Evolutionary responses of plants to environmental changes through the lens of ecological theories: an experimental test using the model species Arabidopsis thaliana – AraBreed

Understanding the ability of plants to adapt to new, potentially harmful, environments is important for monitoring and managing wild and cultivated biodiversity in a changing world. Local adaptation is a pivotal mechanism to explain the maintenance of genetic diversity in natural populations. In the absence of other forces, local adaptation should result in a fitness advantage in the local habitat of adapted populations compared to alternative environments. However, adaptation can be hampered by the lack of genetic variance of underlying traits due to a variety of constraints. For instance, ecological theory states that plants cannot simultaneously be efficient at certain tasks, such as acquiring and conserving resources, or be both competitive and stress tolerant. Resulting trade-offs are described in ecology as major constraints on the diversification of life forms and functions, but the general applicability of these constraints remains to be elucidated.
Studying adaptation in natural populations is complex. Experimental evolution provides a formidable opportunity to examine adaptive processes, rate and strength of selection in real time, as well as to test the validity of prominent ecological hypotheses. The AraBreed project will assess the evolution of major ecological trade-offs and the underlying allelic composition of plant populations, in response to controlled selection pressures. Experimental evolution will be monitored over three generations in four contrasting environments (mesocosms) varying in resource (nutrient and water) availability and disturbance (herbivory). Importantly, AraBreed will benefit from extensive genetic material previously generated on the model species Arabidopsis thaliana. We will use 350 F2 populations (500,000 genotypes in total) previously generated from random crosses (F1 hybrids = parents) between 400 fully sequenced natural accessions collected across Eurasia and fully sequenced (F0s = inbred grand-parents, 1001genomes.org/). This has the main advantages of (i) recreating phenotypes thought to be purged in natural populations, and (ii) giving access to the genetic and phenotypic diversity in both ancestral and adapted populations. Plants under different selection regimes will be phenotyped in situ for six focal traits with the use of Near Infra-Red Spectrometry, a fast and non-destructive method for the quantification of ecophysiological traits. In addition, seeds will be collected for further analysis in controlled conditions (ex situ phenotyping in the PHENOPSIS automaton, and stress experiments in dedicated facilities), and next-generation sequencing (pool-seq).
Experimental evolution on a short-lived model species grown in controlled mesocosms provides a powerful tool to examine the extent of intraspecific variability, the role of constraints and selection in shaping pervasive ecological trade-offs, as well as to identify potential limits for selection. AraBreed offers the opportunity to develop new approaches for the study of evolution in science education through the teaching missions defined in the framework of the project. Moreover, understanding the drivers underpinning ecological trade-offs could also help guide selection methods to optimize crop attributes. The project - at the crossroads of ecology, evolutionary biology and genomics - is multifaceted and highly transdisciplinary. AraBreed therefore carries large potential to advance both fundamental and applied life sciences.