Rapid shifts in thermal reaction norms and tolerance of brooded coral larvae following parental heat acclimation 亲代热适应后育雏珊瑚幼虫热反应规范和耐受性的快速变化
Lei Jiang | Cheng-Yue Liu | Guoxin Cui | Lin-Tao Huang | Lei Jiang | Cheng-Yue Liu | Guoxin Cui | Lin-Tao Huang |Xiao-Lei Yu | You-Fang Sun | Hao-Ya Tong | Guo-Wei Zhou | Xiao-Lei Yu | You-Fang Sun | Hao-Ya Tong | Guo-Wei Zhou |Xiang-Cheng Yuan | Yi-Si Hu | Wen-Liang Zhou Manuel Aranda | Xiang-Cheng Yuan | Yii-Si Hu | Wen-Liang Zhou Manuel Aranda |Pei-Yuan Qian | Hui Huang Pei-Yuan Qian | Hui Huang CAS Key Laboratory of Tropical Marine Bio-resources and Ecology, Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute 中科院热带海洋生物资源与生态重点实验室、广东省海洋生物应用重点实验室、南海研究院of Oceanology (SCSIO), Chinese Academy of Sciences, Guangzhou, China 中国科学院海洋研究所（SCSIO），中国广州 Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China 南方海洋科学与工程广东实验室（广州），中国广州 Department of Ocean Science and Hong Kong Branch (HKB) of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong 香港大学海洋科学系和南方海洋科学与工程广东实验室（广州）香港分部（HKB）。Kong University of Science and Technology (HKUST), Hong Kong, China 中国香港，香港科技大学（HKUST） Biological and Environmental Sciences and Engineering Division, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi 沙特图瓦勒，阿卜杜拉国王科技大学，红海研究中心，生物和环境科学与工程部Arabia 阿拉伯 CAS-HKUST Sanya Joint Laboratory of Marine Science Research, Key Laboratory of Tropical Marine Biotechnology of Hainan Province, Sanya Institute of 中科院-哈工大三亚海洋科学研究联合实验室、海南省热带海洋生物技术重点实验室、三亚学院Ocean Eco-Environmental Engineering, SCSIO, Sanya, China 海洋生态环境工程，中国三亚，南船重工 Sanya National Marine Ecosystem Research Station, Tropical Marine Biological Research Station in Hainan, Chinese Academy of Sciences, Sanya, China 中国科学院海南热带海洋生物研究站三亚国家海洋生态系统研究站，中国三亚 University of Chinese Academy of Sciences, Beijing, China 中国科学院大学，中国北京
Correspondence 通信
Manuel Aranda, Biological and 曼努埃尔-阿兰达，生物和
Environmental Sciences and Engineering Division, Red Sea Research Center, King Abdullah University of Science and Technology, Thuwal, Saudi Arabia. Email: manuel.aranda@kaust.edu.sa 沙特阿拉伯图瓦勒，阿卜杜拉国王科技大学红海研究中心环境科学与工程部。电子邮件：manuel.aranda@kaust.edu.sa
Pei-Yuan Qian, Department of Ocean Science and Hong Kong Branch (HKB) of the Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), The Hong Kong University of Science and Technology (HKUST), Hong Kong, China. 钱培元，中国香港，香港科技大学海洋科学系和南方海洋科学与工程广东实验室（广州）香港分部。
Hui Huang, CAS Key Laboratory of Tropical Marine Bio-resources and Ecology; Guangdong Provincial Key Laboratory of Applied Marine Biology, South China Sea Institute of Oceanology (SCSIO), Chinese Academy of Sciences, Guangzhou 510301, China. 黄晖，中科院热带海洋生物资源与生态重点实验室；中国科学院南海海洋研究所广东省应用海洋生物学重点实验室，中国广州 510301。
National Key Research and Development Program, Grant/Award Number: 2021 YFF0502804 and 2021YFC3100504; 国家重点研发计划，资助/奖励编号：2021 YFF0502804 和 2021YFC3100504；
Abstract 摘要
Thermal priming of reef corals can enhance their heat tolerance; however, the legacy effects of heat stress during parental brooding on larval resilience remain understudied. This study investigated whether preconditioning adult coral Pocillopora damicornis to high temperatures and could better prepare their larvae for heat stress. Results showed that heat-acclimated adults brooded larvae with reduced symbiont density and shifted thermal performance curves. Reciprocal transplant experiments demonstrated higher bleaching resistance and better photosynthetic and autotrophic performance in heat-exposed larvae from acclimated adults compared to unacclimated adults. RNA-seq revealed strong cellular stress responses in larvae from heat-acclimated adults that could have been effective in rescuing host cells from stress, as evidenced by the widespread upregulation of genes involved in cell cycle and mitosis. For symbionts, a molecular coordination between light harvesting, photoprotection and carbon fixation was detected in larvae from heat-acclimated adults, which may help optimize photosynthetic activity and yield under high temperature. Furthermore, heat acclimation led to opposing regulations of symbiont catabolic and anabolic pathways and favoured nutrient translocation to the host and thus a functional symbiosis. Notwithstanding, the improved heat tolerance was paralleled by reduced light-enhanced dark respiration, indicating metabolic depression for energy 珊瑚礁珊瑚的热预处理可以提高它们的耐热性；然而，亲代育雏期间的热应力对幼体恢复能力的遗留影响仍未得到充分研究。本研究调查了将大疣梭子蟹成体置于高温环境中 和 是否能使其幼体更好地适应热应激。结果表明，热适应成体繁殖的幼虫共生体密度降低，热性能曲线发生变化。对等移植实验表明，与未适应热应激的成虫相比，适应热应激的成虫的抗漂白能力更强，光合作用和自养性能更好。RNA-seq发现，来自热适应成虫的幼虫具有强烈的细胞应激反应，这可能有效地将宿主细胞从应激中解救出来，细胞周期和有丝分裂相关基因的广泛上调就是证明。就共生体而言，在来自热螯合成虫的幼虫体内检测到了采光、光保护和碳固定之间的分子协调，这可能有助于优化高温条件下的光合作用和产量。此外，热适应导致共生体分解代谢和合成代谢途径的相反调节，有利于营养物质向宿主转移，从而实现功能性共生。尽管如此，在耐热性提高的同时，光照增强的暗呼吸也减少了，这表明能量代谢受到抑制
Lei Jiang and Cheng-Yue Liu contributed equally to this work. 蒋磊和刘成跃对本研究做出了同样的贡献。
National Natural Science Foundation of China, Grant/Award Number: 42106115 and 41906097; Science and Technology Planning Project of Guangdong Province, China, Grant/Award Number: 2020B212060058 国家自然科学基金，批准/授予号：42106115 和 41906097；广东省科技计划项目，批准/授予号：2020B212060058
Handling Editor: Pim Bongaerts saving. Our findings suggest that adult heat acclimation can rapidly shift thermal tolerance of brooded coral larvae and provide integrated physiological and molecular evidence for this adaptive plasticity, which could increase climate resilience. However, the metabolic depression may be maladaptive for long-term organismal performance, highlighting the importance of curbing carbon emissions to better protect corals. 处理编辑：Pim Bongaerts我们的研究结果表明，成体热适应可以迅速改变育雏珊瑚幼虫的热耐受性，并为这种适应性可塑性提供了综合的生理和分子证据，这可以提高气候适应能力。然而，新陈代谢抑制可能会对生物体的长期表现产生不良影响，这凸显了遏制碳排放以更好地保护珊瑚的重要性。
Reef-building corals, the framework builders of coral reef ecosystems, are symbiotic cnidarians that form an obligate mutualistic relationship with dinoflagellates from the family Symbiodiniaceae (LaJeunesse et al., 2018). The algal symbionts translocate the majority of their photosynthetic products to sustain the energy demand of their coral host, and in return, the host nourishes symbionts with inorganic nutrients to fuel photosynthesis (Yellowlees et al., 2008). Tropical reef corals often live close to their upper thermal limits and are adversely affected by marine heat waves associated with climate change (Hoegh-Guldberg et al., 2017). During prolonged warming conditions, reef corals expel their algal symbionts, resulting in bleaching and mortality which have contributed significantly to the global degradation of coral reefs over the past decades (Hughes et al., 2018). It is therefore imperative to assess the ability of corals to acclimatize and/or adapt to ocean warming in this era of rapid climate change. 珊瑚礁生态系统的框架构建者--造礁珊瑚是一种共生的刺胞动物，与共生藻科的甲藻形成一种强制性的互生关系（LaJeunesse 等人，2018 年）。藻类共生体将其大部分光合产物转运到珊瑚宿主，以维持其能量需求，而作为回报，宿主则用无机营养物质滋养共生体，以促进光合作用（Yellowlees 等人，2008 年）。热带珊瑚礁珊瑚通常生活在其热上限附近，并受到与气候变化相关的海洋热浪的不利影响（Hoegh-Guldberg 等人，2017 年）。在长期变暖的条件下，珊瑚礁珊瑚会排出它们的藻类共生体，导致白化和死亡，这在过去几十年中极大地加剧了全球珊瑚礁的退化（Hughes 等人，2018 年）。因此，在这个气候变化迅速的时代，评估珊瑚适应和/或适应海洋变暖的能力势在必行。
Despite the consensus that the genetic adaptation of reef corals might not keep pace with the current rate of ocean warming due to their long generation time, it has been increasingly recognized that acclimatization through phenotypic plasticity may to some extent buffer against the immediate impacts of ocean warming on reef corals (Hackerott et al., 2021; Torda et al., 2017; Voolstra et al., 2021). Several studies demonstrated that thermal priming and environmental hardening can enhance the acclimatization and resistance of reef corals to thermal stress (Brown et al., 2015; DeMerlis et al., 2022; Hackerott et al., 2021; Yu et al., 2020), either through symbiont shuffling or transcriptional reprogramming (Barshis et al., 2013; Kenkel & Matz, 2016; Silverstein et al., 2015). Furthermore, numerous recent studies showed that adult preconditioning can mitigate and even fully offset the negative effects of climate change stressors on their offspring in a wide range of marine taxa, suggesting that transgenerational and/or developmental plasticity may also serve as key acclimatory mechanisms by which marine organisms can persist under climate change (Donelson et al., 2018; Maboloc & Chan, 2021; Wong et al., 2018; Yin et al., 2019). 尽管人们一致认为，由于珊瑚礁珊瑚的世代较长，其遗传适应性可能跟不上当前海洋变暖的速度，但人们越来越认识到，通过表型可塑性实现的适应性可在一定程度上缓冲海洋变暖对珊瑚礁珊瑚的直接影响（Hackerott等人，2021年；Torda等人，2017年；Voolstra等人，2021年）。多项研究表明，通过共生体洗牌或转录重编程（Barshis 等人，2013 年；Kenkel & Matz，2016 年；Silverstein 等人，2015 年），热引诱和环境硬化可增强珊瑚礁珊瑚对热应力的适应性和抵抗力（Brown 等人，2015 年；DeMerlis 等人，2022 年；Hackerott 等人，2021 年；Yu 等人，2020 年）。此外，最近的许多研究表明，在多种海洋类群中，成体预调节可以减轻甚至完全抵消气候变化压力因素对其后代的负面影响，这表明跨代和/或发育可塑性也可能成为海洋生物在气候变化下持续生存的关键适应机制（Donelson等人，2018年；Maboloc和Chan，2021年；Wong等人，2018年；Yin等人，2019年）。
