Plasticity to wind is modular and genetically variable in Arabidopsis thaliana

Thigmomorphogenesis, the characteristic phenotypic changes by which plants react to mechanical stress, is a widespread and probably adaptive type of phenotypic plasticity. However, little is known about its genetic basis and population variation. Here, we examine genetic variation for thigmomorphogenesis within and among natural populations of the model system Arabidopsis thaliana. Offspring from 17 field-collected European populations was subjected to three levels of mechanical stress exerted by wind. Overall, plants were remarkably tolerant to mechanical stress. Even high wind speed did not significantly alter the correlation structure among phenotypic traits. However, wind significantly affected plant growth and phenology, and there was genetic variation for some aspects of plasticity to wind among A. thaliana populations. Our most interesting finding was that phenotypic traits were organized into three distinct and to a large degree statistically independent covariance modules associated with plant size, phenology, and growth form, respectively. These phenotypic modules differed in their responsiveness to wind, in the degree of genetic variability for plasticity, and in the extent to which plasticity affected fitness. It is likely, therefore, that thigmomorphogenesis in this species evolves quasi-independently in different phenotypic module

Experimental alteration of DNA methylation affects the phenotypic plasticity of ecologically relevant traits in Arabidopsis thaliana

Heritable phenotypic variation in plants can be caused not only by underlying genetic differences, but also by variation in epigenetic modifications such as DNA methylation. However, we still know very little about how relevant such epigenetic variation is to the ecology and evolution of natural populations. We conducted a greenhouse experiment in which we treated a set of natural genotypes of Arabidopsis thaliana with the demethylating agent 5-azacytidine and examined the consequences of this treatment for plant traits and their phenotypic plasticity. Experimental demethylation strongly reduced the growth and fitness of plants and delayed their flowering, but the degree of this response varied significantly among genotypes. Differences in genotypes' responses to demethylation were only weakly related to their genetic relatedness, which is consistent with the idea that natural epigenetic variation is independent of genetic variation. Demethylation also altered patterns of phenotypic plasticity, as well as the amount of phenotypic variation observed among plant individuals and genotype means. We have demonstrated that epigenetic variation can have a dramatic impact on ecologically important plant traits and their variability, as well as on the fitness of plants and their ecological interactions. Epigenetic variation may thus be an overlooked factor in the evolutionary ecology of plant population

Epigenetic variation in plant responses to defence hormones

Background and Aims There is currently much speculation about the role of epigenetic variation as a determinant of heritable variation in ecologically important plant traits. However, we still know very little about the phenotypic consequences of epigenetic variation, in particular with regard to more complex traits related to biotic interactions. Methods Here, a test was carried out to determine whether variation in DNA methylation alone can cause heritable variation in plant growth responses to jasmonic acid and salicylic acid, two key hormones involved in induction of plant defences against herbivores and pathogens. In order to be able to ascribe phenotypic differences to epigenetic variation, the hormone responses were studied of epigenetic recombinant inbred lines (epiRILs) of Arabidopsis thaliana - lines that are highly variable at the level of DNA methylation but nearly identical at the level of DNA sequence. Key Results Significant heritable variation was found among epiRILs both in the means of phenotypic traits, including growth rate, and in the degree to which these responded to treatment with jasmonic acid and salicylic acid. Moreover, there was a positive epigenetic correlation between the responses of different epiRILs to the two hormones, suggesting that plant responses to herbivore and pathogen attack may have a similar molecular epigenetic basis. Conclusions This study demonstrates that epigenetic variation alone can cause heritable variation in, and thus potentially microevolution of, plant responses to defence hormones. This suggests that part of the variation of plant defences observed in natural populations may be due to underlying epigenetic, rather than entirely genetic, variatio

Phenotypic and genetic differentiation between native and introduced plant populations

Plant invasions often involve rapid evolutionary change. Founder effects, hybridization, and adaptation to novel environments cause genetic differentiation between native and introduced populations and may contribute to the success of invaders. An influential idea in this context has been the Evolution of Increased Competitive Ability (EICA) hypothesis. It proposes that after enemy release plants rapidly evolve to be less defended but more competitive, thereby increasing plant vigour in introduced populations. To detect evolutionary change in invaders, comparative studies of native versus introduced populations are needed. Here, we review the current empirical evidence from: (1) comparisons of phenotypic variation in natural populations; (2) comparisons of molecular variation with neutral genetic markers; (3) comparisons of quantitative genetic variation in a common environment; and (4) comparisons of phenotypic plasticity across different environments. Field data suggest that increased vigour and reduced herbivory are common in introduced plant populations. In molecular studies, the genetic diversity of introduced populations was not consistently different from that of native populations. Multiple introductions of invasive plants appear to be the rule rather than the exception. In tests of the EICA hypothesis in a common environment, several found increased growth or decreased resistance in introduced populations. However, few provided a full test of the EICA hypothesis by addressing growth and defence in the same species. Overall, there is reasonable empirical evidence to suggest that genetic differentiation through rapid evolutionary change is important in plant invasions. We discuss conceptual and methodological issues associated with cross-continental comparisons and make recommendations for future research. When testing for EICA, greater emphasis should be put on competitive ability and plant tolerance. Moreover, it is important to address evolutionary change in characteristics other than defence and growth that could play a role in plant invasion

Climate warming can reduce biocontrol efficacy and promote plant invasion due to both genetic and transient metabolomic changes.

Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences

Climate warming can reduce biocontrol efficacy and promote plant invasion due to both genetic and transient metabolomic changes

Climate change may affect plant-herbivore interactions and their associated ecosystem functions. In an experimental evolution approach, we subjected replicated populations of the invasive Ambrosia artemisiifolia to a combination of simulated warming and herbivory by a potential biocontrol beetle. We tracked genomic and metabolomic changes across generations in field populations and assessed plant offspring phenotypes in a common environment. Using an integrated Bayesian model, we show that increased offspring biomass in response to warming arose through changes in the genetic composition of populations. In contrast, increased resistance to herbivory arose through a shift in plant metabolomic profiles without genetic changes, most likely by transgenerational induction of defences. Importantly, while increased resistance was costly at ambient temperatures, warming removed this constraint and favoured both vigorous and better defended plants under biocontrol. Climate warming may thus decrease biocontrol efficiency and promote Ambrosia invasion, with potentially serious economic and health consequences

Transient Stability of Epigenetic Population Differentiation in a Clonal Invader

Epigenetic variation may play an important role in how plants cope with novel environments. While significant epigenetic differences among plants from contrasting habitats have often been observed in the field, the stability of these differences remains little understood. Here, we combined field monitoring with a multi-generation common garden approach to study the dynamics of DNA methylation variation in invasive Chinese populations of the clonal alligator weed (Alternanthera philoxeroides). Using AFLP and MSAP markers, we found little variation in DNA sequence but substantial epigenetic population differentiation. In the field, these differences remained stable across multiple years, whereas in a common environment they were maintained at first but then progressively eroded. However, some epigenetic differentiation remained even after 10 asexual generations. Our data indicate that epigenetic variation in alligator weed most likely results from a combination of environmental induction and spontaneous epimutation, and that much of it is neither rapidly reversible (phenotypic plasticity) nor long-term stable, but instead displays an intermediate level of stability. Such transient epigenetic stability could be a beneficial mechanism in novel and heterogeneous environments, particularly in a genetically impoverished invader

The scale of population structure in Arabidopsis thaliana

The population structure of an organism reflects its evolutionary history and influences its evolutionary trajectory. It constrains the combination of genetic diversity and reveals patterns of past gene flow. Understanding it is a prerequisite for detecting genomic regions under selection, predicting the effect of population disturbances, or modeling gene flow. This paper examines the detailed global population structure of Arabidopsis thaliana. Using a set of 5,707 plants collected from around the globe and genotyped at 149 SNPs, we show that while A. thaliana as a species self-fertilizes 97% of the time, there is considerable variation among local groups. This level of outcrossing greatly limits observed heterozygosity but is sufficient to generate considerable local haplotypic diversity. We also find that in its native Eurasian range A. thaliana exhibits continuous isolation by distance at every geographic scale without natural breaks corresponding to classical notions of populations. By contrast, in North America, where it exists as an exotic species, A. thaliana exhibits little or no population structure at a continental scale but local isolation by distance that extends hundreds of km. This suggests a pattern for the development of isolation by distance that can establish itself shortly after an organism fills a new habitat range. It also raises questions about the general applicability of many standard population genetics models. Any model based on discrete clusters of interchangeable individuals will be an uneasy fit to organisms like A. thaliana which exhibit continuous isolation by distance on many scales

Citizen Science Reveals Unexpected Continental-Scale Evolutionary Change in a Model Organism

Organisms provide some of the most sensitive indicators of climate change and evolutionary responses are becoming apparent in species with short generation times. Large datasets on genetic polymorphism that can provide an historical benchmark against which to test for recent evolutionary responses are very rare, but an exception is found in the brown-lipped banded snail (Cepaea nemoralis). This species is sensitive to its thermal environment and exhibits several polymorphisms of shell colour and banding pattern affecting shell albedo in the majority of populations within its native range in Europe. We tested for evolutionary changes in shell albedo that might have been driven by the warming of the climate in Europe over the last half century by compiling an historical dataset for 6,515 native populations of C. nemoralis and comparing this with new data on nearly 3,000 populations. The new data were sampled mainly in 2009 through the Evolution MegaLab, a citizen science project that engaged thousands of volunteers in 15 countries throughout Europe in the biggest such exercise ever undertaken. A known geographic cline in the frequency of the colour phenotype with the highest albedo (yellow) was shown to have persisted and a difference in colour frequency between woodland and more open habitats was confirmed, but there was no general increase in the frequency of yellow shells. This may have been because snails adapted to a warming climate through behavioural thermoregulation. By contrast, we detected an unexpected decrease in the frequency of Unbanded shells and an increase in the Mid-banded morph. Neither of these evolutionary changes appears to be a direct response to climate change, indicating that the influence of other selective agents, possibly related to changing predation pressure and habitat change with effects on micro-climate