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.     

Linkage disequilibrium and phylogenetic congruence between chloroplast and mitochondrial haplotypes in Silene vulgaris

Both the chloroplast and mitochondrial genomes are used extensively in studies of plant population genetics and systematics. In the majority of angiosperms, the chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) are each primarily transmitted maternally, but rare biparental transmission is possible. The extent to which the cpDNA and mtDNA are in linkage disequilibrium is argued to be dependent on the fidelity of co-transmission and the population structure. This study reports complete linkage disequilibrium between cpDNA and mtDNA haplotypes in 86 individuals from 17 populations of Silene vulgaris, a gynodioecious plant species. Phylogenetic analysis of cpDNA and mtDNA haplotypes within 14 individuals supports a hypothesis that the evolutionary histories of the chloroplasts and mitochondria are congruent within S. vulgaris, as might be expected if this association persists for long periods. This provides the first documentation of the evolutionary consequences of long-term associations between chloroplast and mitochondrial genomes within a species. Factors that contribute to the phylogenetic and linkage associations, as well as the potential for intergenomic hitchhiking resulting from selection on genes in one organellar genome are discussed.     

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.     

Post-glacial history of Trillium grandiflorum (Melanthiaceae) in eastern North America: inferences from phylogeography

Dispersal and migration are important processes affecting the evolutionary history and genetics of species. Here we investigate post-glacial migration and gene flow in Trillium grandiflorum (Melanthiaceae), a wide-ranging, forest herb from eastern North America. Using phylogeographic approaches, we examined cpDNA and allozyme diversity in 35 populations of T. grandiflorum sampled from throughout the geographic range of the species. Nested clade analysis (NCA) of cpDNA haplotypes indicated that T. grandiflorum likely survived in two refugia in the southeastern US during the last glaciation and that long-distance dispersal characterized the post-glacial recolonization of northern areas. There was no evidence for reduced allozyme diversity in populations from glaciated compared to ice-free regions, probably because of the greater abundance and larger effective size of populations in the north. An analysis of isolation-by-distance based on the allozyme data suggested a pattern of population differentiation consistent with restricted gene flow. Notwithstanding the significance of rare seed dispersal events for migration, a comparison of allozyme and cpDNA genetic structure indicates that pollen flow between populations is more likely than seed dispersal. These results for T. grandiflorum represent the first phylogeographic analysis of a temperate woodland herb in eastern North America and support the importance of occasional long-distance dispersal events in the post-glacial migration of plants.     

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.     

Population structure in chicory (Cichorium intybus): A successful U.S. weed since the American revolutionary war

Plant invasions are recognized as major drivers of ecosystem change, yet the precise cause of these invasions remains unknown for many species. Frequency and modes of introductions during the first, transport and colonization, stages of the invasion process as well as phenotypic changes due to plasticity or changing genetic diversity and adaptation during later establishment and expansion stages can all influence the “success” of invasion. Here, we examine some of these factors in, and the origin of, a very successful weed, Cichorium intybus (chicory) which was introduced to North America in the 18th century and which now can be found in all 48 continental U.S. states and much of Canada. We genotyped a Eurasian collection of 11 chicory cultivars, nine native populations and a North American collection of 20 introduced wild populations which span the species range (592 individuals in total). To detect the geographic sources of North American chicory populations and to assess the genetic diversity among cultivars, native, and introduced populations, we used both a sequenced cpDNA region and 12 nuclear simple sequence repeat (SSR), microsatellite loci. Four cpDNA haplotypes were identified and revealed clear geographic subdivisions in the chicory native range and an interspecific hybrid origin of Radicchio group. Nuclear data suggested that domesticated lines deliberately introduced to North America were major contributors to extant weedy populations, although unintended sources such as seed contaminants likely also played important roles. The high private allelic richness and novel genetic groups were detected in some introduced populations, suggesting the potential for local adaptation in natural sites such as deserts and nature reserves. Our findings suggest that the current populations of weedy U.S. chicory have evolved primarily from several sources of domesticated and weedy ancestors and subsequent admixture among escaped lineages.     

