Large haploblocks underlie rapid adaptation in the invasive weed Ambrosia artemisiifolia.

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. Here, we leverage extensive contemporary and historical collections of Ambrosia artemisiifolia-an aggressively invasive weed and primary cause of pollen-induced hayfever-to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks-indicative of chromosomal inversions-contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolia's global spread across vast climatic gradients.

Quantitative trait loci mapping reveals an oligogenic architecture of a rapidly adapting trait during the European invasion of common ragweed.

Biological invasions offer a unique opportunity to investigate evolution over contemporary timescales. Rapid adaptation to local climates during range expansion can be a major determinant of invasion success, yet fundamental questions remain about its genetic basis. This study sought to investigate the genetic basis of climate adaptation in invasive common ragweed (Ambrosia artemisiifolia). Flowering time adaptation is key to this annual species' invasion success, so much so that it has evolved repeated latitudinal clines in size and phenology across its native and introduced ranges despite high gene flow among populations. Here, we produced a high-density linkage map (4493 SNPs) and paired this with phenotypic data from an F2 mapping population (n = 336) to identify one major and two minor quantitative trait loci (QTL) underlying flowering time and height differentiation in this species. Within each QTL interval, several candidate flowering time genes were also identified. Notably, the major flowering time QTL detected in this study was found to overlap with a previously identified haploblock (putative inversion). Multiple genetic maps of this region identified evidence of suppressed recombination in specific genotypes, consistent with inversions. These discoveries support the expectation that a concentrated genetic architecture with fewer, larger, and more tightly linked alleles should underlie rapid local adaptation during invasion, particularly when divergently adapting populations experience high levels of gene flow.

Uncovering the genomic basis of an extraordinary plant invasion.

Invasive species are a key driver of the global biodiversity crisis, but the drivers of invasiveness, including the role of pathogens, remain debated. We investigated the genomic basis of invasiveness in Ambrosia artemisiifolia (common ragweed), introduced to Europe in the late 19th century, by resequencing 655 ragweed genomes, including 308 herbarium specimens collected up to 190 years ago. In invasive European populations, we found selection signatures in defense genes and lower prevalence of disease-inducing plant pathogens. Together with temporal changes in population structure associated with introgression from closely related Ambrosia species, escape from specific microbial enemies likely favored the plant's remarkable success as an invasive species.

The tip of the iceberg: Genome wide marker analysis reveals hidden hybridization during invasion.

Biological invasions are accelerating, and invasive species can have large economic impacts as well as severe consequences for biodiversity. During invasions, species can interact, potentially resulting in hybridization. Here, we examined two Cakile species, C. edentula and C. maritima (Brassicaceae), that co-occur and may hybridize during range expansion in separate regions of the globe. Cakile edentula invaded each location first, while C. maritima established later, apparently replacing the former. We assessed the evidence for hybridization in western North America and Australia, where both species have been introduced, and identified source populations with 4561 SNPs using Genotype-by-Sequencing. Our results indicate that C. edentula in Australia originated from one region of eastern North America while in western North America it is probably from multiple sources. Cakile maritima in Australia is derived from at least two different parts of Europe while the introduction in western North America is from one. Although morphological evidence of hybridization is generally limited to mixed species populations in Australia and virtually absent elsewhere, our genetic analysis revealed relatively high levels of hybridization in Australia (58% hybrids using Admixture) and supported the presence of hybrids in western North America (16% hybrids using Admixture) and New Zealand. Hybrids might be commonly overlooked in invaders, as identification based solely on morphological traits may represent only the tip of the iceberg. Our study reveals a repeated pattern of invasion, hybridization and apparent replacement of one species by another, which offers an opportunity to investigate the role of hybridization and introgression during invasion.

Genetically Based Trait Differentiation but Lack of Trade-offs between Stress Tolerance and Performance in Introduced Canada Thistle.

Trade-offs between performance and tolerance of abiotic and biotic stress have been proposed to explain both the success of invasive species and frequently observed size differences between native and introduced populations. Canada thistle seeds collected from across the introduced North American and the native European range were grown in benign and stressful conditions (nutrient stress, shading, simulated herbivory, drought, and mowing), to evaluate whether native and introduced individuals differ in performance or stress tolerance. An additional experiment assessed the strength of maternal effects by comparing plants derived from field-collected seeds with those derived from clones grown in the glasshouse. Introduced populations tended to be larger in size, but no trade-off of stress tolerance with performance was detected; introduced populations had either superior performance or equivalent trait values and survivorship in the treatment common gardens. We also detected evidence of parallel latitudinal clines of some traits in both the native and introduced ranges and associations with climate variables in some treatments, consistent with recent climate adaptation within the introduced range. Our results are consistent with rapid adaptation of introduced populations, but, contrary to predictions, the evolution of invasive traits did not come at the cost of reduced stress tolerance.

A lack of genetically compatible mates constrains the spread of an invasive weed.