Corals are sessile invertebrates with a pelagic larval phase which plays a vital role in population replenishment and recovery following disturbances. In an era of rapid climate change, it is of great interest to know if parental thermal acclimation/adaptation could improve larval heat resilience. Previous studies on broadcast spawning corals have shown strong maternal and paternal contributions to larval heat tolerance (Dixon et al., 2015; Howells et al., 2016, 2021). On the other hand, studies on the effects of adult stress exposure on offspring performance in brooding corals reported inconclusive results. For instance, preconditioning adult brooding corals to high temperature and/or either led to larval metabolic acclimation and improved settlement and survivorship of new recruits (Galanto et al., 2022; Putnam & Gates, 2015; Putnam et al., 2020), exerted negligible or negative influence on larval traits and tolerance to warmer temperatures (Bellworthy et al., 2019; McRae et al., 2021; Wong et al., 2021). Recently, parental preconditioning and transgenerational plasticity were proposed to be promising mechanisms of evolutionary rescue in coral reef conservation (Torda et al., 2017; Voolstra et al., 2021). However, it remains unclear to what extent heat acclimation of brooding corals could promote larval resilience. More importantly, our understanding of the physiological and molecular mechanisms underpinning this plasticity remains limited. Such information is of paramount importance to predict the adaptive capacity and evolutionary trajectory of reef corals facing global climate change. 珊瑚是一种无梗无脊椎动物，其幼虫处于浮游阶段，在受到干扰后的种群补充和恢复过程中发挥着至关重要的作用。在气候变化迅速的时代，了解亲本的热适应/适应能力是否能提高幼体的抗热能力是非常有意义的。之前对直播产卵珊瑚的研究表明，母体和父体对幼虫的耐热性有很大的贡献（Dixon 等人，2015 年；Howells 等人，2016 年，2021 年）。另一方面，关于成体压力暴露对育雏珊瑚后代表现的影响的研究却没有得出结论。例如，将成体育雏珊瑚预处理在高温和/或 条件下，要么会导致幼虫代谢适应，提高新成员的定居和存活率（Galanto 等人，2022 年；Putnam 与 Gates，2015 年；Putnam 等人，2020 年），要么对幼虫性状和对较高温度的耐受性影响微乎其微或产生负面影响（Bellworthy 等人，2019 年；McRae 等人，2021 年；Wong 等人，2021 年）。最近，有人提出亲本预调节和跨代可塑性是珊瑚礁保护中很有希望的进化拯救机制（Torda 等人，2017 年；Voolstra 等人，2021 年）。然而，目前仍不清楚育雏珊瑚的热适应在多大程度上能促进幼虫的恢复能力。更重要的是，我们对支撑这种可塑性的生理和分子机制的了解仍然有限。这些信息对于预测珊瑚礁珊瑚面对全球气候变化的适应能力和进化轨迹至关重要。
In the present study, we investigated the impact of thermal priming in adult coral Pocillopora damicornis on the heat tolerance of their brooded larvae. P. damicornis is a hermaphrodite species with a predominantly brooding reproductive mode (Fan et al., 2002). Here, we simulated a thermal priming event in adult P. damicornis that coincided with the larval development within the parent polyps. Although this design, similar to most prior studies, could not distinguish between parental effects and developmental acclimation of larval offspring (Donelson et al., 2018), it is ecologically relevant and does not affect the main objective of studying the acclimatory mechanism of corals to cope with future warming. We first examined the influence of thermal preconditioning on adult performance, timing of larval release, larval quantity and quality, and determined the effects of adult exposure on larval thermal performance curves (TPC). We then conducted a reciprocal transplant experiment to test the potential interaction between adult and offspring temperatures on larval physiology and analysed the transcriptomes of the host and symbionts after 在本研究中，我们调查了大鳃珊瑚成虫的热引诱对其育雏幼虫耐热性的影响。P. damicornis 是一种雌雄同体物种，主要采用育雏繁殖模式（Fan 等人，2002 年）。在此，我们模拟了大菱鲆成虫的热引诱事件，该事件与幼虫在亲体息肉中的发育过程相吻合。虽然这种设计与之前的大多数研究类似，无法区分亲本效应和幼虫后代的发育适应（Donelson 等人，2018 年），但它与生态相关，并且不影响研究珊瑚应对未来变暖的适应机制这一主要目标。我们首先考察了热预处理对成体性能、幼虫释放时间、幼虫数量和质量的影响，并确定了成体暴露对幼虫热性能曲线（TPC）的影响。然后，我们进行了一次相互移植实验，以检验成虫和后代温度对幼虫生理的潜在相互作用，并分析了成虫和后代温度变化后宿主和共生体的转录组。
reciprocal exposure to unravel the molecular signatures of thermal acclimation and phenotypic plasticity. 相互接触，以揭示热适应和表型可塑性的分子特征。
2 MATERIALS AND METHODS 2 材料和方法
2.1 | Experimental design 2.1 实验设计
Eight adult colonies of . damicornis diameter) were collected at depth on Luhuitou reef, Sanya, Hainan Island, China (N18 ) on 24 September 2020. P. damicornis from Sanya release free-swimming zooxanthellate larvae following a lunar cycle, with release beginning near the new moon, peaking around the first quarter moon, and ending before the full moon (Zhang, 2015). Gametogenesis and brooding usually overlap in P. damicornis, and larval development is rapid, because the time required for larval growth before release is approximately 3-4weeks (Permata et al., 2000; Stoddart & Black, 1985). 2020 年 9 月 24 日，在中国海南岛三亚鹿回头珊瑚礁（N18 ） ，采集到 8 个 . damicornis 直径）的成体。三亚的 P. damicornis 按月周期释放自由游动的聚氧贝壳幼体，释放从新月附近开始，在第一个季月前后达到高峰，在满月前结束（Zhang，2015 年）。P. damicornis的配子发生和育雏通常是重叠的，幼虫发育迅速，因为释放前幼虫生长所需的时间约为3-4周（Permata等人，2000年；Stoddart和Black，1985年）。
Colonies were immediately transported to the Tropical Marine Biological Research Station and reared in independent 20-L tanks that received flowing sand-filtered seawater and natural sunlight. Four colonies were randomly assigned to either the control treatment , mean or heat treatment , mean , Figure 1a). Seawater temperature in the control and heat treatment was regulated using chillers (Haili, HS90A, China) and digital heaters (Chaning, CN-008-1000 W, China), respectively. The greater temperature variation in the control treatment was due to the lower accuracy of temperature control of the chillers (Figure S1). 菌落被立即运送到热带海洋生物研究站，并在 20 升的独立水箱中饲养，水箱中的海水经过流沙过滤， ，并接受自然阳光照射。四个菌落被随机分配到对照处理 , 平均 或加热处理 , 平均 , 图 1a）。对照处理和加热处理的海水温度分别由制冷器（海利，HS90A，中国）和数字加热器（长宁，CN-008-1000 W，中国）调节。对照处理的温度变化较大，这是因为制冷机的温度控制精度较低（图 S1）。
Temperature in the control treatment represented the mean summer ambient temperature on the reefs, while temperature in the heat treatment was about above the bleaching threshold of local coral communities (Li et al., 2012). The heat ramping commenced on 25 September, which was five days before the full moon and close to the end of larval release in September. Seawater temperature in heat treatment was increased from at a rate of per day to and maintained thereafter for about 1 month until 27 October (Figure S1). Hence, the time course of adult priming encompassed the development duration of larvae that were expected to release in October. 对照处理的温度代表了珊瑚礁夏季的平均环境温度，而加热处理的温度比当地珊瑚群落的白化阈值高出约 （Li 等人，2012 年）。升温从 9 月 25 日开始，此时距满月还有 5 天，接近 9 月份幼虫释放的结束时间。加热处理中的海水温度从 以每天 的速度升至 ，此后维持约 1 个月，直至 10 月 27 日（图 S1）。因此，成虫启动的时间过程包含了预计在 10 月份释放的幼虫的发育期。
During the predicted planulation period in October, three colonies from each treatment were observed to release larvae and larvae were collected as described in Jiang et al. (2020). The number of larvae released by each colony was counted daily and normalized to the colony ecological volume (Levy et al., 2010). On 21 October (lunar day 5) near the peak release, larvae released by the three adults from each treatment were pooled in order to incorporate the maximum number of cohorts and focus on the average effects of thermal acclimation (Wong et al., 2018). Larvae from these two pools were randomly assigned for larval traits and TPCs characterization and the reciprocal transplant experiment (Figure 1b,c). 在 10 月份的预测繁殖期，观察每个处理的三个蜂群释放幼虫的情况，并按照 Jiang 等人（2020 年）的方法收集幼虫。对每个蜂群每天释放的幼虫数量进行计数，并将其归一化为蜂群生态体积（Levy 等，2010 年）。在 10 月 21 日（农历 5 月 5 日）接近释放高峰时，将每个处理的三只成虫释放的幼虫集中起来，以纳入最大数量的群落，并关注热适应的平均效应（Wong 等人，2018 年）。这两个池中的幼虫被随机分配用于幼虫性状和 TPCs 表征以及对等移植实验（图 1b、c）。
2.2 | Larval traits upon release and adult responses 2.2 | 幼虫释放后的性状和成虫的反应
On 12 October 2020, 100 larvae from each parental pool were haphazardly selected and photographed under a stereomicroscope. The length and width of each larva were measured using ImageJ, and larval volume was calculated following Isomura and Nishihira (2001). Four groups of 10 larvae from each adult pool were dark adapted for , and the maximum photochemical efficiency of photosystem (PS) II was measured using a Diving-PAM fluorometer (Walz, Germany) following Putnam et al. (2008). Briefly, one group of 10 larvae within a drop of seawater was loaded onto the tip of the 8 -mm-diameter probe. Both the measuring light intensity and gain were adjusted to seven to ensure optimal initial fluorescence. Furthermore, eight groups of 20 larvae were randomly sampled from each adult group and stored at for symbiont density quantification. Larvae were homogenized in of filtered and UV-sterilized seawater (FSW), centrifuged at for , and the pellet was resuspended in of FSW. The number of algal symbionts was counted using a haemocytometer with six replicate counts per sample, and the symbiont densities were expressed as average cells per larvae. 2020 年 10 月 12 日，从每个亲本池中随机挑选 100 只幼虫，在体视显微镜下拍照。使用 ImageJ 测量每条幼虫的长度和宽度，并按照 Isomura 和 Nishihira（2001 年）的方法计算幼虫体积。将每个成虫池中的四组 10 只幼虫进行黑暗适应 ，并按照 Putnam 等人（2008 年）的方法，使用 Diving-PAM 荧光仪（Walz，德国）测量光系统（PS）II 的最大光化学效率 。简言之，将 一滴海水中的一组 10 只幼虫装入直径为 8 毫米的探针顶端。测量光强和增益均调至 7，以确保最佳的初始荧光。此外，从每组成虫中随机抽取 8 组共 20 只幼虫，保存在 ，用于共生体密度定量。幼体在 的 过滤和紫外线灭菌海水（FSW）中匀化，在 离心 ，然后将沉淀重新悬浮在 的 FSW 中。使用血细胞计数器对藻类共生体的数量进行计数，每个样本重复计数 6 次，共生体密度以每条幼虫的平均细胞数表示。
