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Adaptive significance of Non Genetic Inheritance

Periodic Reporting for period 2 - ANGI (Adaptive significance of Non Genetic Inheritance)

Reporting period: 2017-09-01 to 2019-02-28

Our ability to predict adaptation and the response of populations to selection is limited. Solving this issue is a fundamental challenge of evolutionary ecology with implications for applied sciences such as conservation, and agronomy. Non genetic inheritance (NGI; e.g. ecological niche transmission, epigenetic transmission) is suspected to play a foremost role in adaptive evolution but such hypothesis remains untested. Using quantitative genetics in wild plant populations, experimental evolution, and epigenetics, we will assess the role of NGI in the adaptive response to selection of plant populations. The ANGI project will follow the subsequent research program: (1) Using long-term survey data, we will measure natural selection in wild populations of Antirrhinum majus within its heterogeneous array of micro-habitats. We will calculate the fitness gain provided by multiple traits and stem elongation to plants growing in bushes where they compete for light. Stem elongation was shown to depend on epigenetic variation in several species. (2) Using a statistical approach that we developed, we will estimate the quantitative genetic and non genetic heritability of traits. (3) We will identify phenotypic changes caused by fitness that are based on genetic variation and NGI and assess their respective roles in adaptive evolution. (4) In controlled conditions, we will artificially select for increased stem elongation in clonal lineages, thereby excluding DNA variation. We will quantify the non genetic response to selection and test for a quantitative epigenetic signature of selection. (5) We will build on our results to generate an inclusive theory of genetic and non genetic natural selection. ANGI builds on a confirmed expertise in selection experiments, quantitative genetics and NGI. In addition, the availability of survey data provides a solid foundation for the achievement of this project. Our ambition is to evaluate whether original mechanisms (e.g. NGI) underlie adaptation that are an alternative to selection based on standing genetic variation.
Why will this project have a broad impact on life sciences?
This project will integrate new findings into an inclusive theory of natural selection.
Most [nearly all] research programs to date consider that environmental variation is either imposing a selective demand on organisms or interferes with the process of adaptive evolution. Genetic diversity is the key parameter used to study the evolution of species, predict their adaptive potential, manage genetic resources in agronomy, plan biological conservation strategies and communicate with a general audience on these topics. There is an emerging demand for clarifications by conservation agencies and crop and animal breeders in agronomy to clarify: “how to use the knowledge on the environmental background of populations to predict their response to selection and more generally their adaptive potential?”. There is also a demand by fundamental researchers: Theoreticians call for new concepts and empirical data providing quantitative estimates to parameterize models of adaptive dynamics. Evolutionary biologists investigating the paradoxical absence of genetic evolution in response to selection in natural populations are calling for empirical data on environmental effects shortcutting genetic selection. The ANGI project will participate to answer those demands. We will clarify the extent to which quantified environmentally induced phenotypic variation and epigenetic variability at the molecular level can be used to predict the evolutionary potential of natural populations and the response to artificial selection. Because the ANGI project is already positioned at the interface of proactive demands, we expect our results will be valorized immediately by their communication. It is important to note that public awareness and interest for these issues is increasing daily in the media and in science outreach programs conducted by museums a
During the first 36 months of the project:
We have conducted three exhaustive surveys (2016, 2017 and 2018) of the six natural populations occurring in the fragmented habitat of the abandoned saltmarsh between Peyriac de Mer and Bages in Southern France. During these surveys, we have characterized the phenotype and recorded the geographic coordinates of 11730 plants in natural populations. For all these plants, we have sampled leaves, extracted their DNA and amplified 25 microsatellite marker loci. For 9580 plants, we have scored their genotype in order to reconstruct the pedigree of the populations. We have taken photos to characterize their microenvironment. The environment of 9580 plants was characterized so far. We have also characterized the microhabitat of plants by mapping geographic patches were environmental conditions are more likely to be shared (e.g. open habitat on rocks, grassland). We have built a database that included this information. We are currently constructing the pedigree by genetically assigning parenthood. 3000 plants are included in the pedigree so far.
Experiments in controlled conditions allow us to expose plants to different treatments (different levels of shade exposure). A first experiment was conducted on natural populations, We have acquired seeds of snapdragon highly inbred lines and Arabidopsis thaliana Recombinant Inbred Lines (RILs). RILs are lineages for which the genome was fixed by generations of self-fertilization into an homozygous state. We plan to assess whether phenotypic plasticity is transmitted between generations on the basis of these lines. A sub-sample of plants from the same lineages will be used to explore the possible association between phenotypic plasticity and epigenetic variation (methylation patterns).
