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.

Airborne signals synchronize the defenses of neighboring plants in response to touch.

Plants activate defense-related pathways in response to subtle abiotic or biotic disturbances, changing their volatile profile rapidly. How such perturbations reach and potentially affect neighboring plants is less understood. We evaluated whether brief and light touching had a cascade effect on the profile of volatiles and gene expression of the focal plant and a neighboring untouched plant. Within minutes after contact, Zea mays showed an up-regulation of certain defense genes and increased the emission of specific volatiles that primed neighboring plants, making them less attractive for aphids. Exposure to volatiles from touched plants activated many of the same defense-related genes in non-touched neighboring plants, demonstrating a transcriptional mirroring effect for expression of genes up-regulated by brief contact. Perception of so-far-overlooked touch-induced volatile organic compounds was of ecological significance as these volatiles are directly involved in plant-plant communication as an effective trigger for rapid defense synchronization among nearby plants. Our findings shed new light on mechanisms of plant responses to mechanical contact at the molecular level and on the ecological role of induced volatiles as airborne signals in plant-plant interactions.

North European invasion by common ragweed is associated with early flowering and dominant changes in FT/TFL1 expression.

During the last two centuries, the North American common ragweed (Ambrosia artemisiifolia L.) invaded a large part of the globe. Local adaptation of this species was revealed by a common garden experiment, demonstrating that the distribution of the species in Europe could extend considerably to the North. Our study compares two populations of common ragweed (one from the native range and one from the invaded range) that differ in flowering time in the wild: the invasive population flowers earlier than the native population under non-inductive long-day photoperiods. Experiments conducted in controlled environments established that the two populations differ in their flowering time even under inductive short-day photoperiods, suggesting a change in autonomous flowering control. Genetic analysis revealed that early flowering is dominantly inherited and accompanied by the increased expression of the floral activator AaFTL1 and decreased expression of the floral repressor AaFTL2. Early flowering is also accompanied by reduced reproductive output, which is evolutionarily disadvantageous under long vegetation periods. In contrast, under short vegetation periods, only early-flowering plants can produce any viable seeds, making the higher seed set of late-flowering plants irrelevant. Thus, earlier flowering appears to be a specific adaptation to the higher latitudes of northern Europe.

New gSSR and EST-SSR markers reveal high genetic diversity in the invasive plant Ambrosia artemisiifolia L. and can be transferred to other invasive Ambrosia species.

Ambrosia artemisiifolia L., (common ragweed), is an annual invasive and highly troublesome plant species originating from North America that has become widespread across Europe. New sets of genomic and expressed sequence tag (EST) based simple sequence repeats (SSRs) markers were developed in this species using three approaches. After validation, 13 genomic SSRs and 13 EST-SSRs were retained and used to characterize the genetic diversity and population genetic structure of Ambrosia artemisiifolia populations from the native (North America) and invasive (Europe) ranges of the species. Analysing the mating system based on maternal families did not reveal any departure from complete allogamy and excess homozygosity was mostly due the presence of null alleles. High genetic diversity and patterns of genetic structure in Europe suggest two main introduction events followed by secondary colonization events. Cross-species transferability of the newly developed markers to other invasive species of the Ambrosia genus was assessed. Sixty-five percent and 75% of markers, respectively, were transferable from A. artemisiifolia to Ambrosia psilostachya and Ambrosia tenuifolia. 40% were transferable to Ambrosia trifida, this latter species being seemingly more phylogenetically distantly related to A. artemisiifolia than the former two.

Mechanistic species distribution modeling reveals a niche shift during invasion.