Acute ramping heat experiments were conducted on four groups of 35 larvae randomly sampled from each parental pool, during which net photosynthesis rate and light-enhanced dark respiration rate (LEDR) were measured to establish larval TPC. A customed respirometry system was established, consisting of four transparent glass vials with optical oxygen sensors, a water bath , a magnetic stirrer, and a 4-channel oxygen meter (FireStingO2, Pyroscience). The oxygen sensors were two-point calibrated using air-equilibrated seawater ( oxygen) and a zero solution. Each group of 35 larvae was placed in a beaker filled with FSW and sequentially exposed to six temperatures . Larvae were illuminated with T5 fluorescent bulbs (Giesemann) providing an irradiance of mol photons . After incubation at each temperature for and LEDR rates of the eight samples were measured within . Each group of 35 larvae was transferred to a vial containing temperatureequilibrated FSW, and seawater within the vials was well mixed at a stirring rate of . Larvae gently swirled and remained intact and alive throughout the measurement under this stirring rate. After the respirometry measurement at one temperature, larvae were transferred back to the beaker and exposed to the next temperature for before the next respirometry measurement. was measured as the rate of production over in the light, after which the light was turned off, and LEDR was immediately measured as the consumption rate over another . Seawater concentrations within the vials were recoded every 10 s. and LEDR rates were calculated using the least-squares linear regressions of concentrations plotted against time and expressed as nanomoles of per min per larvae. Gross photosynthesis ) was obtained by adding to LEDR. 从每个亲本池中随机抽取四组共 35 只幼虫进行急性升温实验，在此期间测量净光合速率 和光增强暗呼吸速率 (LEDR) 以确定幼虫 TPC。建立了一套定制的呼吸测量系统，包括四个 带有光学氧气传感器的透明玻璃瓶、一个水浴 、一个磁力搅拌器和一个四通道氧气测量仪（FireStingO2，Pyroscience 公司）。氧传感器使用空气平衡海水 ( oxygen) 和零 溶液进行两点校准。每组 35 只幼虫被放置在一个装有 FSW 的 烧杯中，并依次暴露在六种温度下 。幼虫用 T5 荧光灯（Giesemann）照明，辐照度为 摩尔光子 。在每个温度下孵化 后，在 内测量 8 个样本的 LEDR 率。每组 35 只幼虫被转移到装有温度平衡 FSW 的 小瓶中，小瓶中的海水以 的搅拌速率充分混合。在此搅拌速率下，幼虫轻轻旋转，并在整个测量过程中保持完整和存活。在一个温度下进行呼吸测量后，幼虫被移回烧杯，并在下一个温度下进行 ，然后再进行下一次呼吸测量。 ，测量值为光照下 的产生率超过 ，然后关闭光照，LEDR 立即测量，测量值为 的消耗率超过另一个 。小瓶中的海水 浓度每 10 秒重新编码一次。 和 LEDR 率的计算采用 浓度与时间的最小二乘法线性回归，并以每只幼虫每分钟的纳摩尔 表示。总光合作用 ) 是通过将 加入 LEDR 而得到的。
(4)
Control 控制
Parental acclimation (b) 父母适应性 (b)
(c)
(e)
FIGURE 1 (a) Experimental design showing the adult acclimation to control and heat treatments and larval reciprocal transplant experiment; the potential shift in thermal performance curves and interaction between parental and offspring temperatures due to prior thermal preconditioning; (d) rates of adult net photosynthesis ), light-enhanced dark respiration and dark respiration (LEDR and ), gross photosynthesis , and ratio of to ; (e) symbiont densities and maximum photochemical efficiency ; (f) planulation timing and the number of larvae released by control and heat-acclimated adults, with the grey rectangle showing the larvae collected on lunar day 5 for subsequent larval experiments; (g) larval volume, symbiont density and of freshly-released larvae. Data are mean and 3 for adult physiological traits and larval release, respectively; and 8 for larval volume, and symbiont densities, respectively). Asterisks indicate significant differences between two adult groups at -values determined by Student's -test or Mann-Whitney U test [Colour figure can be viewed at wileyonlinelibrary.com] 图 1 (a) 实验设计显示成虫适应对照和热处理以及幼虫相互移植实验； ，由于先前的热预处理，热性能曲线可能发生变化，亲代和子代温度之间也可能发生相互作用；(d) 成虫净光合作用速率 )、光增强暗呼吸和暗呼吸速率 (LEDR 和 )、总光合作用速率 ，以及 与 之比；(e) 共生体密度和最大光化学效率 ；(f) 对照组和热适温成虫的刨坑时间和释放的幼虫数量，灰色矩形表示在农历第 5 天收集的幼虫，用于随后的幼虫实验；(g) 刚释放幼虫的幼虫体积、共生体密度和 。成虫生理特征和幼虫释放的数据分别为 和 3 的平均值；幼虫体积、 和共生体密度的数据分别为 和 8 的平均值）。星号表示两个成虫组在 -值 上的显著差异，由学生的 -检验或曼-惠特尼 U 检验确定[彩图可在 wileyonlinelibrary.com 上查看]。
At the end of larval release, a branchlet was cut from each colony, glued onto a ceramic base, and allowed to recover overnight. were measured on dark-adapted branchlets using a Diving-PAM. Adult branchlets were placed in chambers with a stir bar to measure and LEDR as described above. Furthermore, dark respiration of branchlets was measured after 1-h dark adaptation. Adult were calculated by adding to LEDR, and the ratio of to was calculated as a proxy for autotrophy. A ratio of suggests the capacity for autotrophy, that is, the net productivity of algal symbionts could satisfy holobiont dark respiration. After respirometry, adult branchlets were stored at to quantify symbiont densities and skeletal surface area. Coral tissue was airbrushed into FSW, and the tissue slurry was homogenized and centrifuged at for . The resulting symbiont pellets were resuspended in FSW for symbiont density quantification as aforementioned. Adult metabolic rates and symbiont densities were normalized to the skeletal surface area, which was measured using a JTscan-MS 在幼虫释放结束时，从每个群落中切下一个 小枝，粘在一个陶瓷基座上，并让其过夜恢复。 ，使用 Diving-PAM 对暗适应小枝进行测量。将成年小枝放入带有搅拌棒的 室中，如上所述测量 和 LEDR。此外，小枝的黑暗呼吸 是在黑暗适应 1 小时后测量的。成体 的计算方法是将 与 LEDR 相加，并计算 与 的比率，作为自营养的代表。 与 之比表明具有自养能力，即藻类共生体的净生产力可以满足全生物体的黑暗呼吸。呼吸测定后，将成体小枝保存在 ，以量化共生体密度和骨骼表面积。将珊瑚组织气刷到 FSW 中，然后将组织浆液匀浆并在 下离心 。将得到的共生体颗粒重新悬浮在 FSW 中，如上所述进行共生体密度定量。成体代谢率和共生体密度根据骨骼表面积进行归一化处理，骨骼表面积使用 JTscan-MS 测量。
high precision 3D scanner (Jeatech) following the manufacturer's instructions. 高精度 3D 扫描仪（Jeatech）。
To test the interaction between parental temperature ( ) and offspring temperature (To) on larval physiology, larvae from each parental pool were directly exposed to either ambient temperature , mean or high temperature , mean SD, Figure 1c and Figure S2). This typical reciprocal transplant design generated four treatments: (1) larvae from control and unacclimated adults raised at (U29), (2) larvae from control and unacclimated adults raised at (U32), (3) larvae from heat-acclimated adults raised at (A29), and (4) larvae from heat-acclimated adults raised at (A32). Coral larvae were incubated under these four treatments for five days, an ecologically relevant duration that could reliably detect the physiological effects of increased temperature on P. damicornis larvae (Cumbo et al., 2013). 为了检验亲本温度（ ）和子代温度（To）对幼虫生理的交互作用，将每个亲本池中的幼虫直接暴露于环境温度 ，平均值 或高温 ，平均值 SD，图 1c 和图 S2）。这种典型的对等移植设计产生了四种处理：(1)在 (U29)培养的对照组和非恒温成体的幼虫；(2)在 (U32)培养的对照组和非恒温成体的幼虫；(3)在 (A29)培养的热恒温成体的幼虫；(4)在 (A32)培养的热恒温成体的幼虫。珊瑚幼虫在这四种处理条件下孵化五天，这是一个与生态相关的持续时间，可以可靠地检测温度升高对 P. damicornis 幼虫的生理影响（Cumbo 等人，2013 年）。
Temperature treatments were created in eight 50-L tanks filled with fresh water. Four tanks were controlled at and the other four at using digital temperature controllers connected to titanium heaters (Weipro). Two 1-L beakers with of FSW were submerged into each tank, and 150 larvae from either adult group were transferred to each 1-L beaker for the sampling and analyses of physiology and transcriptomes (Figure S2). Furthermore, two glass vials, each containing 30 larvae from one of the two parental pools, were allocated to each tank to assess larval survivorship (Figure S2). The larval incubation system was illuminated with T5 fluorescent bulbs (Giesemann) on a 12:12 h light-dark cycle from 07:00 AM to 7:00 PM with a mean light intensity of photons . The light intensity was representative of that at the collection depth of adult colonies (Lei Jiang, personal observations), although the ecological relevance still depends on larval position in the water column. Seawater within beakers and glass vials was completely exchanged with temperature equilibrated FSW at 10:00 PM every day, and we used a mesh during seawater exchange to ensure that all larvae were retained and then transferred back to their corresponding container. 在八个装满淡水的 50 升水箱中进行温度处理。使用连接到钛加热器（Weipro）的数字温度控制器，将四个水箱的温度控制在 ，另外四个水箱的温度控制在 。将两个装有 FSW 的 1-L 烧杯浸入每个水槽中，并将来自任一成虫组的 150 只幼虫转移到每个 1-L 烧杯中，以进行生理和转录组的取样和分析（图 S2）。此外，两个 玻璃瓶分别装有来自两个亲本池之一的 30 只幼虫，被分配到每个池中以评估幼虫存活率（图 S2）。幼虫孵化系统采用 T5 荧光灯（Giesemann）照明，光暗周期为 12:12 小时，从早上 7:00 到晚上 7:00，平均光强为 photons 。光照强度代表了成体采集深度的光照强度（蒋磊，个人观察），但生态相关性仍取决于幼体在水体中的位置。烧杯和玻璃瓶中的海水每天晚上 10:00 与温度平衡的 FSW 完全交换，我们在海水交换过程中使用了 网眼，以确保保留所有幼虫，然后将其转移回相应的容器中。
At the end of the 5-day exposure, the number of larvae within glass vials were counted and those missing were considered dead. Larval mortality was calculated as the number of dead larvae divided by the initial number of 30 . At 10:00 AM on day 5 , one group of 10 larvae were sampled from each 1-L beaker. The effective photochemical efficiency was immediately measured on those light-adapted larvae using a Diving-PAM fluorometer, and then larvae were dark-adapted for to measure . Maximum excitation pressure over PSII and nonphotochemical quenching (NPQ) were calculated using the following equations: and (Iglesias-Prieto et al., 2004). Furthermore, one group of 35 larvae was sampled from each 1-L beaker, and rates of , LEDR, , and were measured and calculated as aforementioned (Figure S2). Following respirometry, these larvae were preserved for symbiont density quantification as described above. Larval bleaching rates were assessed as the relative change in symbiont density after five days exposure relative to the initial average. 在 5 天暴露结束时，对 玻璃瓶中的幼虫数量进行计数，未计数的幼虫视为死亡。幼虫死亡率的计算方法是：死亡幼虫数除以初始幼虫数 30。第 5 天上午 10:00 时，从每个 1 升烧杯中取样，每组 10 只幼虫。立即使用 Diving-PAM 荧光仪测量这些光适应幼虫的有效光化学效率 ，然后将幼虫进行暗适应 ，以测量 。PSII 和非光化学淬灭（NPQ）的最大激发压力是通过以下公式计算得出的： 和 （Iglesias-Prieto 等人，2004 年）。此外，从每个 1-L 烧杯中抽取一组 35 只幼虫，按照上述方法测量和计算 、LEDR、 和 的速率（图 S2）。在进行呼吸测定后，这些幼虫被保存起来，以便按上述方法进行共生体密度定量。幼虫漂白率是以暴露五天后共生体密度相对于初始平均值的相对变化来评估的。
