Evolutionary footprints of a cold relic in a rapidly warming world

Abstract

With accelerating global warming, understanding the evolutionary dynamics of plant adaptation to environmental change is increasingly urgent. Here we reveal the enigmatic history of the genus Cochlearia (Brassicaceae), a Pleistocene relic that originated from a drought-adapted Mediterranean sister genus during the Miocene. Cochlearia rapidly diversified and adapted to circum-Arctic regions and other cold-characterized habitat types during the Pleistocene. This sudden change in ecological preferences was accompanied by a highly complex, reticulate polyploid evolution, which was apparently triggered by the impact of repeated Pleistocene glaciation cycles. Our results illustrate that two early diversified arctic-alpine diploid gene pools contributed differently to the evolution of this young polyploid genus now captured in a cold-adapted niche. Metabolomics revealed central carbon metabolism responses to cold in diverse species and ecotypes, likely due to continuous connections to cold habitats that may have facilitated widespread adaptation to alpine and subalpine habitats, and which we speculate were coopted from existing drought adaptations. Given the growing scientific interest in adaptive evolution of temperature-related traits, our results provide much-needed taxonomic and phylogenomic resolution of a model system as well as first insights into the origins of its adaptation to cold.

Evolutionary footprints of cold adaptation in arctic-alpine Cochlearia (Brassicaceae) – evidence from freezing experiments and electrolyte leakage

“…danica were considered as a separate cluster 4, which shows closest affinities with Mediterranean Ionopsidium representing cluster 5 also defined exclusively by monocarpic taxa. These results are consistent with the findings of Wolf et al (2021), who identified the same groups based on nine of the 19 bioclimatic variables. These results show that Cochlearia and Ionopsidium accessions are exposed to varying environmental conditions, which is expected considering their geographically distant distribution.Ionopsidium accessions can be aggregated into a single group, suggesting that they inhabit regions with similar precipitation rates and temperatures.…”

“…Information on chromosome number and ploidy level is provided in Suppl. Material Table 1 (Koch et al, 1996;Koch et al, 1998;Koch et al, 1999;Koch, 2002;Koch et al, 2003;Koch & Bernhardt, 2004;Cieslak et al, 2007;Koch, 2012;Wolf et al, 2021).…”

“…It represents a promising system to study cold adaptation, as it shows distinctive traits that have evolved over a short time span. These traits include adaptations to extreme bedrock types, heavy metal soils, salt habitats, and high alpine and Arctic regions (Wolf et al, 2021). The tribe includes two genera, Cochlearia and Ionopsidium , which were separated by a deep evolutionary split during the mid-Miocene, approximately 13.8 million years ago (Koch, 2012).…”

“…The tribe includes two genera, Cochlearia and Ionopsidium , which were separated by a deep evolutionary split during the mid-Miocene, approximately 13.8 million years ago (Koch, 2012). Where-asIonopsidium species adapted to western Mediterranean bioclimatic conditions, progenitors of present-day Cochlearia expanded their distribution range to the northern hemisphere and rapidly diversified during the Pleistocene to ecological conditions in central and northern Europe and the circumarctic (Koch, 2012;Wolf et al, 2021). Even though these taxa are closely related, they have colonized substantially different ecological niches, such as salt marshes, sand dunes, coastal areas, cold and calcareous springs, and high alpine and arctic environments.…”

“…We previously demonstrated that both Cochlearia andIonopsidium show a strong but very similar cold metabolome response to cold treatment (Wolf et al, 2021). We hypothesized that adaptations to drought (Mediterranean habitats), salinity (coastal line habitats), and cold (arctic-alpine environments, cold spring water) may be achieved via the same primary response in herbaceous (non-woody) plants, thus posing the question of an evolutionary shared molecular-physiological trait among Ionopsidium andCochlearia .…”