there was a single introduction event on the northern coast of Senegal, from an exogenous (probably West European) source, followed by a secondary introduction from northern Senegal into a coastal site further south. The geographic locations of these introduction sites were consistent with the colonial history of Senegal. Overall, the marked microsatellite genetic structure observed in Senegal, even between sites located close together, revealed a complex interplay of different demographic processes occurring during house mouse spatial expansion, including sequential founder effects and stratified dispersal due to human transport along major roads.

Invasion genetics of a human commensal rodent: the black rat Rattus rattus in Madagascar.

Studies focusing on geographical genetic patterns of commensal species and on human history complement each other and provide proxies to trace common colonization events. On Madagascar, the unintentional introduction and spread of the commensal species Rattus rattus by people may have left a living clue of human colonization patterns and history. In this study, we addressed this question by characterizing the genetic structure of natural populations of R. rattus using both microsatellites and mitochondrial sequences, on an extensive sampling across the island. Such data sets were analysed by a combination of methods using population genetics, phylogeography and approximate Bayesian computation. Our results indicated two introduction events to Madagascar from the same ancestral source of R. rattus, one in the extreme north of the island and the other further south. The latter was the source of a large spatial expansion, which may have initially started from an original point located on the southern coast. The inferred timing of introduction events-several centuries ago-is temporally congruent with the Arabian trade network in the Indian Ocean, which was flourishing from the middle of the first millennium.

Rapid increase in dispersal during range expansion in the invasive ladybird Harmonia axyridis.

The evolutionary trajectories associated with demographic, genetic and spatial disequilibrium have become an issue of growing interest in population biology. Invasive species provide unique opportunities to explore the impact of recent range expansion on life-history traits, making it possible to test for a spatial arrangement of dispersal abilities along the expanding range, in particular. We carried out controlled experiments in laboratory conditions to test the hypothesis of an increase in dispersal capacity with range expansion in Harmonia axyridis, a ladybird that has been invading Europe since 2001. We found a marked increase in the flight speed of the insects from the core to the front of the invasion range in two independent sampling transects. By contrast, we found that two other traits associated with dispersal (endurance and motivation to fly off) did not follow the same spatial gradient. Our results provide a striking illustration of the way in which predictable directional genetic changes may occur rapidly for some traits associated with dispersal during biological invasions. We discuss the consequences of our results for invasion dynamics and the evolutionary outcomes of spatially expanding populations.

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.

Experimental evidence for the phenotypic impact of admixture between wild and biocontrol Asian ladybird (Harmonia axyridis) involved in the European invasion.

Hybridization can fuel evolutionary processes during biological invasions. The harlequin ladybird Harmonia axyridis has long been used as a biocontrol agent before the species became invasive worldwide. Previous analysis based on microsatellite data has shown that European invasive populations bear traces of admixture between an eastern North American source, which is at the origin of the worldwide invasion, and biocontrol strains used in Europe. In this study, we tested the hypothesis that this early admixture event may have fostered the European invasion by impacting on the phenotypes of wild European populations. Mean life history traits of experimental F(1) hybrids are compared with pure parental sources and wild European crosses. Our results reveal a biased impact whereby North American beetles benefitted from being admixed with European biocontrol strains. Resemblance between experimental hybrids and wild European invasive crosses further suggests a long-lasting effect of admixture that may still be at work and fostering invasiveness.

Thelytokous parthenogenesis, male clonality and genetic caste determination in the little fire ant: new evidence and insights from the lab.

Previous studies indicate that some populations of the little fire ant, Wasmannia auropunctata, display an unusual reproduction system polymorphism. Although some populations have a classical haplodiploid reproduction system, in other populations queens are produced by thelytokous parthenogenesis, males are produced by a male clonality system and workers are produced sexually. An atypical genetic caste determination system was also suggested. However, these conclusions were indirectly inferred from genetic studies on field population samples. Here we set up experimental laboratory nests that allow the control of the parental relationships between individuals. The queens heading those nests originated from either putatively clonal or sexual populations. We characterized the male, queen and worker offspring they produced at 12 microsatellite loci. Our results unambiguously confirm the unique reproduction system polymorphism mentioned above and that male clonality is strictly associated with thelytokous parthenogenesis. We also observed direct evidence of the rare production of sexual gynes and arrhenotokous males in clonal populations. Finally, we obtained evidence of a genetic basis for caste determination. The evolutionary significance of the reproduction system polymorphism and genetic caste determination as well as future research opportunities are discussed.

Inferring introduction routes of invasive species using approximate Bayesian computation on microsatellite data.