Comparison between mitochondrial and chloroplast DNA variation in the native range of Silene vulgaris

A detailed survey of mitochondrial and chloroplast diversity in eight populations of Silene vulgaris from Central Europe was conducted for comparison with previously published data on diversity from S. vulgaris populations in the introduced range. Mitochondrial DNA (mtDNA) variation around the coxI gene was assessed with Southern blotting/restriction fragment length polymorphism methods. Chloroplast variation was assessed by sequencing the intergenic spacer separating the trnH and psbA genes. Thirty mtDNA haplotypes and 24 chloroplast DNA (cpDNA) haplotypes were found within 86 individuals. The overall genetic diversity h (0.941 for mitochondrial, and 0.893 for chloroplast markers) and within-population diversity were higher than reported in previous population studies of S. vulgaris in the USA and Europe. The frequency of private alleles was surprisingly high - more than 90% for both kinds of markers. Most of our populations were large and located in relatively undisturbed meadows, whereas surveys in Virginia consisted of smaller roadside populations. The slow rate of population turnover in European populations is discussed as a factor responsible for the relatively high diversity of S. vulgaris in undisturbed areas of its native range. Association between mtDNA and cpDNA haplotypes was also demonstrated. Finally, gender and mtDNA haplotype were associated in the Alps populations, where females were very rare.     

Evolutionary history of Silene latifolia sex chromosomes revealed by genetic mapping of four genes

The sex chromosomes of dioecious white campion, Silene latifolia (Caryophyllaceae), are of relatively recent origin (10-20 million years), providing a unique opportunity to trace the origin and evolution of sex chromosomes in this genus by comparing closely related Silene species with and without sex chromosomes. Here I demonstrate that four genes that are X-linked in S. latifolia are also linked in nondioecious S. vulgaris, which is consistent with Ohno's (1967) hypothesis that sex chromosomes evolve from a single pair of autosomes. I also report a genetic map for four S. latifolia X-linked genes, SlX1, DD44X, SlX4, and a new X-linked gene SlssX, which encodes spermidine synthase. The order of the genes on the S. latifolia X chromosome and divergence between the homologous X- and Y-linked copies of these genes supports the "evolutionary strata" model, with at least three consecutive expansions of the nonrecombining region on the Y chromosome (NRY) in this plant species.     

Phylogeographic pattern of range expansion provides evidence for cryptic species lineages in Silene nutans in Western Europe

As a result of recent or past evolutionary processes, a single species might consist of distinct Evolutionary Significant Units (ESUs), even corresponding to cryptic species. Determining the underlying mechanisms of range shifts and the processes at work in the build-up of divergent ESUs requires elucidating the factors that contribute to population genetic divergence across a species'' range. We investigated the large-scale patterns of genetic structure in the perennial herbaceous plant species Silene nutans (Caryophyllaceae) in Western Europe. We sampled and genotyped 111 populations using 13 nuclear microsatellite loci and 6 plastid single-nucleotide polymorphisms. Broad-scale spatial population genetic structure was examined using Bayesian clustering, spatial multivariate analyses and measures of hierarchical genetic differentiation. The genotypic structure of S. nutans was typical of a predominantly allogamous mating system. We also identified plastid lineages with no intra-population polymorphism, mirroring two genetically differentiated nuclear lineages. No evidence of admixture was found. Spatial trends in genetic diversity further suggested independent leading-edge expansion associated with founding events and subsequent genetic erosion. Overall, our findings suggested speciation processes in S. nutans and highlighted striking patterns of distinct stepwise recolonisation of Western Europe shaped by Quaternary climate oscillations. Two main potential ESUs can be defined in Western Europe, corresponding to Eastern and Western nuclear-plastid lineages. In situ preservation of populations and genetic rescue implying ex situ conservation techniques should take the lineage identity into account. This is particularly true in Great Britain, northern France and Belgium, where S. nutans is rare and where distinct lineages co-occur in close contact.     