In terms of results linked to the study of natural populations (WP1-2-3), we have obtained preliminary results and are digging further into the underlying ecological and evolutionary mechanisms in order to prepare scientific publications. The following findings require to be confirmed by a thorough analysis based on the complete dataset and by using methods that are more costly in time to meet the assumptions of natural population data distributions. In natural populations, there is dispersal between populations and microhabitats. On the basis of preliminary results, we have found that dispersal distance may lead to observe a large proportion of short distance events that may take place between environments and microhabitats. We have published an article on gene flow between natural populations at the level of the species geographic distribution (http://dx.doi.org/10.1080/23818107.2017.1310056) that will be a useful reference for the study of gene flow at the local level of our six surveyed populations. We are currently preparing a manuscript on that specific topic (based on the pedigree reconstruction). We have also found that there was no reproductive versus vegetative growth trade-off but that in some particular environments, fitness related traits are associated with developmental aspects. We have started theoretical simulations and empirical analyses that suggest a reduction of the opportunity for natural selection caused by the actual demographic growth of the populations. We have also started to quantify natural selection pressures and are currently preparing a manuscript on this topic.
In terms of results linked to experimental approaches (WP4), we have obtained preliminary results on natural populations but it is important to note that experiments are still ongoing. So far, preliminary analyses show that stem elongation in response to shade is strong when plants were grown in a common garden experiment outside of the greenhouse (a manuscript is currently being prepared on this topic). In the greenhouse and in growth chambers, the magnitude of the stem elongation response is much smaller. However, we found so far a strong response of the specific leaf
At this stage of the project (36 months), most advances beyond the state of art are conceptual advances and theoretical predictions. These aspects have been addressed in conferences and published in peer reviewed articles in international journals. There is still a lot of debate animating the scientific community about the evolutionary significance of non genetic inheritance (e.g. ecological niche transmission and epigenetic transmission). A large part of the argument between pros and cons originates in the complexity surrounding a non equivocal separation of genetic and non genetic transgenerational variation. Evidence keeps accumulating that plasticity and epigenetic variation can be inherited, be it directly or through phenotypic reconstruction in similar environmental conditions. However, most experimental results are based on studies where genetic variation was excluded (e.g. by using one lineage of clones). Evidence for a direct role played by non genetic variation in evolution in nature where there is genetic variation is still scarce. We have developed methods to identify epigenetic mechanisms in experimental populations and separate genetic and non genetic causes of phenotypic variation in natural and experimental populations. So far, our conceptual progress supports the need to assess empirically the role of non genetic inheritance in adaptive evolution. Our extensive surveys of the scientific literature support the hypothesis that it has the potential to influence the outcome of evolution and that epigenetic variation may play a role in relaying environmental variation across generations and serve as standing variation upon which selection can act. It is important to note that these hypotheses remain to be tested empirically. We are currently running empirical research in order to test for these hypotheses and communicating on the fact that the absence of empirical evidence, as well as the existence of partial evidence are neither validating nor invalidating this hypothesis. This goes against several papers published in the scientific literature that argue one way or another without their conclusions being rooted on solid empirical evidence. It is crucial to test this hypothesis, be it confirmed or rejected, because a validation of this hypothesis would lead to considering a new source of environmentally induced opportunities for adaptive evolution. The focus of many studies in the actual context of global change is to assess the cost of changes in the environmental background of populations in terms of diversity loss. The ANGI project proposes an alternative perspective by investigating what are the potential effects of environmental modifications in terms of evolutionary potential. Our aim is to assess whether alternative sources of adaptive evolution can be identified in natural populations. Such knowledge would have implications for building original strategies in applied conservation based on the non genetic adaptive potential of populations. Most [nearly all] research programs to date consider that environmental variation is either imposing a selective demand on organisms or interferes with the process of adaptive evolution. Genetic diversity is the key parameter used to study the evolution of species, predict their adaptive potential, manage genetic resources in agronomy, plan biological conservation strategies and communicate with a general audience on those topics. There is an emerging demand for clarifications by conservation agencies and crop and animal breeders in agronomy to clarify how to use the knowledge on the environmental background of populations to predict their response to selection and more generally their adaptive potential. There is also a demand by fundamental researchers: Theoreticians call for new concepts and empirical data providing quantitative estimates to parameterize models of adaptive dynamics. Evolutionary biologists investigating the paradoxical absence of genetic change in res