Introduced populations often experience lag times before invasion, but the mechanisms constraining rapid expansions of introduced populations are unclear. Solidago altissima is a North American native plant with highly invasive Japanese populations and introduced Australian populations that are not invasive despite the climatic and ecological suitability of the region. By contrasting Australian with Japanese populations, we tested the hypothesis that Australian population growth is limited by a lack of long-distance dispersal via seeds owing to a limited number of compatible mates. In the field, Australian populations rarely produced viable seeds. A cross-pollination experiment found that Australian plants are fertile, yet lack compatible mates within Australia. Genetic analysis revealed that Australian individuals descend from a small set of self-incompatible genetic clones, which explains the negligible seed set within Australia. Our results show that low genetic diversity, leading to mate incompatibility, inhibits invasiveness of Australian S.  altissima, and provides compelling evidence for genetic, rather than ecological, factors constraining invasion in Australia.

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.

Convergent local adaptation to climate in distantly related conifers.

When confronted with an adaptive challenge, such as extreme temperature, closely related species frequently evolve similar phenotypes using the same genes. Although such repeated evolution is thought to be less likely in highly polygenic traits and distantly related species, this has not been tested at the genome scale. We performed a population genomic study of convergent local adaptation among two distantly related species, lodgepole pine and interior spruce. We identified a suite of 47 genes, enriched for duplicated genes, with variants associated with spatial variation in temperature or cold hardiness in both species, providing evidence of convergent local adaptation despite 140 million years of separate evolution. These results show that adaptation to climate can be genetically constrained, with certain key genes playing nonredundant roles.

Expression Divergence Is Correlated with Sequence Evolution but Not Positive Selection in Conifers.

The evolutionary and genomic determinants of sequence evolution in conifers are poorly understood, and previous studies have found only limited evidence for positive selection. Using RNAseq data, we compared gene expression profiles to patterns of divergence and polymorphism in 44 seedlings of lodgepole pine (Pinus contorta) and 39 seedlings of interior spruce (Picea glauca × engelmannii) to elucidate the evolutionary forces that shape their genomes and their plastic responses to abiotic stress. We found that rapidly diverging genes tend to have greater expression divergence, lower expression levels, reduced levels of synonymous site diversity, and longer proteins than slowly diverging genes. Similar patterns were identified for the untranslated regions, but with some exceptions. We found evidence that genes with low expression levels had a larger fraction of nearly neutral sites, suggesting a primary role for negative selection in determining the association between evolutionary rate and expression level. There was limited evidence for differences in the rate of positive selection among genes with divergent versus conserved expression profiles and some evidence supporting relaxed selection in genes diverging in expression between the species. Finally, we identified a small number of genes that showed evidence of site-specific positive selection using divergence data alone. However, estimates of the proportion of sites fixed by positive selection (α) were in the range of other plant species with large effective population sizes suggesting relatively high rates of adaptive divergence among conifers.

Conservation and divergence of gene expression plasticity following c. 140 million years of evolution in lodgepole pine (Pinus contorta) and interior spruce (Picea glauca×Picea engelmannii).

Species respond to environmental stress through a combination of genetic adaptation and phenotypic plasticity, both of which may be important for survival in the face of climatic change. By characterizing the molecular basis of plastic responses and comparing patterns among species, it is possible to identify how such traits evolve. Here, we used de novo transcriptome assembly and RNAseq to explore how patterns of gene expression differ in response to temperature, moisture, and light regime treatments in lodgepole pine (Pinus contorta) and interior spruce (a natural hybrid population of Picea glauca and Picea engelmannii). We found wide evidence for an effect of treatment on expression within each species, with 6413 and 11,658 differentially expressed genes identified in spruce and pine, respectively. Comparing patterns of expression among these species, we found that 74% of all orthologs with differential expression had a pattern that was conserved in both species, despite 140 million yr of evolution. We also found that the specific treatments driving expression patterns differed between genes with conserved versus diverged patterns of expression. We conclude that natural selection has probably played a role in shaping plastic responses to environment in these species.

The molecular basis of invasiveness: differences in gene expression of native and introduced common ragweed (Ambrosia artemisiifolia) in stressful and benign environments.

Although the evolutionary and ecological processes that contribute to plant invasion have been the focus of much research, investigation into the molecular basis of invasion is just beginning. Common ragweed (Ambrosia artemisiifolia) is an annual weed native to North America and has been introduced to Europe where it has become invasive. Using a custom-designed NimbleGen oligoarray, we examined differences in gene expression between five native and six introduced populations of common ragweed in three different environments (control, light stress and nutrient stress), as well as two different time points. We identified candidate genes that may contribute to invasiveness in common ragweed based on differences in expression between native and introduced populations from Europe. Specifically, we found 180 genes where range explained a significant proportion of the variation in gene expression and a further 103 genes with a significant range by treatment interaction. Several of these genes are potentially involved in the metabolism of secondary compounds, stress response and the detoxification of xenobiotics. Previously, we found more rapid growth and greater reproductive success in introduced populations, particularly in benign and competitive (light stress) environments, and many of these candidate genes potentially underlie these growth differences. We also found expression differences among populations within each range, reflecting either local adaptation or neutral processes, although no associations with climate or latitude were identified. These data provide a first step in identifying genes that are involved with introduction success in an aggressive annual weed.