Human‐aided admixture may fuel ecosystem transformation during biological invasions: theoretical and experimental evidence

Biological invasions can transform our understanding of how the interplay of historical isolation and contemporary (human‐aided) dispersal affects the structure of intraspecific diversity in functional traits, and in turn, how changes in functional traits affect other scales of biological organization such as communities and ecosystems. Because biological invasions frequently involve the admixture of previously isolated lineages as a result of human‐aided dispersal, studies of invasive populations can reveal how admixture results in novel genotypes and shifts in functional trait variation within populations. Further, because invasive species can be ecosystem engineers within invaded ecosystems, admixture‐induced shifts in the functional traits of invaders can affect the composition of native biodiversity and alter the flow of resources through the system. Thus, invasions represent promising yet under‐investigated examples of how the effects of short‐term evolutionary changes can cascade across biological scales of diversity. Here, we propose a conceptual framework that admixture between divergent source populations during biological invasions can reorganize the genetic variation underlying key functional traits, leading to shifts in the mean and variance of functional traits within invasive populations. Changes in the mean or variance of key traits can initiate new ecological feedback mechanisms that result in a critical transition from a native ecosystem to a novel invasive ecosystem. We illustrate the application of this framework with reference to a well‐studied plant model system in invasion biology and show how a combination of quantitative genetic experiments, functional trait studies, whole ecosystem field studies and modeling can be used to explore the dynamics predicted to trigger these critical transitions.     

Northern range expansion of European populations of the wasp spider Argiope bruennichi is associated with global warming–correlated genetic admixture and population‐specific temperature adaptations

Poleward range expansions are observed for an increasing number of species, which may be an effect of global warming during the past decades. However, it is still not clear in how far these expansions reflect simple geographical shifts of species ranges, or whether new genetic adaptations play a role as well. Here, we analyse the expansion of the wasp spider Argiope bruennichi into Northern Europe during the last century. We have used a range‐wide sampling of contemporary populations and historical specimens from museums to trace the phylogeography and genetic changes associated with the range shift. Based on the analysis of mitochondrial, microsatellite and SNP markers, we observe a higher level of genetic diversity in the expanding populations, apparently due to admixture of formerly isolated lineages. Using reciprocal transplant experiments for testing overwintering tolerance, as well as temperature preference and tolerance tests in the laboratory, we find that the invading spiders have possibly shifted their temperature niche. This may be a key adaptation for survival in Northern latitudes. The museum samples allow a reconstruction of the invasion's genetic history. A first, small‐scale range shift started around 1930, in parallel with the onset of global warming. A more massive invasion of Northern Europe associated with genetic admixture and morphological changes occurred in later decades. We suggest that the latter range expansion into far Northern latitudes may be a consequence of the admixture that provided the genetic material for adaptations to new environmental regimes. Hence, global warming could have facilitated the initial admixture of populations and this resulted in genetic lineages with new habitat preferences.     

Mitochondrial DNA offers unique insights into invasion history of the common starling

Mitochondrial DNA (mtDNA) can be a powerful genetic marker for tracing origins and history of invasive populations. Here, we use mtDNA to address questions relevant to the understanding of invasion pathways of common starlings (Sturnus vulgaris) into Western Australia (WA) and discuss the utility of this marker to provide information useful to invasive species management. Mitochondrial sequence data indicate two geographically restricted genetic groups within Australia. Evidence of dispersal from genetically distinct sources outside the sampled range of starlings in Australia suggests increased vigilance by management agencies may be required to prevent further incursions from widely separated localities. Overall, genetic diversity in Australia was lower than in samples from the native range. Within Australia, genetic diversity was lowest in the most recently colonized area in the west, indicating that demographic bottlenecks have occurred in this area. Evidence of restricted dispersal between localities on the edge of the range expansion (ERE) in WA and other Australian sampling localities suggests that localized control within the ERE may be effective in preventing further range expansion. Signatures of spatial and demographic expansion are present in mismatch analyses from sampling localities located at the ERE, but neutrality indices did not support this finding, suggesting that the former may be more sensitive to recent expansion. Additionally, mismatch analyses support the presence of admixture, which is likely to have occurred pre-introduction. We compare our findings with those from a microsatellite study of the same samples and discuss how the mtDNA analyses used here offer valuable and unique insights into the invasion history of introduced species.     