2.4 RNA-Seq and transcriptome analysis 2.4 RNA-Seq 和转录组分析
On completion of the incubation, one group of 50 swimming larvae were sampled from each 1-L beaker and snap-frozen in liquid nitrogen for transcriptome analysis (Figure S2). Total RNA was extracted using a Trizol reagent kit (Invitrogen), and RNA quantity and quality were assessed on an Agilent 2100 Bioanalyser and checked using RNase free agarose gel electrophoresis. One of the four U32 samples was discarded because of poor RNA quality. For each sample, of total RNA was processed (including mRNA enrichment via polyA+ selection) using the NEB Next Ultra RNA Library Prep Kit (NEB) to construct cDNA libraries. Sequencing of paired-end reads on a total of 15 samples was performed on Illumina Novaseq 6000 at Gene Denovo Biotechnology Co., Ltd. 培养结束后，从每个 1 升烧杯中抽取一组 50 只游动幼虫，在液氮中速冻，用于转录组分析（图 S2）。使用 Trizol 试剂盒（Invitrogen 公司）提取总 RNA，在 Agilent 2100 生物分析仪上评估 RNA 的数量和质量，并使用无 RNase 琼脂糖凝胶电泳进行检测。四个 U32 样本中有一个因 RNA 质量不佳而被放弃。使用 NEB Next Ultra RNA 文库制备试剂盒（NEB）处理 总 RNA（包括通过 polyA+ 选择富集 mRNA），构建 cDNA 文库。 成对末端读数的测序是在 Gene Denovo Biotechnology Co., Ltd. 的 Illumina Novaseq 6000 上进行的。
Raw data were trimmed using FASTP to remove low-quality reads, -content reads, and reads containing adapters and poly-A tails (Chen et al., 2018), and then subjected to rRNA filtering using the short reads alignment tool Bowtie2 (Langmead & Salzberg, 2012). The remaining high-quality clean reads were first mapped to P. damicornis genome using HISAT2.2.4 (Cunning et al., 2018; Kim et al., 2015). The mapping rate ranged from to , and these reads were assembled using StringTie version 1.3.1 in a reference-based approach to construct the coral transcriptomes (Pertea et al., 2015). The remaining unmapped reads were assembled de novo using the Trinity program (Grabherr et al., 2011), and then aligned against a constructed database of Symbiodiniaceae genomes and transcriptomes (Table S1) using BLASTN (E-value cutoff of . . Those transcripts significantly aligned to Symbiodiniaceae references were labelled as symbiont genes. Redundancy of symbiont transcripts was removed using CD-HIT-EST (Huang et al., 2010) with a threshold of at least sequence similarity. Details of raw reads quality control, mapping, and information on coral and symbiont transcriptomes are provided in Table S1. Transcripts were functionally annotated using BLAST with a cutoff E-value of based on the following databases: Swiss-Prot, NCBI nonredundant (Nr) protein, EuKaryotic orthologous groups (KOG), gene ontology (GO), and KEGG orthologue database (KO). 使用 FASTP 对原始数据进行修剪，以去除低质量读数、 -content 读数以及含有适配体和 poly-A 尾部的读数（Chen 等，2018 年），然后使用短读数比对工具 Bowtie2（Langmead & Salzberg，2012 年）进行 rRNA 过滤。剩余的高质量洁净读数首先使用 HISAT2.2.4 （Cunning 等，2018；Kim 等，2015）映射到 P. damicornis 基因组。映射率从 到 不等，这些读数使用 StringTie 1.3.1 版进行组装，采用基于参考的方法构建珊瑚转录组（Pertea 等人，2015 年）。剩余的未映射读数使用 Trinity 程序（Grabherr 等人，2011 年）从头组装，然后使用 BLASTN（E 值截断为 .与 Symbiodinceae 参考文献明显对齐的转录本被标记为共生体基因。共生转录本的冗余采用 CD-HIT-EST（Huang 等，2010 年）去除，阈值为至少 序列相似性。表 S1 提供了原始读数质量控制、绘图以及珊瑚和共生体转录组信息的详细信息。使用 BLAST 对转录本进行功能注释，E-value 临界值为 ，基于以下数据库：Swiss-Prot、NCBI 非冗余（Nr）蛋白质、EuKaryotic orthologous groups (KOG)、gene ontology (GO) 和 KEGG orthologue database (KO)。
Differentially expressed genes (DEGs) were identified using DESeq2 with thresholds of an adjusted -value of and an absolute (fold change) value of (Love et al., 2014). Four pairwise comparisons were designated in the DEG analyses: versus U32, U29 versus A29, A29 versus A32 and U32 versus A32. The short time-series expression miner (STEM) program was used to cluster DEGs into profiles based on the expression trend across treatments (Ernst & Bar-Joseph, 2006). GO functional enrichment analyses were 使用 DESeq2 鉴定差异表达基因（DEGs），阈值为 的调整 - 值和 的绝对 （折合变化）值（Love 等人，2014 年）。在 DEG 分析中指定了四个配对比较： 与 U32、U29 与 A29、A29 与 A32 和 U32 与 A32。使用短时序列表达挖掘程序（STEM）根据不同处理间的表达趋势将 DEGs 聚类为剖面图（Ernst & Bar-Joseph, 2006）。GO功能富集分析
performed on the STEM-defined profiles to identify the enriched GO terms (Yu et al., 2012). 对 STEM 定义的图谱进行分析，以确定富集的 GO 术语（Yu 等人，2012 年）。
To identify the symbiont genotypes within larvae, we conducted a local BLAST search of the symbiont transcriptomes against a database containing sequences of three molecular markers (PSII protein D1, mitochondrial cytochrome b, and elongation factor 2) from the eight genera of Symbiodiniaceae downloaded from GenBank. 为了确定幼虫体内的共生体基因型，我们对共生体转录组进行了局部 BLAST 搜索，并将其与从 GenBank 下载的、包含三个分子标记（PSII 蛋白 D1、线粒体细胞色素 b 和伸长因子 2）序列的数据库进行了比对。
2.5 | Data analysis 2.5 数据分析
Acute TPC of metabolic traits was fitted for each larval group using four functions: second-order polynomial, Gaussian, GaussianGompertz and Sharpe-Schoolfield. Using the Akaike information criterion (AIC) approach, the second-order polynomial was selected as the best-fit function to describe the relationship between temperature and larval metabolism based on the lowest AIC score. AIC is a mathematical method that estimates the relative amount of information lost by a given model, and therefore the model with the lowest AIC score is considered as the best-fit. Curve fitting and model selection were performed using the nls package in R. The optimal temperatures and maximal performance rates were determined from the parameterized functions. The critical thermal maximum was defined as the temperature at which larval metabolic rates were reduced to only of the maximal performance. of and was calculated from the parameterized functions, while of LEDR was not determined due to its insensitivity to high temperature. 用四种函数拟合了每个幼虫组的代谢特征的急性TPC：二阶多项式函数、高斯函数、高斯-冈珀兹函数和夏普-斯考菲尔德函数。使用阿凯克信息准则（AIC）方法，根据最低的 AIC 分数，选择二阶多项式作为描述温度与幼虫代谢之间关系的最佳拟合函数。AIC 是一种数学方法，用于估算特定模型损失的相对信息量，因此 AIC 分数最低的模型被认为是最佳拟合模型。曲线拟合和模型选择使用 R 软件包 nls 进行。临界最高温度 被定义为幼虫新陈代谢率降低到仅为最高性能的 时的温度。 和 的 是通过参数化函数计算得出的，而 LEDR 的 由于对高温不敏感而没有确定。
Data were checked for normality and homogeneity of variance using Shapiro-Wilk and Levene's tests, respectively. Data were In- or arctan-transformed when normality and homogeneity assumptions were violated. Student's test and Mann-Whitney test were used to examine the differences in adult and larval traits and TPC-related parameters among the two temperature treatments. For reciprocal transplant experiment, the main and interactive effects of Tp and To on larval physiology were evaluated by two-way ANOVAs. 数据分别采用 Shapiro-Wilk 检验和 Levene 检验进行正态性和方差齐性检验。如果违反了正态性和同质性假设，则对数据进行 In- 或 arctan 转换。学生 检验和 Mann-Whitney 检验用于检验两种温度处理之间成虫和幼虫性状以及 TPC 相关参数的差异。在对等移植实验中，采用双因素方差分析评估了 Tp 和 To 对幼虫生理的主效应和交互效应。
3 | RESULTS 3 结果
3.1 Adult and larval conditions following heat acclimation 3.1 热适应后的成虫和幼虫状况
After 1-month acclimation to , adult colonies of . damicornis significantly decreased and but increased LEDR and (Figure ), thus resulting in a lower ratio and a reduced autotrophic capacity (Figure ). was slightly lowered in heat-acclimated adults, but the difference was not statistically significant (Figure 1e). In contrast, symbiont densities decreased by in heat-acclimated adults (Figure 1e), suggesting symbiont loss and bleaching. 在 中适应 1 个月后， 的成虫群落。damicornis 显著降低了 和 ，但增加了 LEDR 和 （图 ），从而导致 比率降低，自养能力下降（图 ）。热适应成虫的 略有降低，但差异无统计学意义（图 1e）。与此相反，共生体密度在热气候条件下的成体中降低了 （图 1e），表明共生体损失和漂白。
Peak larval release occurred 4 days earlier in heat-acclimated adults, and the number of planulae larvae during the peak release in the heat treatment was twice that of the control (Figure 1f). Larval volume and were similar in freshly-released larvae among the two parental groups (Figure 1g). In contrast, the number of algal symbionts declined by in larvae brooded by the heat-acclimated parents (Figure 1g). TPC parameterization showed that heat acclimation shifted TPCs of , LEDR and (Figure 2a-c), resulting in significantly higher maximal but lower maximal LEDR in larvae (Figure 2d,e). Furthermore, the optimal temperatures of , LEDR and increased by , while of increased by in larvae from heat-acclimated parents compared to those from control (Figure 2d-f). 热适温成虫的幼虫释放高峰期提前了 4 天，热处理组释放高峰期的刨状幼虫数量是对照组的两倍（图 1f）。两个亲本组刚释放的幼虫体积和 相似（图 1g）。与此相反，在热适温亲本育雏的幼虫中，藻类共生体的数量减少了 （图 1g）。TPC参数化结果表明，热适应改变了 、LEDR和 的TPC（图2a-c），导致幼虫的最大 ，但最大LEDR却明显降低（图2d,e）。此外，与对照组相比，热适应亲本幼虫的 、LEDR 和 的最适温度增加了 ，而 的 增加了 （图 2d-f）。
3.2 | Larval physiology following reciprocal exposure 3.2 | 相互接触后的幼虫生理机能
After reciprocal transplantation of larvae, mortality varied significantly in response to , To and their interaction, with lower larval mortality in A32 (Figure 3a). was reduced by To, irrespective of parental origin, while the values were still above 0.58 at (Figure 3b). There was a significant interaction between and To on and NPQ. The U32 larvae exhibited significantly lower but higher and NPQ than those in A32 (Figure ), indicating chronic photoinhibition and the dominance of photoinhibitory quenching in U32. Symbiont density per larvae was significantly affected by To, and there was a marginally significant interaction between Tp and To (Figure 3f). Remarkably, symbiont densities of the larvae from the control adults declined by after five days exposure to , indicating symbiont expulsion and bleaching (Figure ). In contrast, those from the heat-acclimated adults doubled symbiont populations when incubated at and showed a zero change at , suggesting the maintenance of symbiont density and enhanced bleaching tolerance (Figure ). 幼虫对等移植后，死亡率对 、To 及其交互作用的影响显著不同，A32 的幼虫死亡率较低（图 3a）。无论亲本来源如何，To 都会降低 的死亡率，而 的死亡率值仍高于 0.58（图 3b）。 和 To 对 和 NPQ 有明显的交互作用。U32 幼虫的 明显低于 A32 幼虫，但 和 NPQ 却高于 A32 幼虫（图 ），这表明 U32 幼虫长期受光抑制，光抑制淬灭占主导地位。每只幼虫的共生体密度受到 To 的显著影响，Tp 与 To 之间的交互作用略微显著（图 3f）。值得注意的是，对照成虫的幼虫共生体密度在暴露于 五天后下降了 ，表明共生体被驱逐和漂白（图 ）。与此相反，在 条件下孵化的热适应成虫的共生体数量增加了一倍，在 条件下变化为零，这表明共生体密度得以维持，漂白耐受性增强（图 ）。
