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 the 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.
Highlights
Vast spatiotemporal variation across natural environments subjects all organisms to abiotic stressors (Gienapp et al 2008)
The genus 62 Cochlearia comprises 16 accepted species and 4 subspecies (Kiefer et al 2014, Supplementary File 1). 63 64 While on species-level it has been shown in Arabidopsis thaliana that drought- and temperature65 adaptive genetic variants are shared among Mediterranean and Nordic regions (Exposito-Alonso et al 2018), the separation of Cochlearia from Ionopsidium is much deeper, dating to the mid-Miocene (Koch 2012)
Our phylogenetic and cytogenetic analysis uncovers a recurrent boosting of speciation by glaciation cycles in this cytotypically very diverse genus and indicates that, despite clear challenges brought by global warming, the genus survives evolutionarily while, we speculate, rescuing its species diversity with reticulate and polyploid evolution. 94 95 Results Cytogenetic analyses show geographic structuring and parallel evolutionary trends towards shrinking haploid genomes in higher polyploids In order to first resolve its cytogenetic evolution, we generated a comprehensive survey of 575 99 georeferenced chromosome counts and/or genome sizes across the Cochlearia genus (Supplementary File 2) based on our novel cytogenetic data (Supplementary File 3) and a review of published literature over the last century (Supplementary File 4)
Summary
Vast spatiotemporal variation across natural environments subjects all organisms to abiotic stressors (Gienapp et al 2008). 94 95 Results Cytogenetic analyses show geographic structuring and parallel evolutionary trends towards shrinking haploid genomes in higher polyploids In order to first resolve its cytogenetic evolution, we generated a comprehensive survey of 575 99 georeferenced chromosome counts and/or genome sizes across the Cochlearia genus (Supplementary File 2) based on our novel cytogenetic data (Supplementary File 3) and a review of published literature over the last century (Supplementary File 4) This survey revealed a clear continental-scale geographical partitioning of diploid cytotypes (2n=12 and 2n=14; Figure 1a). In order to further investigate the cytogenetic dynamics within Cochlearia, we analyzed the relationships of 1) chromosome number vs genome size and 2) chromosome number vs DNA content per chromosome via rank correlation tests (Supplementary File 5) and, if normality of data was given, via linear regression analyses (Figure 1d, Appendix 1-figure 3). Discriminating between the four gene flow models was ambiguous
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