Patterns of cyto-nuclear linkage disequilibrium in Silene latifolia: genomic heterogeneity and temporal stability

Non-random association of alleles in the nucleus and cytoplasmic organelles, or cyto-nuclear linkage disequilibrium (LD), is both an important component of a number of evolutionary processes and a statistical indicator of others. The evolutionary significance of cyto-nuclear LD will depend on both its magnitude and how stable those associations are through time. Here, we use a longitudinal population genetic data set to explore the magnitude and temporal dynamics of cyto-nuclear disequilibria through time. We genotyped 135 and 170 individuals from 16 and 17 patches of the plant species Silene latifolia in Southwestern VA, sampled in 1993 and 2008, respectively. Individuals were genotyped at 14 highly polymorphic microsatellite markers and a single-nucleotide polymorphism (SNP) in the mitochondrial gene, atp1. Normalized LD (D′) between nuclear and cytoplasmic loci varied considerably depending on which nuclear locus was considered (ranging from 0.005–0.632). Four of the 14 cyto-nuclear associations showed a statistically significant shift over approximately seven generations. However, the overall magnitude of this disequilibrium was largely stable over time. The observed origin and stability of cyto-nuclear LD is most likely caused by the slow admixture between anciently diverged lineages within the species'' newly invaded range, and the local spatial structure and metapopulation dynamics that are known to structure genetic variation in this system.     

Evolutionary History of the Morocco lizard-Fingered Geckos of the <Emphasis Type="Italic">Saurodactylus brosseti</Emphasis> Complex

Studies of biodiversity in the Maghreb have revealed high genetic diversity and divergent genetic lineages among many taxa including squamates. Geographic barriers such as the Atlas Mountains are one of the key factors promoting genetic differentiation and the high levels of endemism. The lizard-fingered gecko Saurodactylus brosseti is endemic to Morocco. Its range includes both sides of the Atlas Mountains, and although high diversity was previously identified within the species, much of the range was unsampled. To understand the evolutionary and biogeographical history of this species, we used mitochondrial and nuclear DNA sequence data from 64 populations sampled across the entire species range. We employed phylogenetic methods based on gene trees and species trees as well as a time calibrated Bayesian genealogy and coalescent species delimitation approaches. We uncovered four highly divergent and allopatric mitochondrial lineages that did not share haplotypes at variable nuclear loci, suggesting the four groups have been evolving independently since the Miocene, according to our molecular dating estimates. These results coupled with the geographic pattern of genetic diversity suggest a possible role of the Atlas Mountains for the divergence observed between the four lineages of S. brosseti, while each lineage probably later underwent several episodes of fragmentation followed by (re-) expansion during Pleistocene climatic oscillations. Bayesian species delimitation analysis indicates that the four lineages may well be distinct species but we suggest that detailed morphological analyses are needed prior to taxonomic changes. The four lineages represent ancient independent evolutionary units, and deserve conservation management as distinct entities.     

Independent origin of sex chromosomes in two species of the genus Silene

Here we introduce a new model species, Silene colpophylla, that could facilitate research of sex chromosome evolution and sex-determining systems. This species is related to the well-established dioecious plant model Silene latifolia. Our results show that S. colpophylla is, similarly to S. latifolia, a male heterogametic species, but its sex chromosomes have evolved from a different pair of autosomes than in S. latifolia. The results of our phylogenetic study and mapping of homologs of S. latifolia X-linked genes indicate that the sex determination system in S. colpophylla evolved independently from that in S. latifolia. We assert that this model species pair will make it possible to study two independent patterns of sex chromosome evolution in related species.     

Inheritance of chloroplast DNA is not strictly maternal in Silene vulgaris (Caryophyllaceae): evidence from experimental crosses and natural populations

Chloroplast DNA (cpDNA) is maternally inherited in the majority, but not all, of angiosperm species. The mode of inheritance of cpDNA is a critical determinant of its molecular evolution and of its population genetic structure. Here, we present the results of investigations of the inheritance of cpDNA in Silene vulgaris, a plant used in a variety of studies in which cpDNA is an important component. PCR/RFLP markers were used to compare mother and offspring cpDNA genotypes sampled from two natural populations, and mother, father, and offspring genotypes obtained from controlled greenhouse crosses. Ten of 215 offspring cpDNA genotypes studied in the controlled crosses and three of 156 offspring from natural populations did not match that of the mother, demonstrating rare nonmaternal inheritance. That the chloroplast genome is occasionally transmitted through pollen is discussed in the context of using S. vulgaris cpDNA as a marker in studies of seed dispersal and when considering the joint evolution of the chloroplast and mitochondrial genomes.     