Larval was significantly affected by the interaction between Tp and To, with the highest in A32 (Figure 3h). LEDR was significantly reduced in larvae from heat-acclimated parents than those from control (Figure 3i). However, was comparable among treatments (Figure ). There was a significant interaction between Ta and To for , with higher when Tp and To were correlated (Figure ). The ratio was significantly affected by , with the highest ratio above 1 (i.e., autotrophy) observed in A32 (Figure 3I). 幼虫 受到 Tp 和 To 交互作用的显著影响，A32 的 最高（图 3h）。与对照组相比，来自热适 应亲本的幼虫的 LEDR 明显降低（图 3i）。然而，不同处理的 具有可比性（图 ）。Ta 和 To 对 有明显的交互作用，当 Tp 和 To 相关时， 更高（图 ）。 比率受 的影响很大，A32 的比率最高，超过 1（即自养）（图 3I）。
3.3 Transcriptomes, DEG analysis and functional enrichment 3.3 转录组、DEG 分析和功能富集
To better understand the physiological responses of larvae, we evaluated changes in gene expression through RNA-Seq. Ordination plots and Adonis analyses showed that the separation of transcriptomes according to and To was statistically significant in both the host and symbionts, and a significant interaction between and To was detected for the host transcriptomes (Figure S3). The largest number of DEGs was identified in U32 为了更好地了解幼虫的生理反应，我们通过 RNA-Seq 评估了基因表达的变化。排序图和 Adonis 分析表明，在宿主和共生体中，根据 和 To 对转录组进行的分离具有统计学意义，而且在宿主转录组中检测到 和 To 之间存在显著的交互作用（图 S3）。在 U32 中发现的 DEGs 数量最多。
(e)
FIGURE 2 (a-c) thermal performance curves of net photosynthesis, lightenhanced dark respiration, and gross photosynthesis rates of larvae from control and heat-acclimated adults, with lines displaying the best-fit secondorder polynomial; (d-f) modelled acute optimal temperatures, critical thermal maximum, and maximal metabolic rates. Critical thermal maximum of LEDR was not determined due to its insensitivity to high temperature. Data are mean . Asterisks indicate significant differences between two larval groups at -values determined by Student's t-test versus in both the host and symbiont transcriptomes, most of which were unique to this comparison (Figure 4a,b). Blast search found only Symbiodiniaceae Durusdinium (clade D) in all samples (Table S1). 图 2 (a-c)对照组和热螯合成虫幼体的净光合作用、光增强暗呼吸作用和总光合作用率的热性能曲线，线条显示最佳拟合的二阶多项式；(d-f)模拟的急性最适温度、临界最高热量和最大代谢率。由于 LEDR 对高温不敏感，因此没有确定其临界最高热量。数据为平均值 。星号表示两个幼虫组之间在 -值 由学生 t 检验确定与 在宿主和共生体转录组中的显著差异，其中大部分差异是本次比较所独有的（图 4a,b）。Blast 搜索在所有样本中只发现了共生藻科的 Durusdinium（支系 D）（表 S1）。
STEM analyses of host DEGs identified significantly assigned profiles (Figure 4c) for genes that: (i) displayed the highest expression levels in A32 (profile 9); and (ii) were specifically downregulated in U32 (profile 3). The majority of DEGs (78.4%) in profile 9 exhibited higher baseline expression and greater plasticity (sensu Rivera, Aichelman, et al., 2021) in response to heat stress in bleachingtolerant larvae from heat-acclimated parents (Figure S4a), and were mainly enriched with terms related to cellular response to stress, mitotic cell cycle, cell division, and transporter activity. Within profile 3, GO terms that were identified included small molecule metabolic process and cellular amino acid catabolic process (Table S2). 对宿主 DEGs 的 STEM 分析为以下基因确定了显著的分配图谱（图 4c）：(i) 在 A32 中表达水平最高（图谱 9）；(ii) 在 U32 中特异性下调（图谱 3）：(i)在 A32 中表达水平最高（图谱 9）；(ii)在 U32 中特别下调（图谱 3）。在图谱 9 中，大多数 DEGs（78.4%）表现出较高的基线表达量和较强的可塑性（sensu Rivera, Aichelman, et al. 2021），以应对来自耐热亲本的耐漂白幼虫的热胁迫（图 S4a），并且主要富含 与细胞对胁迫的反应、有丝分裂细胞周期、细胞分裂和转运体活性相关的术语。在图谱 3 中，确定的 GO 术语包括小分子代谢过程和细胞氨基酸分解代谢过程（表 S2）。
STEM analyses of all symbiont DEGs identified several gene profiles (Figure 4d), including: (1) DEGs that were increased from U29 to A32 (profile 9), (2) DEGs that were downregulated from U29 to A32 (profile 0) and (3) DEGs that were specifically upregulated in U32 (profile 6). Profiles 9 and 0 were both enriched with GO terms related to photosynthesis, such as photosystem reaction centres and photosynthesis, suggesting mixed responses of photosynthesisrelated genes to Tp and To (Table S6). Within symbiont profile 6, DEGs were enriched with GO terms primarily regarding metabolism, including nitrogen compound metabolic process, cellular catabolic process, and cellular amino acid metabolic process (Table S6). 对所有共生体 DEGs 的 STEM 分析确定了几个基因图谱（图 4d），包括：(1) 从 U29 到 A32 增加的 DEGs（图谱 9）；(2) 从 U29 到 A32 下调的 DEGs（图谱 0）；(3) 在 U32 中特异性上调的 DEGs（图谱 6）。图谱 9 和图谱 0 都富含与光合作用有关的 GO 术语，如光合系统反应中心和光合作用，这表明光合作用相关基因对 Tp 和 To 的反应是混合的（表 S6）。在共生体图谱 6 中，DEGs 富集了主要与代谢有关的 GO 术语，包括氮化合物代谢过程、细胞分解代谢过程和细胞氨基酸代谢过程（表 S6）。
3.4 | Host transcriptomic responses 3.4 宿主转录组反应
3.4.1 Cellular stress response 3.4.1 细胞应激反应
Most host DEGs related to cellular stress response exhibited higher baseline expression and responsiveness to heat stress in larvae from heat-acclimated adults (Figure S4b). This functional group included genes involved in cellular redox control, heat shock proteins (HSPs)-mediated protein folding, unfolded protein response (UPR), and endoplasmic reticulum-associated degradation of misfolded proteins (ERAD, Figure S5; Table S3). These genes are well-known stress response genes involved in redox regulation and refolding and processing of misfolded proteins to aid the recovery of cells from heat-induced damage. Notably, 49 prosurvival and prodeath genes and those with dual roles in inducing and inhibiting programmed cell death (PCD) were highly upregulated in A32 (Table S5; Figure S4). 大多数与细胞应激反应有关的宿主 DEGs 在来自热适应成虫的幼虫中表现出较高的基线表达和对热应激的反应性（图 S4b）。该功能组包括参与细胞氧化还原控制、热休克蛋白（HSPs）介导的蛋白质折叠、未折叠蛋白反应（UPR）和内质网相关的错误折叠蛋白降解（ERAD，图 S5；表 S3）的基因。这些基因都是众所周知的应激反应基因，它们参与氧化还原调节以及错误折叠蛋白的重折叠和处理，以帮助细胞从热诱导的损伤中恢复。值得注意的是，在 A32 中，49 个促生存和促死亡基因以及在诱导和抑制细胞程序性死亡（PCD）中具有双重作用的基因高度上调（表 S5；图 S4）。
3.4.2 | Broad upregulation of genes involved in cell cycle and mitosis 3.4.2 | 参与细胞周期和有丝分裂的基因广泛上调
DEGs linked to cell cycle and mitosis were the largest functional group, with the highest expression in A32 and greater plasticity in larvae from heat-acclimated adults (Figure S4c). In particular, 93 DEGs involved in cell cycle checkpoints and regulations of cell cycle transitions were identified (Figures S7 and S8; Table S4). 与细胞周期和有丝分裂相关的 DEGs 是最大的功能组，在 A32 中的表达量最高，在来自热适应成虫的幼虫中的可塑性更大（图 S4c）。特别是发现了 93 个参与细胞周期检查点和细胞周期转换调控的 DEGs（图 S7 和 S8；表 S4）。
FIGURE 3 Larval physiology following the 5-day reciprocal transplant experiment: (a) mortality, (b) maximum photochemical efficiency, (c) effective photochemical efficiency, (d) maximum excitation pressure over PSII, (e) nonphotochemical quenching, (f) symbiont density, (g) relative change in symbiont density, (h) net photosynthesis, (i) light-enhanced dark respiration, (j) dark respiration, (k) gross photosynthesis, and (I) ratio of net photosynthesis and dark respiration. Data are mean . The effects of parent and offspring temperatures ( and to) and their interaction were determined using two-way ANOVAs 图 3 5 天互惠移植实验后的幼虫生理学：(a) 死亡率，(b) 最大光化学效率，(c) 有效光化学效率，(d) PSII 的最大激发压力，(e) 非光化学淬灭，(f) 共生体密度，(g) 共生体密度的相对变化，(h) 净光合作用，(i) 光增强暗呼吸，(j) 暗呼吸，(k) 总光合作用，以及 (I) 净光合作用与暗呼吸的比率。数据为平均值 。使用双向方差分析确定了亲代和子代温度 ( 和至) 的影响及其交互作用
small molecule metabolic process cellular amino acid catabolic process (d) STEM-defined symbiont gene profiles 小分子代谢过程 细胞氨基酸分解代谢过程 (d) STEM-defined 共生基因图谱
photosystem I reaction center photosystem I 光系统 I 反应中心 光系统 I
photosystem II reaction center 光系统 II 反应中心
nitrogen compound metabolic process cellular catabolic process cellular amino acid metabolic process 氮化合物代谢过程 细胞分解代谢过程 细胞氨基酸代谢过程
FIGURE 4 (a, b) Venn diagram displaying the number and overlaps of differentially expressed genes for each pairwise comparison in the host and symbionts; (c, d) STEM-defined profiles of all host and symbiont DEGs along with the associated GO terms [Colour figure can be viewed at wileyonlinelibrary.com] 图 4 (a, b) 维恩图显示宿主和共生体中每对比较的差异表达基因的数量和重叠情况；(c, d) STEM 定义的所有宿主和共生体 DEGs 图谱以及相关的 GO 术语[彩图可在 wileyonlinelibrary.com 上查看]。
Furthermore, we found over 200 upregulated DEGs linked to DNA replication, replication-coupled nucleosome disassembly and reassembly, DNA repair mechanisms, centrosome cycle, chromosome condensation and decondensation, mitotic spindle assembly, and cytokinesis (Figures S9-S15). 此外，我们还发现了 200 多个与 DNA 复制、复制耦合核小体拆分和重组、DNA 修复机制、中心体周期、染色体凝聚和解聚、有丝分裂纺锤体组装和细胞分裂相关的 DEGs 上调（图 S9-S15）。
3.4.3 Nutrient transport 3.4.3 营养物质运输
