A map of climate change-driven natural selection in Arabidopsis thaliana

Abstract

Through the lens of evolution, climate change is an agent of natural selection that forces populations to change and adapt, or face extinction. Current assessments of the risk of biodiversity associated with climate change1, however, do not typically take into account the genetic makeup of populations and how natural selection impacts it2. We made use of the extensive genome information in Arabidopsis thaliana and measured how rainfall-manipulation affected the fitness of 517 natural lines grown in Spain and Germany. This allowed us to directly infer selection along the genome3. Natural selection was particularly strong in the hot-dry Spanish location, killing 63% of lines and significantly changing the frequency of ~5% of all genome-wide variants. A significant portion of this climate-driven natural selection over variants was predictable from signatures of local adaptation (R2=29-52%), as genetic variants found in geographic areas with climates more similar to the experimental sites were positively selected. Field-validated predictions across the species range indicated that Mediterranean and Western Siberian populations — at the edges of the species’ environmental limits — currently experience the strongest climate-driven selection. With more frequent droughts and rising temperatures in Europe4, we forecast an increase in directional natural selection moving northwards from the southern end, and putting many native A. thaliana populations at evolutionary risk.

Evolutionary and ecological functional genomics, from lab to the wild

“…Fortunately, it is now possible to capture the diversity of accessions, varieties, ecotypes, related species and plant interactors in genetic studies, thereby making EEFG comparative approaches and association studies to identify genetic components of traits and adaptations possible (Juenger et al ., ; Lai et al ., ; Fournier‐Level et al ., ; Brachi et al ., ; Gloss et al ., ; Mähler et al ., ; Exposito‐Alonso et al ., ; Nallu et al ., ; Wang et al ., ,,; von Wettberg et al ., ). Work on the model plant Arabidopsis (and other Brassicaceae species) in natural habitats, for example, has provided valuable insights into the role of natural selection on disease‐resistance genes, and on the metabolic fluxes in auxin and glucosinolate metabolism (Tian et al ., ; Prasad et al ., ; Olson‐Manning et al ., , ; Horton et al ., ; MacQueen and Bergelson, ).…”

The Genetic Basis of Plant Functional Traits and the Evolution of Plant-Environment Interactions

“…Despite these challenges, we foresee increasing conceptual synergy and convergence of methods between the fields of molecular genetics, physiology and development, and ecological genetics. Multiple studies have leveraged our rich understanding of Arabidopsis molecular genetics in field studies which assess the environmental dependence of traits such as flowering time and fitness (Agren et al 2013), and infer the history of natural selection acting on putatively functional variants (Fournier-Level et al 2011, Exposito-Alonso et al 2018 or the association between climate and variants (Hancock et al 2011, Lasky et al 2012, Lasky et al 2014. In some cases, specific genetic variants in genes of known function have been experimentally demonstrated to underlie loci identified in the field (e.g.…”

A rainfall-manipulation experiment with 517Arabidopsis thalianaaccessions

“…This experiment was designed to be of a sufficiently large scale to enable powerful genome-wide associa on analyses 14 and to maximize the replicability of species-wide pa erns, which increases with the diversity of genotypes included in an experiment 15 . This dataset will be invaluable for the study of natural selec on and adapta on in the context of global climate change at the gene c level 16 , building on the gene c catalog of the 1001 Genomes Project 13 and complemen ng the already published extensive set of traits measured in controlled growth chamber or greenhouse condi ons 17,18 .…”