Leaf economics and slow-fast adaptation across the geographic range of Arabidopsis thaliana

International audience; Life history strategies of most organisms are constrained by resource allocation patterns that follow a 'slow-fast continuum'. It opposes slow growing and long-lived organisms with late investment in reproduction to those that grow faster, have earlier and larger reproductive effort and a short longevity. In plants, the Leaf Economics Spectrum (LES) depicts a leaf-level trade-off between the rate of carbon assimilation and leaf lifespan, as stressed in functional ecology from interspecific comparative studies. However, it is still unclear how the LES is connected to the slow-fast syndrome. Interspecific comparisons also impede a deep exploration of the linkage between Les variation and adaptation to climate. Here, we measured growth, morpho-physiological and life-history traits, at both the leaf and whole-plant levels, in 378 natural accessions of Arabidopsis thaliana. We found that the Les is tightly linked to variation in whole-plant functioning, and aligns with the slow-fast continuum. A genetic analysis further suggested that phenotypic differentiation results from the selection of different slow-fast strategies in contrasted climates. slow growing and long-lived plants were preferentially found in cold and arid habitats while fast growing and short-lived ones in more favorable habitats. Our findings shed light on the role of the slow-fast continuum for plant adaptation to climate. More broadly, they encourage future studies to bridge functional ecology, genetics and evolutionary biology to improve our understanding of plant adaptation to environmental changes. Investigations of the genetic and phenotypic differentiation of plant lineages along environmental gradients is crucial for the understanding of plant evolutionary responses to current and future climate variations. As plants cannot simultaneously optimize competing eco-physiological functions, an important question is how plant adaptation occurs under the influence of major trade-offs between traits. The slow-fast continuum is a pervasive trade-off between resource allocation to growth, reproduction and survival , spread across the tree of life 1. The slow end of this continuum is characterized by slow growing, long-lived species and low reproductive output, while species at the fast end reach reproductive maturity faster and produce more offsprings. In plants, the leaf economics spectrum (LES hereafter) 2-4 is thought to reflect the physiological basis of the slow-fast continuum 4. The LES arrays plant species along a continuum of leaf trait syndromes going from short-lived leaves with fast metabolism to the reverse syndrome 3. Core LES traits include leaf dry mass per area (LMA), leaf lifespan (LLS) and net photosynthetic rate per mass unit (A mass) 3,5-7. LES traits are widely used in comparative ecology to infer whole-plant ecological strategies 4,8-12. However, the extent to which leaf-level resource economics reflects whole-plant physiology, performance, and ultimately fitness, is still under debate 13. Many processes can lead to a mismatch between LES and whole-plant functioning 14 , including the impact of self-shading among leaves and resource allocation patterns, such as carbon investment in non-photosynthetic tissues 15,16. To gain insights into the robustness of the slow-fast continuum at different organizational levels, we need