Numerous transporter genes involved in the transmembrane transporting of nutrients were highly upregulated in A32 (Figure S16; Table S5). Most of these genes belong to the ATP-binding cassette (ABC) transporter and solute carrier (SLC) superfamilies. transporters have been found localized in symbiosome membrane, implying potential and important roles in host uptake of nutrients from symbionts (Peng et al., 2010). Of particular interest, we noted transporter genes that were specifically responsible for translocating metabolites from symbionts to the host, including monocarboxylates (SLC16s), glucose (SLC5A8), and lipid (NPC1). In addition, one vacuolar-type -ATPase (ATP6VOA1) and three bicarbonate transporters (SLC4 and SLC26) were highly upregulated in A32, which are critical in carbon concentrating mechanisms (CCMs) for symbiont photosynthesis. 参与营养物质跨膜转运的许多转运体基因在 A32 中高度上调（图 S16；表 S5）。这些基因大多属于 ATP 结合盒（ABC）转运体和溶质载体（SLC）超家族。 转运体已被发现定位在共生体膜上，这意味着它们在宿主从共生体吸收营养物质的过程中发挥着潜在的重要作用（Peng 等，2010 年）。特别值得注意的是，我们注意到一些转运体基因专门负责将代谢物从共生体转运到宿主体内，包括单羧酸盐（SLC16s）、葡萄糖（SLC5A8）和脂质（NPC1）。此外，一个液泡型 -ATP酶（ATP6VOA1）和三个碳酸氢盐转运体（SLC4和SLC26）在A32中高度上调，它们在共生体光合作用的碳浓缩机制（CCM）中至关重要。
3.5.1 | Mixed changes in expression of photosynthesis related genes 3.5.1 光合作用相关基因表达的混合变化
To explore the molecular response patterns underlying the thermal acclimation of symbionts, we also quantified the transcriptomic changes in algal symbionts. DEGs encoding the subunits of PSII, PSI and cytochrome b6-f complex were found either downregulated in A29 and A32, or were specifically upregulated in A32 (Figure 5a-c; Table S7). In particular, four genes encoding the PSII core subunits, that is, protein D1 and D2 (psbA and psbB), and CP43 and CP47 (psbC and psbD), and 3 genes encoding the PSI core subunits PSI P700 chlorophyll a apoprotein A1 and A2 (psaA and psaB) and PSI reaction centre subunit IV (psaE) were highly upregulated in A32. 为了探索共生体热适应的分子响应模式，我们还量化了藻类共生体的转录组变化。发现编码 PSII、PSI 和细胞色素 b6-f 复合物亚基的 DEGs 在 A29 和 A32 中要么下调，要么在 A32 中特异性上调（图 5a-c；表 S7）。其中，编码 PSII 核心亚基（即蛋白 D1 和 D2（psbA 和 psbB）、CP43 和 CP47（psbC 和 psbD））的 4 个基因，以及编码 PSI 核心亚基 PSI P700 叶绿素 a 蛋白 A1 和 A2（psaA 和 psaB）和 PSI 反应中心亚基 IV（psaE）的 3 个基因在 A32 中高度上调。
Eight light harvesting complex (LHC) genes, including fucoxanthin-chlorophyll a-c binding protein (FCP), carotenochlorophyll a-c-binding protein (CCAC), and chloroplast soluble peridinin-chlorophyll a-binding (PCP), were downregulated in A29 and A32 compared to U32 (Figure 5d). Consistent with the downregulation in LHC genes, expression levels of 14 genes related to chlorophyll metabolism were lower in A32 compared with U32. Among them, those related to chlorophyll synthesis, such as chlorophyllide a oxygenase (CAO) and protoporphyrinogen oxidase, chloroplastic (PPOX1), exhibited the highest expression level in U32 (Figure S17; Table S7). In addition, 2 DEGs encoding LHC stress-related proteins 与 U32 相比，A29 和 A32 中的 8 个采光复合物（LHC）基因，包括岩藻黄素-叶绿素 a-c 结合蛋白（FCP）、胡萝卜素-叶绿素 a-c 结合蛋白（CCAC）和叶绿体可溶性过叶绿素-叶绿素 a 结合蛋白（PCP）的表达水平均有所下降（图 5d）。与 LHC 基因的下调一致，与 U32 相比，14 个与叶绿素代谢相关的基因在 A32 中的表达水平较低。其中，与叶绿素合成相关的基因，如叶绿素化合加氧酶（CAO）和原卟啉原氧化酶，叶绿体（PPOX1），在 U32 中的表达水平最高（图 S17；表 S7）。此外，2 个编码 LHC 应激相关蛋白的 DEGs
(LHCSR1 and LHCSR3.1), as the major effector of NPQ, were highly upregulated in U32 (Figure 5d). However, three genes encoding violaxanthin de-epoxidase (VED) and zeaxanthin epoxidase (ZEP), the two key enzymes in xanthophyll cycle, were highly upregulated in A32 (Figure 5b-d). (在 U32 中，作为 NPQ 主要效应因子的 LHCSR1 和 LHCSR3.1 基因高度上调（图 5d）。然而，编码中黄素循环中两种关键酶--中黄素脱氧化酶（VED）和玉米黄素环氧化酶（ZEP）的三个基因在 A32 中高度上调（图 5b-d）。
Furthermore, four key genes related to photorespiration were downregulated in A32 (Figure 5b-d), including the core photorespiratory transporter plastidal glycolate/glycerate translocator 1 (PLGG1) and phosphoglycolate phosphatase (PGLP) and D-glycerate 3-kinase (GLYK), which catalyse the first and last reactions in photorespiration, respectively. In contrast, nine DEGs involved in algal CCM and C4 pathway and 14 DEGs involved in Calvin cycle, starch synthesis and transformation were highly upregulated in A32 (Figure 5b-d), suggesting higher carbon fixation efficiency and photosynthetic yield. 此外，4 个与光呼吸相关的关键基因在 A32 中下调（图 5b-d），包括核心光呼吸转运体质体乙醇/甘油酸转运体 1（PLGG1）、磷酸乙醇磷酸酶（PGLP）和 D-甘油酸 3-激酶（GLYK），它们分别催化光呼吸的第一个和最后一个反应。相比之下，参与藻类 CCM 和 C4 途径的 9 个 DEGs 和参与卡尔文循环、淀粉合成和转化的 14 个 DEGs 在 A32 中高度上调（图 5b-d），表明其碳固定效率和光合产量更高。
3.5.2 | Regulation of symbiont catabolic and anabolic metabolism 3.5.2 | 对共生体分解代谢和合成代谢的调控
Symbionts from the control and heat-acclimated adults exhibited differential transcriptional responses of metabolic pathways. Symbiont genes related to several metabolic pathways, such as oxidative phosphorylation, TCA cycle, sulphur metabolism, glycolysis, catabolism of cholesterol and diacylglycerol, and fatty acid -oxidation, were downregulated in A29 and A32 compared to their respective controls (Figure S18; Table S8). These changes were indicative of a pronounced metabolic depression and decreased catabolic activity in algal symbionts after heat acclimation (Figure 6). Regarding nitrogen compound metabolism in symbionts, the expression levels of five genes critically involved in nitrogen assimilation and cycling (including high-affinity nitrate transporter, nitrate reductase, nitrite reductase, and ammonia transporters) and 49 genes implicated in both the biosynthesis and degradation of amino acids were higher in U32 than A32 (Figure S18; Table S8). 对照组和热螯合成体的共生体在代谢途径上表现出不同的转录反应。与各自的对照组相比，A29 和 A32 中与氧化磷酸化、TCA 循环、硫代谢、糖酵解、胆固醇和二酰基甘油的分解代谢以及脂肪酸 -氧化等几种代谢途径相关的共生体基因都出现了下调（图 S18；表 S8）。这些变化表明藻类共生体在热适应后出现了明显的代谢抑制和分解代谢活性降低（图 6）。在共生体的氮化合物代谢方面，U32 中关键参与氮同化和循环的 5 个基因（包括高亲和性硝酸盐转运体、硝酸盐还原酶、亚硝酸盐还原酶和氨转运体）以及参与氨基酸生物合成和降解的 49 个基因的表达水平均高于 A32（图 S18；表 S8）。
Contrary to the downregulation in catabolic pathways, several symbiont genes associated with lipid biosynthesis, including the bile acid-sodium symporter family protein (BASS2) and acyl-CoAbinding proteins (ACBP3 and ACBP6), were highly upregulated in A32 (Figure S18; Table S8). BASS2 is responsible for importing pyruvate into chloroplasts for the plastid-localized biosynthesis of fatty acids, while ACBPs are critical in exporting fatty acids synthesized de novo in chloroplasts to ER for lipid biosynthesis and storage in plants. Furthermore, twenty DEGs encoding transporters for sugars, lipids, amino acids, and minerals were upregulated in A29 and A32 relative to their respective controls, including putative sodiumcoupled neutral amino acid transporter 11, sodium-dependent dicarboxylate transporter SDCS, sugar transporter SWEET1, and putative sugar phosphate/phosphate translocators (Figure S19). Among them, SWEET1 has been suggested to transfer sugar from symbionts to the cnidarian host (Maor-Landaw et al., 2020; Xiang et al., 2017). 与分解代谢途径的下调相反，与脂质生物合成相关的几个共生基因，包括胆汁酸-钠交感蛋白家族蛋白（BASS2）和酰基-CoA 结合蛋白（ACBP3 和 ACBP6）在 A32 中高度上调（图 S18；表 S8）。BASS2 负责将丙酮酸输入叶绿体，以进行质体定位的脂肪酸生物合成，而 ACBPs 则是将叶绿体中从头合成的脂肪酸输出到 ER 以进行植物体内脂质生物合成和储存的关键。此外，与各自的对照组相比，A29 和 A32 中 20 个编码糖类、脂类、氨基酸和矿物质转运体的 DEGs 上调，包括推定的钠偶联中性氨基酸转运体 11、钠依赖性二羧酸转运体 SDCS、糖类转运体 SWEET1 和推定的糖磷酸/磷酸盐转运体（图 S19）。其中，SWEET1 被认为能将糖从共生体转移到刺胞动物宿主体内（Maor-Landaw 等人，2020 年；Xiang 等人，2017 年）。
FIGURE 5 (a) Overview of the changes in genes and processes related to algal photosynthesis. The red and blue texts indicate upregulated and downregulated genes and functions in A32 relative to U32, respectively. Heatmaps showing the expression levels of DEGs related to (b) PSII, (c) PSI and cytochrome b6-f complex, (d) light harvesting complex, (e) xanthophyll cycle and C4-pathway, (f) photorespiration and Calvin cycle, (g) starch synthesis and transformation. Refer to Table S7 for the full names of all symbiont DEGs [Colour figure can be viewed at wileyonlinelibrary.com] 图 5 (a) 与藻类光合作用有关的基因和过程的变化概览。红色和蓝色文字分别表示 A32 相对于 U32 上调和下调的基因和功能。热图显示了与(b) PSII、(c) PSI 和细胞色素 b6-f 复合物、(d) 采光复合物、(e) 黄绿素循环和 C4 途径、(f) 光呼吸和卡尔文循环、(g) 淀粉合成和转化相关的 DEGs 表达水平。所有共生体 DEGs 的全称见表 S7 [彩图可在 wileyonlinelibrary.com 上查看]。
4 | DISCUSSION 4 | 讨论
4.1 Shifts in peak planula release, larval TPC and heat tolerance 4.1 鳃丝释放峰值、幼虫 TPC 和耐热性的变化
In the present study, we analysed the effects of adult thermal acclimation on the performance of larval offspring in the reef-building coral P. damicornis. Although heat-acclimated adult P. damicornis exhibited bleaching and compromised metabolic status, corals brooded more larvae with an earlier peak release. Our observation was congruent with multiple previous studies (Crowder et al., 2014; Galanto et al., 2022; McRae et al., 2021), and suggests that the sublethal doses of heat stress accelerates planulation and alters the reproductive investment and timing of larval release. Notably, larvae released 在本研究中，我们分析了造礁珊瑚 P. damicornis 成体热适应对幼体后代表现的影响。虽然热驯化成体 P. damicornis 表现出白化和新陈代谢受损的状态，但珊瑚繁殖了更多的幼虫，并提前达到了释放高峰。我们的观察结果与之前的多项研究（Crowder 等人，2014 年；Galanto 等人，2022 年；McRae 等人，2021 年）一致，表明亚致死剂量的热应力会加速刨根，并改变繁殖投资和幼虫释放的时间。值得注意的是，释放的幼虫