Glacial refugia in pathogens: European genetic structure of anther smut pathogens on Silene latifolia and Silene dioica

Climate warming is predicted to increase the frequency of invasions by pathogens and to cause the large-scale redistribution of native host species, with dramatic consequences on the health of domesticated and wild populations of plants and animals. The study of historic range shifts in response to climate change, such as during interglacial cycles, can help in the prediction of the routes and dynamics of infectious diseases during the impending ecosystem changes. Here we studied the population structure in Europe of two Microbotryum species causing anther smut disease on the plants Silene latifolia and Silene dioica. Clustering analyses revealed the existence of genetically distinct groups for the pathogen on S. latifolia, providing a clear-cut example of European phylogeography reflecting recolonization from southern refugia after glaciation. The pathogen genetic structure was congruent with the genetic structure of its host species S. latifolia, suggesting dependence of the migration pathway of the anther smut fungus on its host. The fungus, however, appeared to have persisted in more numerous and smaller refugia than its host and to have experienced fewer events of large-scale dispersal. The anther smut pathogen on S. dioica also showed a strong phylogeographic structure that might be related to more northern glacial refugia. Differences in host ecology probably played a role in these differences in the pathogen population structure. Very high selfing rates were inferred in both fungal species, explaining the low levels of admixture between the genetic clusters. The systems studied here indicate that migration patterns caused by climate change can be expected to include pathogen invasions that follow the redistribution of their host species at continental scales, but also that the recolonization by pathogens is not simply a mirror of their hosts, even for obligate biotrophs, and that the ecology of hosts and pathogen mating systems likely affects recolonization patterns.     

Retention of gene diversity during the spread of a non‐native plant species

Spatial expansion, which is a crucial stage in the process to successful biological invasion, is anticipated to profoundly affect the magnitude and spatial distribution of genetic diversity in novel colonized areas. Here, we show that, contrasting common expectations, Pyrenean rocket (Sisymbrium austriacum), retained SNP diversity as this introduced plant species descended in the Meuse River Basin. Allele frequencies did not mirror between‐population distances along the predominant expansion axis. Reconstruction of invasion history based on the genotypes of historical herbarium specimens indicated no influence of additional introductions or multiple points of entry on this nongradual pattern. Assignment analysis suggested the admixture of distant upstream sources in recently founded downstream populations. River dynamics seem to have facilitated occasional long‐distance dispersal which brought diversity to the expansion front and so maintained evolutionary potential. Our findings highlight the merit of a historical framework in interpreting extant patterns of genetic diversity in introduced species and underscore the need to integrate long‐distance dispersal events in theoretical work on the genetic consequences of range expansion.     

Multiple introductions,admixture and bridgehead invasion characterize the introduction history of Ambrosia artemisiifolia in Europe and Australia

Admixture between differentiated populations is considered to be a powerful mechanism stimulating the invasive success of some introduced species. It is generally facilitated through multiple introductions; however, the importance of admixture prior to introduction has rarely been considered. We assess the likelihood that the invasive Ambrosia artemisiifolia populations of Europe and Australia developed through multiple introductions or were sourced from a historical admixture zone within native North America. To do this, we combine large genomic and sampling data sets analysed with approximate Bayesian computation and random forest scenario evaluation to compare single and multiple invasion scenarios with pre‐ and postintroduction admixture simultaneously. We show the historical admixture zone within native North America originated before global invasion of this weed and could act as a potential source of introduced populations. We provide evidence supporting the hypothesis that the invasive populations established through multiple introductions from the native range into Europe and subsequent bridgehead invasion into Australia. We discuss the evolutionary mechanisms that could promote invasiveness and evolutionary potential of alien species from bridgehead invasions and admixed source populations.