Determining the routes of introduction provides not only information about the history of an invasion process, but also information about the origin and construction of the genetic composition of the invading population. It remains difficult, however, to infer introduction routes from molecular data because of a lack of appropriate methods. We evaluate here the use of an approximate Bayesian computation (ABC) method for estimating the probabilities of introduction routes of invasive populations based on microsatellite data. We considered the crucial case of a single source population from which two invasive populations originated either serially from a single introduction event or from two independent introduction events. Using simulated datasets, we found that the method gave correct inferences and was robust to many erroneous beliefs. The method was also more efficient than traditional methods based on raw values of statistics such as assignment likelihood or pairwise F(ST). We illustrate some of the features of our ABC method, using real microsatellite datasets obtained for invasive populations of the western corn rootworm, Diabrotica virgifera virgifera. Most computations were performed with the DIYABC program (http://www1.montpellier.inra.fr/CBGP/diyabc/).

Parental crowding influences life-history traits in Locusta migratoria females.

Parental environments could play an important role in controlling insect outbreaks, provided they influence changes in physiological, developmental or behavioural life-history traits related to fluctuations in population density. However, the potential implication of parental influence in density-related changes in life-history traits remains unclear in many insects that exhibit fluctuating population dynamics, particularly locusts. In this study, we report a laboratory experiment, which enabled us to characterize the life-history trait modifications induced by parental crowding of female individuals from a frequently outbreaking population of Locusta migratoria (Linnaeus) (Orthoptera: Acrididae). We found that a rearing history of crowding led to reduced female oviposition times and increased offspring size but did not affect the developmental time, survival, fecundity, and the sex-ratio and the number of offspring. Because all studied females were raised in a common environment (isolation conditions), these observed reproductive differences are due to trans-generational effects induced by density. We discuss the ecological and evolutionary implications of the observed density-dependent parental effects on the life-history of L. migratoria.

Spatial genetic structure of a small rodent in a heterogeneous landscape.

Gene flow in natural populations may be strongly influenced by landscape features. The integration of landscape characteristics in population genetic studies may thus improve our understanding of population functioning. In this study, we investigated the population genetic structure and gene flow pattern for the common vole, Microtus arvalis, in a heterogeneous landscape characterised by strong spatial and temporal variation. The studied area is an intensive agricultural zone of approximately 500 km(2) crossed by a motorway. We used individual-based Bayesian methods to define the number of population units and their spatial borders without prior delimitation of such units. Unexpectedly, we determined a single genetic unit that covered the entire area studied. In particular, the motorway considered as a likely barrier to dispersal was not associated with any spatial genetic discontinuity. Using computer simulations, we demonstrated that recent anthropogenic barriers to effective dispersal are difficult to detect through analysis of genetic variation for species with large effective population sizes. We observed a slight, but significant, pattern of isolation by distance over the whole study site. Spatial autocorrelation analyses detected genetic structuring on a local scale, most probably due to the social organisation of the study species. Overall, our analysis suggests intense small-scale dispersal associated with a large effective population size. High dispersal rates may be imposed by the strong spatio-temporal heterogeneity of habitat quality, which characterises intensive agroecosystems.

Invasion of Europe by the western corn rootworm, Diabrotica virgifera virgifera: multiple transatlantic introductions with various reductions of genetic diversity.

The early stages of invasion involve demographic bottlenecks that may result in lower genetic variation in introduced populations as compared to source population/s. Low genetic variability may decrease the adaptive potential of such populations in their new environments. Previous population genetic studies of invasive species have reported varying levels of losses of genetic variability in comparisons of source and invasive populations. However, intraspecific comparisons are required to assess more thoroughly the repeatability of genetic consequences of colonization events. Descriptions of invasive species for which multiple introductions from a single source population have been demonstrated may be particularly informative. The western corn rootworm (WCR), Diabrotica virgifera virgifera, native to North America and invasive in Europe, offers us an opportunity to analyse multiple introduction events within a single species. We investigated within- and between-population variation at eight microsatellite markers in WCR in North America and Europe to investigate the routes by which WCR was introduced into Europe, and to assess the effect of introduction events on genetic variation. We detected five independent introduction events from the northern USA into Europe. The diversity loss following these introductions differed considerably between events, suggesting substantial variation in introduction, foundation and/or establishment conditions. Genetic variability at evolutionarily neutral loci does not seem to underlie the invasive success of WCR in Europe. We also showed that the introduction of WCR into Europe resulted in the redistribution of genetic variance from the intra- to the interpopulational level contrary to most examples of multiple introductions.

Do outbreaks affect genetic population structure? A worldwide survey in Locusta migratoria, a pest plagued by microsatellite null alleles.

