The role of glycine betaine in range expansions; protecting mangroves against extreme freeze events

1. Due to a warming climate, mangrove populations within the Gulf of Mexico and along the Florida Atlantic coastline are expanding their range poleward. As mangroves expand their range limit, leading edge individuals are more likely to experience an increased incidence of freeze events. However, we still lack a clear understanding of the mechanisms used by mangroves to survive freezing conditions. 2. Here, we conducted common garden experiments at different locations experiencing variable winter freeze conditions to show glycine betaine, an organic osmolyte, increases significantly with freeze exposure, playing an important role in the freeze tolerance of Avicennia germinans, a widespread Neotropical mangrove. 3. We found glycine betaine accumulation was similar across all source populations and freeze exposure locations, suggesting glycine betaine is not a range limit adaptation and is instead used for freeze tolerance by A. germinans irrespective of source population. Plants sourced from populations that experience freezing conditions exhibited greater rates of survival, indicating range edge populations of A. germinans have other heritable adaptations in addition to glycine betaine for freeze tolerance. 4. Synthesis. Continued mangrove expansion poleward will result in a greater incidence of freeze events for individuals at the leading edge. Our findings suggest freeze tolerance in this species may be genetically based and that leading edge A. germinans have the potential to survive extreme freeze events and recover post-freeze, allowing for their continued expansion poleward. This process of selective survival may act to promote adaptation of freeze tolerance in range edge populations.

1. 受气候变暖影响，墨西哥湾及佛罗里达大西洋沿岸的红树林（mangrove）种群正逐步向极地拓展分布范围。随着红树林分布边界的扩张，分布前沿个体遭遇冻害事件的概率显著升高。但目前学界仍未明确红树林抵御冻害的具体机制。
2. 本研究在冬季冻害条件存在差异的多个地点开展同质园实验（common garden experiments），结果显示：有机渗透调节剂（organic osmolyte）甘氨酸甜菜碱（glycine betaine）的含量会随冻害暴露程度显著升高，这在广布新热带界红树林物种海榄雌（Avicennia germinans）的冻害耐受过程中发挥关键作用。
3. 研究发现，不同源种群以及不同冻害暴露地点的个体中，甘氨酸甜菜碱的积累模式均无显著差异，这表明甘氨酸甜菜碱并非用于适应分布边界的冻害压力，而是海榄雌通用的冻害耐受机制，与源种群来源无关。此外，源自曾经历冻害环境的种群的植株存活率更高，说明海榄雌的分布边缘种群除甘氨酸甜菜碱外，还存在其他可遗传的冻害耐受适应性特征。
4. 综合分析：红树林持续向极地拓展分布，将导致分布前沿个体遭遇冻害事件的频率进一步提升。本研究结果表明，该物种的冻害耐受能力具有遗传基础，且分布前沿的海榄雌个体具备在极端冻害事件中存活并在灾后恢复的潜力，这将助力其持续向极地拓展分布。这种选择性存活过程可能会推动分布边缘种群的冻害耐受适应性演化。