FIGURE 6 Schematic diagram of the key regulations of genes and pathways in Pocillopora damicornis and symbionts (Durusdinium) that could have determined the contrasting thermal tolerance and photosynthetic performance between larvae from control and acclimated adults. Genes and functions in red and blue denote upregulation and downregulation in A32 compared to U32, respectively. Those transporter genes in grey indicate uncharacterized subcellular localizations and functions. The coral transcriptome data suggest that the pronounced upregulation of cellular stress response (including regulations of redox status and cell death, HSP-mediated protein folding, and ER protein quality control) could have been efficient and effective in rescuing host cells from stress in A32 larvae. Consequently, genes associated with cell cycle and mitosis are highly upregulated. Complex changes in symbiont transcriptomic machinery include coordination between light harvesting, photoprotection and carbon fixation, as well as the opposing regulations of catabolic and anabolic pathways that could create a large energy and nutrient pool for the host. Accordingly, both the host and symbionts upregulate various nutrient transporters to facilitate the nutrient transfer from symbionts to the host, thus favouring a functional symbiosis under heat stress. Expression data for all genes are included in supporting information figures and tables [Colour figure can be viewed at wileyonlinelibrary.com] 图 6 Pocillopora damicornis 和共生体（Durusdinium）中基因和通路的关键调控示意图，这些基因和通路可能决定了对照幼体和适应成体幼体之间截然不同的耐热性和光合作用表现。红色和蓝色的基因和功能分别表示 A32 与 U32 相比的上调和下调。灰色的转运体基因表示未表征的亚细胞定位和功能。珊瑚转录组数据表明，细胞应激反应（包括氧化还原状态和细胞死亡调控、HSP介导的蛋白质折叠和ER蛋白质量控制）的明显上调可能有效地将A32幼虫的宿主细胞从应激中解救出来。因此，与细胞周期和有丝分裂相关的基因被高度上调。共生体转录组机制的复杂变化包括光采集、光保护和碳固定之间的协调，以及分解代谢和合成代谢途径的对立调节，这可能会为宿主创造一个巨大的能量和营养池。因此，宿主和共生体都会上调各种营养物质转运体，以促进营养物质从共生体向宿主的转移，从而有利于热胁迫下的功能性共生。所有基因的表达数据都包含在辅助信息图和表中[彩图可在 wileyonlinelibrary.com 上查看]。
by heat-acclimated P. damicornis contained fewer algal symbionts, suggesting that either bleached adults have reduced the vertical transmission of symbionts to their larvae or larvae have undergone bleaching while brooding within parental polyps. Since symbionts in cnidarians can become a major source of harmful reactive oxygen species (ROS) under heat stress (Nielsen et al., 2018; Yakovleva et al., 2009), brooding larvae with fewer symbionts may moderate symbiont-induced harm and confer offspring with benefits to cope with higher temperatures. 大米棘尾藻类中含有较少的藻类共生体，这表明要么是漂白的成虫减少了共生体对幼虫的垂直传播，要么是幼虫在亲本息肉中育雏时经历了漂白。由于在热胁迫下，刺胞动物的共生体可能成为有害活性氧（ROS）的主要来源（Nielsen 等人，2018 年；Yakovleva 等人，2009 年），因此育雏幼体中共生体较少可能会减轻共生体引起的伤害，并使后代在应对较高温度时受益。
Thermal priming of adult P. damicornis corals shifted TPCs of their brooded larval offspring, which was in agreement with Rivera, Chen, et al. (2021) who found that adult exposure to elevated temperatures in the sea anemone Nematostella vectensis altered the survival curves and increased tolerance of their larvae under heat stress. Furthermore, reciprocal transplant experiment demonstrated that heat acclimation of brooding parents led to higher survival, better symbiont photochemical performance and the ability to maintain symbiont densities and autotrophy in their larvae under high temperature compared to those from control parents. Similarly, prior studies showed that preconditioning to high temperatures in symbiotic cnidarians could dampen PSII inactivation and bleaching, and enhance photosynthetic activity when re-exposed to high temperatures (Hawkins & Warner, 2017; Middlebrook et al., 2008; Takahashi et al., 2012; Yu et al., 2020). The enhanced larval tolerance described here most probably stemmed from developmental acclimation, particularly given that larvae were also primed inside the polyp during adult preconditioning. Although we tried to constrain larval development to the experimental period, the timing of gametogenesis was not explicitly studied, and thus we cannot exclude the possibility of any direct parental effects. We found that heat-acclimated parents produced more larvae with similar volume to those in control, and further investigation of the provisioning of energy reserves (e.g., lipids and fatty acid compositions) in larvae could provide more insights into actual parental effects. 达米科尼珊瑚成体的热初始化改变了其育雏幼体后代的 TPCs，这与 Rivera、Chen 等人（2021 年）发现海葵成体暴露于升高的温度改变了其幼体的存活曲线并提高了其对热应力的耐受性一致。此外，相互移植实验表明，与对照亲本的幼体相比，育雏亲本的热适应性可使其幼体在高温下存活率更高、共生体光化学性能更好，并能维持共生体密度和自养能力。同样，先前的研究表明，共生刺胞动物的高温预处理可以抑制 PSII 失活和漂白，并在再次暴露于高温时增强光合作用活性（Hawkins & Warner，2017 年；Middlebrook 等人，2008 年；Takahashi 等人，2012 年；Yu 等人，2020 年）。这里描述的幼虫耐受性增强很可能源于发育适应，特别是考虑到幼虫在成虫预处理期间也在息肉内进行了预处理。虽然我们试图将幼虫的发育限制在实验期间，但配子发生的时间并未明确研究，因此我们不能排除亲本直接影响的可能性。我们发现，热气候条件下的亲本能产出更多体积与对照组相似的幼虫，而进一步研究幼虫体内的能量储备（如脂质和脂肪酸组成）可为了解亲本的实际影响提供更多信息。
Our findings here are in stark contrast to those of McRae et al. (2021) who reported detrimental rather than beneficial effects of adult thermal conditioning on the growth and symbiont photochemical performance of new recruits in the reef coral P. acuta. Although Pocillopora at both study sites predominately harbours the thermally-tolerant Durusdinium (McRae et al., 2022), corals in McRae et al. (2021) were sourced from a chronically warmed reef due to its vicinity to a thermal effluence of the nuclear power plant, and this environmental history could have greatly restricted their capacity for further acclimatization and plasticity. In contrast, corals at our study site experiencing greater seasonal and diurnal fluctuations in temperature may evolve and exhibit higher levels of plasticity (Chevin & Hoffmann, 2017). Second, the differences in thermal sensitivity 我们的研究结果与 McRae 等人（2021 年）的研究结果形成鲜明对比，后者报告了成体热调节对珊瑚礁珊瑚 P. acuta 的生长和新生共生体光化学性能的有害而非有利影响。虽然这两个研究地点的珊瑚虫主要栖息耐高温的Durusdinium（McRae等人，2022年），但McRae等人（2021年）研究的珊瑚来自长期变暖的珊瑚礁，因为该珊瑚礁靠近核电厂的热排放物，这种环境历史可能极大地限制了它们进一步适应环境和可塑性的能力。相比之下，在我们的研究地点，珊瑚经历了更大的季节性和昼夜温度波动，可能会进化并表现出更高水平的可塑性（Chevin 和 Hoffmann，2017 年）。第二，热敏感性的差异
among life stages could also account for these contrasting results, given that the calcifying recruits might be more susceptible to heat stress than larvae. Furthermore, it is also possible that the thermal tolerance conferred by parental acclimation may tend to wane as larvae grow into juveniles (Rivera, Chen, et al., 2021). Clearly, future studies need to examine whether this rapid plasticity could improve the post-settlement tolerance and performance under thermal stress. However, it should be noted that even if the beneficial effect of parental acclimation could not persist into subsequent life stages, it may still help larvae better tolerate and resist the heatwaves, especially in summer months when temperatures are already near their peaks. 鉴于钙化的新生幼体可能比幼体更容易受到热应激的影响，不同生命阶段之间的热耐受性差异也可能是造成这些对比结果的原因。此外，亲本适应所赋予的热耐受性也有可能随着幼体成长为幼体而减弱（Rivera、Chen 等，2021 年）。显然，未来的研究需要考察这种快速可塑性是否能改善定居后的耐受性以及在热应力下的表现。不过，需要注意的是，即使亲本适应的有利影响不能持续到以后的生命阶段，它仍然可以帮助幼虫更好地耐受和抵御热浪，尤其是在气温已经接近峰值的夏季。
Interestingly, the improved thermal tolerance of larvae from heat-acclimated adults was consistently coupled with significantly reduced LEDR, indicative of a potential tradeoff between metabolism and enhanced heat tolerance. In contrast, the basic metabolic demand and aerobic capacity, measured as dark respiration, was maintained. High-temperature acclimation in corals and fish has been related to depressed metabolism and mitochondrial oxidative capacities (Castillo & Helmuth, 2005; Chung & Schulte, 2015). However, transgenerational studies reported that preconditioning of adult fish to warming could completely restore the aerobic scope and mitochondrial capacities in next generations (Donelson et al., 2012; Shama et al., 2014, 2016). Likewise, P. acuta adults that have acclimated to high temperature- produced smaller larvae with lower respiration, but larval size-normalized respiration rates showed compensation when re-exposed (Putnam & Gates, 2015). However, this was not the case in our study where larval size was unaffected by adult acclimation. Furthermore, we found that larvae and adult corals showed opposite respiratory responses to heat acclimation, which could be due to the distinct tissue organization, physiology and energy needs between life stages. 有趣的是，热适应成虫幼体耐热性的提高始终与发光二极管还原率的显著降低相关联，这表明新陈代谢与耐热性提高之间可能存在权衡。与此相反，基本代谢需求和有氧能力（以黑暗呼吸衡量）得以维持。珊瑚和鱼类的高温适应与新陈代谢和线粒体氧化能力下降有关（Castillo 和 Helmuth，2005 年；Chung 和 Schulte，2015 年）。然而，跨代研究报告称，对成鱼进行升温预处理可完全恢复下一代的有氧范围和线粒体能力（Donelson 等人，2012 年；Shama 等人，2014 年，2016 年）。同样，适应了高温的 P. acuta 成鱼 ，其幼鱼体型较小，呼吸作用较低，但幼鱼体型正常化后的呼吸率在再次暴露时显示出补偿作用（Putnam 和 Gates，2015 年）。然而，在我们的研究中情况并非如此，幼虫的大小不受成虫适应性的影响。此外，我们发现幼体和成体珊瑚对热适应表现出相反的呼吸反应，这可能是由于生命阶段之间不同的组织结构、生理和能量需求造成的。
The depressed metabolism in larvae from heat-acclimated adults appeared unlikely to arise from the deprivation of larval energy reserves, given the higher in A29 and A32. Instead, this metabolic adjustment could provide an apparent acclimation of symbiont photosynthesis and overall holobiont fitness by reducing energy depletion. Similarly, bleached coral Montipora capitata from Hawai'i depressed LEDR during heatwaves, but their metabolic rates recovered in few weeks after the heatwave (Innis et al., 2021). Heat-induced metabolic depression is a common adaptive response in intertidal organisms that reduces the costs of living at high temperatures and confers tolerance to harsh environments (Liao et al., 2021; Marshall & McQuaid, 2011). Therefore, the observed reduction in LEDR here could be an acclimation strategy to improve energy balance, extend larval persistence in a high-temperature environment, and increase the chances of survival as conditions improved. 考虑到 A29 和 A32 中较高的 ，热适应成虫的幼虫新陈代谢降低似乎不太可能是由于幼虫能量储备被剥夺所致。相反，这种新陈代谢调整可以通过减少能量消耗，明显改善共生体的光合作用和整体适应性。同样，来自夏威夷的漂白珊瑚 Montipora capitata 在热浪期间的发光二级管减少，但它们的新陈代谢率在热浪过后几周内就恢复了（Innis 等人，2021 年）。热引起的代谢抑制是潮间带生物常见的适应性反应，可降低在高温下生活的成本，并赋予其对恶劣环境的耐受性（Liao 等人，2021 年；Marshall 和 McQuaid，2011 年）。因此，这里观察到的发光潜能值降低可能是一种适应策略，以改善能量平衡，延长幼虫在高温环境中的存活时间，并在条件改善时增加存活机会。
