Abstract
Diatoms contribute roughly 20% of global primary production, but the factors determining their ability to adapt to global warming are unknown. Here we quantify the capacity for adaptation to warming in the marine diatom Thalassiosira pseudonana. We find that evolutionary rescue under severe (32 °C) warming is slow, but adaptation to more realistic scenarios where temperature increases are moderate (26 °C) or fluctuate between benign and severe conditions is rapid and linked to phenotypic changes in metabolic traits and elemental composition. Whole-genome re-sequencing identifies genetic divergence among populations selected in the different warming regimes and between the evolved and ancestral lineages. Consistent with the phenotypic changes, the most rapidly evolving genes are associated with transcriptional regulation, cellular responses to oxidative stress and redox homeostasis. These results demonstrate that the evolution of thermal tolerance in marine diatoms can be rapid, particularly in fluctuating environments, and is underpinned by major genomic and phenotypic change.
Highlights
Earth system models predict that global warming will result in significant declines in net primary production by marine phytoplankton throughout the 21st century[1,2] driven by rising temperatures exceeding limits of thermal tolerance and increases in grazing and nutrient limitation in warmer, more stratified oceans[3,4,5]
Consistent with our hypothesis, lineages selected under the fluctuating regime maintained substantially larger population sizes relative to those experiencing severe warming (Supplementary Figure 2 and Supplementary Tables 1 and 3), suggesting that temporary restoration of benign conditions increased the probability of fixing beneficial mutations required for adaptation to the severe (32 °C) environment via a positive demographic effect
We found that evolutionary rescue under severe warming was slow (>1 year), but adaptation to more realistic warming scenarios, where temperature increases were moderate or where they fluctuated between benign and severe conditions, was rapid
Summary
Earth system models predict that global warming will result in significant declines in net primary production by marine phytoplankton throughout the 21st century (up to 20%)[1,2] driven by rising temperatures exceeding limits of thermal tolerance and increases in grazing and nutrient limitation in warmer, more stratified oceans[3,4,5]. Do not consider the potential for marine phytoplankton to rapidly adapt to environmental changes associated with global warming[6,7,8] Such shortcomings have unknown consequences for projected changes in global ocean primary production and arise because the mechanisms that facilitate or constrain the capacity for rapid adaptation to warming in marine phytoplankton are largely unknown. We address this fundamental knowledge gap by carrying out a 300-generation selection experiment, with the model marine diatom Thalassiosira pseudonana, to assess the potential for, and mechanisms that might facilitate rapid adaptation to warming in this globally important phytoplankton[9,10,11]. We found that adaption to warming was linked to major phenotypic changes in metabolic traits and elemental composition and consistent with these phenotypic changes, the most rapidly evolving genes were associated with transcriptional regulation, cellular responses to oxidative stress, and redox homeostasis
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