An understanding of the role of factors intrinsic to a species' life history in structuring contemporary genetic variation is a fundamental, but understudied, aspect of evolutionary biology. Here, we assessed the influence of the propensity to outbreak in shaping worldwide genetic variation in Locusta migratoria, a cosmopolitan pest well known for its expression of density-dependent phase polyphenism. We scored 14 microsatellites in nine subspecies from 25 populations distributed over most of the species' range in regions that vary in the historical frequency and extent of their outbreaks. We rejected the hypothesis that L. migratoria consists of two genetically distinct clusters adapted to habitats either rarely (nonoutbreaking) or cyclically (outbreaking) favourable to increases in population density. We also invalidated the current subspecific taxonomic classification based on morphometrics. Bayesian inferences indicated evidence of a homogenizing effect of outbreaks on L. migratoria population structure. Geographical and ecological barriers to gene flow in conjunction with historical events can also explain the observed patterns. By systematically assessing the effects of null alleles using computer simulations, we also provide a template for the analysis of microsatellite data sets characterized by a high prevalence of null alleles.

Absence of genetic divergence between western corn rootworms (Coleoptera: Chrysomelidae) resistant and susceptible to control by crop rotation.

The western corn rootworm, Diabrotica virgifera virgifera LeConte (Coleoptera: Chrysomelidae), is a major pest of corn, Zea mays L., in North America that has recently invaded Europe. A loss of ovipositional fidelity to cornfields has allowed the species to circumvent crop rotation as a means of control in part of its range in the United States. Analyses of variation at eight microsatellite loci provided no evidence for general genetic differentiation between samples of western corn rootworm collected in soybean, Glycine max (L.) Merr., fields and those collected in cornfields both inside and outside the rotation-resistance problem area. This result suggests that few or no barriers to gene flow exist between rotation-resistant and -susceptible rootworm populations. The implications of this result for the management of western corn rootworm in North America and Europe are discussed.

Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models.

Samples from nine populations belonging to three African (intermissa, scutellata and capensis) and four European (mellifera, ligustica, carnica and cecropia) Apis mellifera subspecies were scored for seven microsatellite loci. A large amount of genetic variation (between seven and 30 alleles per locus) was detected. Average heterozygosity and average number of alleles were significantly higher in African than in European subspecies, in agreement with larger effective population sizes in Africa. Microsatellite analyses confirmed that A. mellifera evolved in three distinct and deeply differentiated lineages previously detected by morphological and mitochondrial DNA studies. Dendrogram analysis of workers from a given population indicated that super-sisters cluster together when using a sufficient number of microsatellite data whereas half-sisters do not. An index of classification was derived to summarize the clustering of different taxonomic levels in large phylogenetic trees based on individual genotypes. Finally, individual population x loci data were used to test the adequacy of the two alternative mutation models, the infinite allele model (IAM) and the stepwise mutation models. The better fit overall of the IAM probably results from the majority of the microsatellites used including repeats of two or three different length motifs (compound microsatellites).

New methods employing multilocus genotypes to select or exclude populations as origins of individuals.

A new method for assigning individuals of unknown origin to populations, based on the genetic distance between individuals and populations, was compared to two existing methods based on the likelihood of multilocus genotypes. The distribution of the assignment criterion (genetic distance or genotype likelihood) for individuals of a given population was used to define the probability that an individual belongs to the population. Using this definition, it becomes possible to exclude a population as the origin of an individual, a useful extension of the currently available assignment methods. Using simulated data based on the coalescent process, the different methods were evaluated, varying the time of divergence of populations, the mutation model, the sample size, and the number of loci. Likelihood-based methods (especially the Bayesian method) always performed better than distance methods. Other things being equal, genetic markers were always more efficient when evolving under the infinite allele model than under the stepwise mutation model, even for equal values of the differentiation parameter F(st). Using the Bayesian method, a 100% correct assignment rate can be achieved by scoring ca. 10 microsatellite loci (H approximately 0.6) on 30-50 individuals from each of 10 populations when the F(st) is near 0.1.

Inferring population history from microsatellite and enzyme data in serially introduced cane toads, Bufo marinus.