Niche shifts of nonnative plants can occur when they colonize novel climatic conditions. However, the mechanistic basis for niche shifts during invasion is poorly understood and has rarely been captured within species distribution models. We quantified the consequence of between-population variation in phenology for invasion of common ragweed (Ambrosia artemisiifolia L.) across Europe. Ragweed is of serious concern because of its harmful effects as a crop weed and because of its impact on public health as a major aeroallergen. We developed a forward mechanistic species distribution model based on responses of ragweed development rates to temperature and photoperiod. The model was parameterized and validated from the literature and by reanalyzing data from a reciprocal common garden experiment in which native and invasive populations were grown within and beyond the current invaded range. It could therefore accommodate between-population variation in the physiological requirements for flowering, and predict the potentially invaded ranges of individual populations. Northern-origin populations that were established outside the generally accepted climate envelope of the species had lower thermal requirements for bud development, suggesting local adaptation of phenology had occurred during the invasion. The model predicts that this will extend the potentially invaded range northward and increase the average suitability across Europe by 90% in the current climate and 20% in the future climate. Therefore, trait variation observed at the population scale can trigger a climatic niche shift at the biogeographic scale. For ragweed, earlier flowering phenology in established northern populations could allow the species to spread beyond its current invasive range, substantially increasing its risk to agriculture and public health. Mechanistic species distribution models offer the possibility to represent niche shifts by varying the traits and niche responses of individual populations. Ignoring such effects could substantially underestimate the extent and impact of invasions.

Phenological Variation in Ambrosia artemisiifolia L. Facilitates Near Future Establishment at Northern Latitudes.

The invasive weed Ambrosia artemisiifolia (common ragweed) constitutes a great threat to public health and agriculture in large areas of the globe. Climate change, characterized by higher temperatures and prolonged vegetation periods, could increase the risk of establishment in northern Europe in the future. However, as the species is a short-day plant that requires long nights to induce bloom formation, it might still fail to produce mature seeds before the onset of winter in areas at northern latitudes characterized by short summer nights. To survey the genetic variation in flowering time and study the effect of latitudinal origin on this trait, a reciprocal common garden experiment, including eleven populations of A. artemisiifolia from Europe and North America, was conducted. The experiment was conducted both outside the range limit of the species, in Sweden and within its invaded range, in Croatia. Our main hypothesis was that the photoperiodic-thermal requirements of A. artemisiifolia constitute a barrier for reproduction at northern latitudes and, thus, halts the northern range shift despite expected climate change. Results revealed the presence of a north-south gradient in flowering time at both garden sites, indicating that certain European populations are pre-adapted to photoperiodic and thermal conditions at latitudes up to, at least, 60° N. This was confirmed by phenological recordings performed in a region close to the northern range limit, the north of Germany. Thus, we conclude that there exists a high risk for establishment and spread of A. artemisiifolia in FennoScandinavia in the near future. The range shift might occur independently of climate change, but would be accelerated by it.

Degradation of sexual reproduction in Veronica filiformis after introduction to Europe.

BACKGROUND: Baker's law predicts that self-incompatible plant species are generally poor colonizers because their mating system requires a high diversity of genetically differentiated individuals and thus self-compatibility should develop after long-distance dispersal. However, cases like the introduction of the self-incompatible Veronica filiformis (Plantaginaceae) to Europe constitute an often overlooked alternative to this rule. This species was introduced from subalpine areas of the Pontic-Caucasian Mountains and colonized many parts of Central and Western Europe in the last century, apparently without producing seeds. To investigate the consequences of the absence of sexual reproduction in this obligate outcrosser since its introduction, AFLP fingerprints, flower morphology, pollen and ovule production and seed vitality were studied in introduced and native populations. RESULTS: Interpopulation crossings of 19 introduced German populations performed in the greenhouse demonstrated that introduced populations are often unable to reproduce sexually. These results were similar to intrapopulation crossings, but this depended on the populations used for crossings. Results from AFLP fingerprinting confirmed a lack of genetic diversity in the area of introduction, which is best explained by the dispersal of clones. Flower morphology revealed the frequent presence of mutations affecting the androecium of the flower and decreasing pollen production in introduced populations. The seeds produced in our experiments were smaller, had a lower germination rate and had lower viability than seeds from the native area. CONCLUSIONS: Taken together, our results demonstrate that V. filiformis was able to spread by vegetative means in the absence of sexual reproduction. This came at the cost of an accumulation of phenotypically observable mutations in reproductive characters, i.e. Muller's ratchet.