Long-term dynamics of adaptive evolution in a globally important coccolithophore to ocean acidification

Recent evolution experiments have revealed that marine phytoplankton may adapt to global change, for example to ocean warming or acidification. Long-term adaptation to novel environments is a dynamic process and phenotypic change can take place thousands of generations after exposure to novel conditions. Using the longest evolution experiment performed in any marine species to date (4 yrs, = 2100 generations), we show that in the coccolithophore Emiliania huxleyi, long-term adaptation to ocean acidification is complex and initial phenotypic responses may revert for important traits. While fitness increased continuously, calcification was restored within the first 500 generations but later reduced in response to selection, enhancing physiological declines of calcification in response to ocean acidification. Interestingly, calcification was not constitutively reduced but revealed rates similar to control treatments when transferred back to present-day CO2 conditions. Growth rate increased with time in controls and adaptation treatments, although the effect size of adaptation assessed through reciprocal assay experiments varied. Several trait changes were associated with selection for higher cell division rates under laboratory conditions, such as reduced cell size and lower particulate organic carbon content per cell. Our results show that phytoplankton may evolve phenotypic plasticity that can affect biogeochemically important traits, such as calcification, in an unforeseen way under future ocean conditions.近期的演化实验表明，海洋浮游植物可适应全球环境变化，例如海洋变暖与海洋酸化。对新环境的长期适应性演化是一个动态过程，表型变化可能在暴露于新环境条件数千代后才会显现。依托目前已开展的最长海洋物种演化实验（历时4年，共计2100个世代），我们的研究显示，在赫氏颗石藻（Emiliania huxleyi）中，对海洋酸化的长期适应性演化过程十分复杂，部分重要性状的初始表型响应甚至可能出现逆转。尽管适合度（fitness）持续提升，但钙化作用（calcification）在最初的500个世代内得以恢复，后续却因选择压力出现下降，加剧了海洋酸化诱导的钙化生理衰退。值得注意的是，钙化作用并非固有降低，当被转移至当前二氧化碳浓度的环境条件时，其速率与对照组相近。对照组与适应性处理组的生长速率均随时间推移而提升，但通过互反测定实验评估的适应性效应量存在差异。实验室条件下，多项性状变化与选择压力下更高的细胞分裂速率相关，例如细胞体积减小、单位细胞颗粒有机碳（particulate organic carbon）含量降低。我们的研究结果表明，浮游植物可演化出表型可塑性（phenotypic plasticity），在未来海洋环境中，这种可塑性可能以未被预见的方式影响诸如钙化作用这类具有重要生物地球化学意义的性状。