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Adaptive significance of Non Genetic Inheritance

Periodic Reporting for period 4 - ANGI (Adaptive significance of Non Genetic Inheritance)

Reporting period: 2020-09-01 to 2022-02-28

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, selection experiments, and epigenetics, we assessed the potential role of NGI in the adaptive response to selection of plant populations. The ANGI project followed the subsequent research program: (1) Using long-term survey data, we measured natural selection in wild populations of snapdragon plants within their heterogeneous array of micro-habitats. (2) Using a statistical approach that we developed, we estimated the quantitative genetic and nongenetic variation of traits. (3) We identified potential 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 assessed mechanisms underlying selection. (5) We built on our results to improve the theory on genetic and non genetic natural selection
Why will this project has a broad impact on life sciences? This project participates to integrate new findings into an inclusive theory of natural selection. 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 about the role of transgenerational environmental effects on the response to selection and more generally on the associated adaptive potential. There is also a demand by fundamental researchers to account for these effects in quantitative estimates and parameterize models of adaptive dynamics. Evolutionary biologists investigating the paradoxical absence of genetic evolution in response to selection in natural populations are also calling for empirical data on environmental effects shortcutting genetic selection. The ANGI project participated to answer those demands.
During the first 72 months of the project:
We have conducted six exhaustive surveys (2016-2021) of the six natural populations occurring in the fragmented habitat of the abandoned saltmarsh between Peyriac de Mer and Bages in Southern France and characterized >18000 plants in natural populations (phenotype, geographic coordinates, 25 genetic [microsatellite] marker genotypes, microenvironment on the basis of photos). We have mapped the geographic patches were environmental conditions are more likely to be shared (e.g. open habitat on rocks, grassland). We have constructed the pedigree by genetically assigning parenthood to reach >5000 plants included in a highly reliable pedigree.
Experiments in controlled conditions allowed us to expose plants to different treatments (different levels of shade exposure and climate conditions). Experiments conducted in natural conditions were used to identify traits that might be involved with snapdragon plant adaptive evolution. Other experiments conducted in more controlled conditions (greenhouse and growth chambers) were conducted to test for an epigenetic basis of trait variation, with a focus on the developmental response to shade of snapdragon plants. We used Antirrhinum majus highly inbred lines and Arabidopsis thaliana Recombinant Inbred Lines, where the genome was fixed by generations of self-fertilization into a homozygous state, to investigate fundamental ecological and evolutionary mechanisms related to epigenetic trait variation.
Our results on natural populations (WP1-2-3) were published in several peer-reviewed articles in international journals (e.g. Evolution, Open Research europe) and presented in international conferences (e.g. ESEB) and local seminars (e.g. Vienna, Montpellier). They imply low connectivity between fragmented populations, fluctuating selection at an extremely small spatial-scale, and low genetic heritability for fitness related traits.
Our experimental results (WP4) were also published in several peer-reviewed articles in international journals (e.g. Molecular Ecology) and presented in international conferences and local seminars. They imply that snapdragon plants exhibit strong phenotypic plasticity in response to shade (SLA, stem elongation in response to shade, etc.) that are associated with some epigenetic changes in methylation patterns.
In terms of theoretical and conceptual developments (WP5). We have developed and published a methodological guide and review articles (e.g. Trends in Ecology & Evolution) on how and why the potential role of epigenetic and genetic variation in the response to selection should be studied simultaneously and what are the potential implications for agronomic sciences.
At the end of this project, advances beyond the state of art on the role of non genetic inheritance in adaptation were provided by the conceptual and methodological frameworks that we built, which rationale was supported by our empirical results obtained in wild populations and experiments. 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). We participated to the current accumulation of evidence that plasticity and epigenetic variation can be inherited. We took into account the limits of current approaches that exclude genetic variation, which is not reflecting the reality of natural populations, or may confound nongenetic and genetic population differentiation. We have developed and published methods to quantify the effect of ecological and epigenetic transgenerational variation in experimental and wild populations. We have synthesized the current knowledge on the potential role that non genetic inheritance could play in the adaptive evolution of wild populations, with a focus on epigenetic variation because it is at the center of the current debate. This advances are supported by the empirical assessments conducted in this project through experiments in controlled conditions and wild population studies. The findings of this project can be seen as proof of concept evidence for the role of nongenetic (and in particular epigenetic) inheritance in adaptation. The door is now open for accumulating empirical background knowledge, which will be necessary to reach a general consensus on this mechanisms and their adaptive significance. Such knowledge would have implications for building original strategies in applied conservation based on the nongenetic adaptive potential of populations. We expect our results will raise public awareness and interest for these issues.
snapdragon plant