Supplementary material on within- and trans-generational responses to combined global changes in two congeneric species of marine annelids

The extent of species' geographical distribution can help us define their sensitivity to environmental challenges. Rare species are expected to have narrower tolerance windows and reduced plasticity compared to their common relatives. Assessing rare species' tolerance and plasticity under environmental changes will thus help predicting future changes in the structure and functions of ecosystems. We examined the level of tolerance and transgenerational responses of life-history and physiological traits in a rare (Ophryotrocha robusta) and common (Ophryptrocha japonica) marine polychaete species exposed over two generations to ocean acidification (OA: pH -0.5) and warming (OW: + 4 °C) in isolation and combined (OAW: + 4 °C, pH -0.5). Life history traits (growth, fecundity and eggs volume) were measured on a four months period, after which metabolomics profiles were analysed to highlight molecular pattern (energetic metabolism) linked to life history traits' changes. In the rare species, warming scenarios (OW and OAW) led to a decrease in energy production together with an increase in energy requirements, which were shortly lethal before viable offspring could be produced at the first generation. Under OA conditions, the rare species was able to reach the second generation, despite showing lower survival and reproductive performance when compared to control conditions. This was accompanied by a marked increase in fecundity and eggs volume in F2 females, suggesting higher capacity for transgenerational plasticity. Differently, the common species thrived under all scenarios across both generations, by maintaining fitness levels via adjusting its metabolic profile. Overall, whilst the rare species shows greater capacity to plastically adjust its life history responses after two generations under OA, it is not able to cope with future warming conditions due to lower tolerance to heat. If our results are to apply more broadly, given that rare species are most represented across taxa, and possess key ecological roles, our results support the idea that global changes will lead to an important loss in both specific and functional diversity in marine ecosystems.

物种的地理分布范围可用于界定其对环境胁迫的敏感性。相较于广布近缘物种，稀有种通常具备更窄的耐受阈值范围与更低的表型可塑性。因此，探究稀有种在环境变化下的耐受能力与可塑性，有助于预测生态系统结构与功能的未来演变趋势。本研究以两种海洋多毛类物种为研究对象：稀有种（Ophryotrocha robusta）与广布种（Ophryptrocha japonica），将其历经两代暴露于四种实验处理：单独海洋酸化（ocean acidification, OA：pH降低0.5）、单独增温（warming, OW：温度升高4℃）以及复合胁迫（OAW：温度升高4℃且pH降低0.5），检测其生活史性状与生理性状的耐受水平及跨代响应。研究周期为四个月，期间测定生活史性状（生长、繁殖力与卵体积），随后通过代谢组学（metabolomics）分析，解析与生活史性状变化相关的分子模式（能量代谢）。对于稀有种，单独增温与复合胁迫处理下，其能量生成减少且能量需求升高，在第一代可产生存活子代前便快速引发个体死亡。在海洋酸化胁迫条件下，稀有种虽存活率与繁殖表现较对照组有所下降，但可顺利繁育至第二代；且F2代雌性个体的繁殖力与卵体积显著提升，提示其具备更强的跨代可塑性能力。与之形成鲜明对比的是，广布种在两代实验的所有处理组中均生长良好，通过调控代谢谱维持适合度水平。总体而言，尽管稀有种在海洋酸化胁迫下历经两代后，其生活史响应的可塑性调节能力有所提升，但由于对高温的耐受性较低，无法应对未来的增温环境。考虑到在各类生物类群中，稀有种占据多数且发挥着关键的生态功能，若本研究结果具备普适性，则支持"全球变化将导致海洋生态系统物种多样性与功能多样性显著丧失"这一观点。