Much progress has been made on inferring population history from molecular data. However, complex demographic scenarios have been considered rarely or have proved intractable. The serial introduction of the South-Central American cane toad Bufo marinus in various Caribbean and Pacific islands involves four major phases: a possible genetic admixture during the first introduction, a bottleneck associated with founding, a transitory population boom, and finally, a demographic stabilization. A large amount of historical and demographic information is available for those introductions and can be combined profitably with molecular data. We used a Bayesian approach to combine this information with microsatellite (10 loci) and enzyme (22 loci) data and used a rejection algorithm to simultaneously estimate the demographic parameters describing the four major phases of the introduction history. The general historical trends supported by microsatellites and enzymes were similar. However, there was a stronger support for a larger bottleneck at introductions for microsatellites than enzymes and for a more balanced genetic admixture for enzymes than for microsatellites. Very little information was obtained from either marker about the transitory population boom observed after each introduction. Possible explanations for differences in resolution of demographic events and discrepancies between results obtained with microsatellites and enzymes were explored. Limits of our model and method for the analysis of nonequilibrium populations were discussed.

Investigating the genetic load of an emblematic invasive species: the case of the invasive harlequin ladybird Harmonia axyridis.

Introduction events can lead to admixture between genetically differentiated populations and bottlenecks in population size. These processes can alter the adaptive potential of invasive species by shaping genetic variation, but more importantly, they can also directly affect mean population fitness either increasing it or decreasing it. Which outcome is observed depends on the structure of the genetic load of the species. The ladybird Harmonia axyridis is a good example of invasive species where introduced populations have gone through admixture and bottleneck events. We used laboratory experiments to manipulate the relatedness among H. axyridis parental individuals to assess the possibility for heterosis or outbreeding depression in F1 generation offspring for two traits related to fitness (lifetime performance and generation time). We found that inter-populations crosses had no major impact on the lifetime performance of the offspring produced by individuals from either native or invasive populations. Significant outbreeding depression was observed only for crosses between native populations for generation time. The absence of observed heterosis is indicative of a low occurrence of fixed deleterious mutations within both the native and invasive populations of H. axyridis. The observed deterioration of fitness in native inter-population crosses most likely results from genetic incompatibilities between native genomic backgrounds. We discuss the implications of these results for the structure of genetic load in H. axyridis in the light of the available information regarding the introduction history of this species.

Stratified dispersal and increasing genetic variation during the invasion of Central Europe by the western corn rootworm, Diabrotica virgifera virgifera.

Invasive species provide opportunities for investigating evolutionary aspects of colonization processes, including initial foundations of populations and geographic expansion. Using microsatellite markers and historical information, we characterized the genetic patterns of the invasion of the western corn rootworm (WCR), a pest of corn crops, in its largest area of expansion in Europe: Central and South-Eastern (CSE) Europe. We found that the invaded area probably corresponds to a single expanding population resulting from a single introduction of WCR and that gene flow is geographically limited within the population. In contrast to what is expected in classical colonization processes, an increase in genetic variation was observed from the center to the edge of the outbreak. Control measures against WCR at the center of the outbreak may have decreased effective population size in this area which could explain this observed pattern of genetic variation. We also found that small remote outbreaks in southern Germany and north-eastern Italy most likely originated from long-distance dispersal events from CSE Europe. We conclude that the large European outbreak is expanding by stratified dispersal, involving both continuous diffusion and discontinuous long-distance dispersal. This latter mode of dispersal may accelerate the expansion of WCR in Europe in the future.

Identification of 21 polymorphic microsatellites in the African parasitoid wasp, Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae).

We have developed 21 dinucleotide repeat microsatellite loci from African populations of Psyttalia lounsburyi (Silvestri) (Hymenoptera: Braconidae), a parasitoid wasp of the olive fruit fly, as part of a study assessing the role of introgression/hybridization in the success of a biological control introduction. We proposed suitable conditions for polymerase chain reaction multiplexing. All 21 loci were polymorphic with two to 21 alleles per locus within the Kenyan and South African populations tested. Most of them were successfully amplified in two other Psyttalia species.

Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods.

Drosophila subobscura is a Palearctic species that was first observed in South and North America in the early 1980s, and that rapidly invaded broad latitudinal ranges on both continents. To trace the source and history of this invasion, we obtained genotypic data on nine microsatellite loci from two South American, two North American and five European populations of D. subobscura. We analysed these data with traditional statistics as well as with an approximate Bayesian computation (ABC) framework. ABC methods yielded the strongest support for the scenario involving a serial introduction with founder events from Europe into South America, and then from South America into North America. Stable effective population size of the source population was very large (around one million individuals), and the propagule size was notably smaller for the introduction into South America (i.e. high bottleneck severity index with only a few effective founders) but considerably larger for the subsequent introduction into North America (i.e. low bottleneck severity index with around 100-150 effective founders). Finally, the Mediterranean region of Europe (and most likely Barcelona from the localities so far analysed) is proposed as the source of the New World flies, based on mean individual assignment statistics.