Cellular mechanisms, such as redox regulation, molecular chaperones, ER stress and immune response, are a series of conserved and forefront processes to offset the deleterious effects of heat stress, termed heat stress responses (HSR) (Richter et al., 2010). Two main molecular HSR pathways, transcriptional frontloading and plasticity, have been proposed as potential mechanisms for enhanced heat tolerance of reef corals (Barshis et al., 2013; Kenkel & Matz, 2016), whereas one recent study suggested a combined strategy (BrenerRaffalli et al., 2022). In our study, the transcriptional HSR was more heat-responsive in larvae from heat-acclimated adults. Rather than a direct heat response and increased loading of cellular defence transcripts from parents, the most plausible explanation is that heat acclimation could have activated cellular stress responses in developing larvae while brooding within the adult polyp cavity. Likewise, Rivera, Chen, et al. (2021) also found that larvae from the heatprimed anemone . vectensis exhibited higher expression levels of stress-responsive genes (including HSP70). In our study, when returned to ambient temperature, this higher "baseline" expression could have decayed but still maintained at a level higher than the larvae from control adults; however, HSR that were already present at high levels remained active if heat persisted, thus shaping such a more plastic transcriptional reaction norm. In contrast, Kitchen et al. (2022) showed that heat stress greatly reduced the magnitude of transcriptional HSR in symbiotic A. digitifera larvae, thus decreasing larval survival. This contrasting response reinforced the notion that the capacity of mounting a strong and full HSR, either in a plastic and/or frontloading manner, could be key for coral thermal resilience (Barshis et al., 2013; Brener-Raffalli et al., 2022; Kenkel & Matz, 2016). 氧化还原调节、分子伴侣、ER应激和免疫反应等细胞机制是一系列抵消热应激有害影响的保守前沿过程，被称为热应激反应（HSR）（Richter等人，2010年）。转录前负荷和可塑性这两种主要的分子 HSR 途径被认为是增强珊瑚礁珊瑚耐热性的潜在机制（Barshis 等人，2013 年；Kenkel & Matz，2016 年），而最近的一项研究则提出了一种综合策略（BrenerRaffalli 等人，2022 年）。在我们的研究中，来自热螯合成虫的幼虫的转录 HSR 对热的反应更强。最合理的解释是，在成虫息肉腔内育雏时，热适应可能激活了发育中幼虫的细胞应激反应，而不是直接的热反应和亲本细胞防御转录本负载的增加。同样，Rivera、Chen 等人（2021 年）也发现，来自热刺海葵 . vectensis 的幼虫表现出较高的应激反应基因（包括 HSP70）表达水平。在我们的研究中，当恢复到环境温度时，这种较高的 "基线 "表达可能会衰减，但仍能维持在高于对照成体幼虫的水平；然而，如果持续受热，已经存在于高水平的 HSR 仍会保持活跃，从而形成这种更具可塑性的转录反应规范。与此相反，Kitchen 等人（2022 年）的研究表明，热胁迫大大降低了共生 A. digitifera 幼虫转录 HSR 的水平，从而降低了幼虫的存活率。这种截然不同的反应强化了一个概念，即以可塑性和/或前负荷方式启动强大而全面的 HSR 的能力可能是珊瑚热复原力的关键（Barshis 等人，2013 年；Brener-Raffalli 等人，2022 年；Kenkel & Matz，2016 年）。
For corals under heat stress, activation of the antioxidative system, protein folding, and ER stress response are thought to be the first line of defence in detoxifying ROS, regulating cellular redox state, and dealing with protein folding problems, as transcriptomic changes related to these processes are commonly observed in heatstressed and bleached cnidarians (Cleves et al., 2020; Maor-Landaw et al., 2014; Wuitchik et al., 2021). In line with these findings, our study found upregulation of several anti-oxidative genes, which have also been reported previously (Barshis et al., 2013; Cleves et al., 2020; Louis et al., 2017). Furthermore, genes related to protein folding, UPR and ERAD usually showed a rapid upregulation in symbiotic cnidarians during early heat exposure, which declined to baseline levels when bleaching was evident (Cleves et al., 2020; Maor-Landaw et al., 2014). Nevertheless, our study showed that this set of genes remained unresponsive to heat stress in those bleached larvae from control parents, whereas they were maintained at high expression levels in heat-exposed but unbleached larvae from heat-acclimated adults. This expression pattern could ensure efficient and continuous disposing of misfolded proteins to buffer ER stress in heat-exposed larvae from heat-acclimated adults (Figure 6), hence re-establishing cellular homeostasis and protein function (Hetz, 2012; Walter & Ron, 2011). 对于热应激下的珊瑚而言，抗氧化系统、蛋白质折叠和ER应激反应的激活被认为是解毒ROS、调节细胞氧化还原状态和处理蛋白质折叠问题的第一道防线，因为在热应激和漂白的刺胞动物中通常会观察到与这些过程相关的转录组变化（Cleves等人，2020年；Maor-Landaw等人，2014年；Wuitchik等人，2021年）。与这些发现一致，我们的研究发现了一些抗氧化基因的上调，这些基因以前也有报道（Barshis 等人，2013 年；Cleves 等人，2020 年；Louis 等人，2017 年）。此外，与蛋白质折叠、UPR 和 ERAD 相关的基因通常会在共生刺胞动物早期受热时迅速上调，而当漂白现象明显时，这些基因又会下降到基线水平（Cleves 等人，2020 年；Maor-Landaw 等人，2014 年）。然而，我们的研究表明，在那些来自对照亲本的白化幼体中，这组基因对热应力仍然没有反应，而在来自热适应成体的暴露于热但未白化的幼体中，这些基因则维持在高表达水平。这种表达模式可确保有效、持续地处置错误折叠的蛋白质，以缓冲来自热螯合成虫的暴露于热环境的幼虫体内的ER应激（图6），从而重建细胞平衡和蛋白质功能（Hetz，2012；Walter & Ron，2011）。
Generally, ER stress responses are adaptive reactions that promote cell survival under heat stress, however, if homoeostasis cannot be restored, unmitigated ER stress will trigger PCD (Hetz, 2012). In the model of oxidative theory of bleaching, the 一般来说，ER应激反应是促进细胞在热应激下存活的适应性反应，但是，如果不能恢复平衡，不加缓解的ER应激就会引发多核衰变（Hetz，2012）。在氧化漂白理论模型中，ER
activation of PCD plays a central role in symbiont expulsion and cnidarian thermal bleaching (Weis, 2008), and studies have verified its roles in inducing bleaching (Li et al., 2021; Pernice et al., 2011; Tchernov et al., 2011). Surprisingly, we found almost equivalent upregulation of both prosurvival and prodeath genes, as well as genes with dual roles in promoting and opposing PCD in A32 larvae (Figure 6). The enhanced heat tolerance of corals after environmental preconditioning is linked to the modulations in PCD pathways, either through constitutive frontloading of genes involved in cell death regulation (Barshis et al., 2013), the upregulation of antideath genes (Bellantuono et al., 2012), or by increasing the expression ratio of key prosurvival to prodeath genes (Majerova et al., 2021). The co-upregulation pattern and flexible regulatory mechanism observed herein suggests active regulation of PCD and a delicate balance between cell survival and death, which could facilitate the timely clearance of thermally-damaged cells, but also block PCD in surviving cells by upregulating the prosurvival genes, hence promoting cell viability and survival under heat stress (Ainsworth et al., 2011; Pernice et al., 2011). 激活 PCD 在共生体驱逐和刺胞动物热白化过程中起着核心作用（Weis，2008 年），相关研究已经验证了它在诱导白化过程中的作用（Li 等人，2021 年；Pernice 等人，2011 年；Tchernov 等人，2011 年）。令人惊讶的是，我们发现在 A32 幼体中，促生存基因和促死亡基因以及在促进和对抗 PCD 方面具有双重作用的基因的上调量几乎相当（图 6）。珊瑚在环境预处理后的耐热性增强与 PCD 通路的调节有关，这可能是通过参与细胞死亡调控的基因构成性前置（Barshis 等人，2013 年）、抗凋亡基因的上调（Bellantuono 等人，2012 年）或通过增加关键的促存活基因与促凋亡基因的表达比（Majerova 等人，2021 年）实现的。本研究观察到的共调模式和灵活的调控机制表明，细胞存活与死亡之间存在一种微妙的平衡关系，即细胞存活与死亡之间存在一种微妙的平衡关系，这种平衡关系既能促进及时清除热损伤细胞，又能通过上调促存活基因阻止存活细胞中的细胞存活与死亡，从而促进细胞在热胁迫下的存活能力和存活率（Ainsworth 等人，2011 年；Pernice 等人，2011 年）。
If cellular stress is not relieved at later HSR stage, cell cycle and proliferation are arrested and stagnated. However, we noted widespread upregulation of over 350 key genes involved in cell cycle and mitosis in A32, implying that heat acclimation could have promoted cell proliferation and larval development and thus earlier larval release in heat-acclimated adults. Conversely, most previous studies reported cell cycle arrest and cell proliferation suppression in corals under high temperatures (DeSalvo et al., 2010; MaorLandaw et al., 2014; Poquita-Du et al., 2019). For instance, Kitchen et al. (2022) found that heat stress resulted in a nonreversible and permanent cell cycle arrest in symbiotic A. digitifera larvae, a state similar to cellular senescence. Therefore, our results indicate that the concerted and strong transcriptional HSR in larvae from heatacclimated adults could have been effective in rescuing host cells from stress, hence favouring cell cycle transitions and division (Figure 6). Cell division is the fundamental process that allows eukaryotic organisms to renew, repair and grow their tissues, and host cell cycle regulation has been suggested as a primary mechanism to govern symbiont density and sustain symbiosis in cnidarians (Gorman et al., 2022; Rivera & Davies, 2021; Tivey et al., 2020). The transcriptional signatures of accelerated host cell cycle and mitosis not only imply a faster self-renewal and turnover of host cells but also a potentially greater capacity to maintain symbiosis, which is further reflected in the enhanced heat tolerance and the maintenance of symbiont population in A32 larvae. 如果细胞应激在 HSR 后期得不到缓解，细胞周期和增殖就会停止和停滞。然而，我们注意到 A32 中涉及细胞周期和有丝分裂的 350 多个关键基因普遍上调，这意味着热适应可能促进了细胞增殖和幼体发育，从而使热适应成体的幼体提前释放。相反，之前的大多数研究都报告了高温条件下珊瑚细胞周期的停滞和细胞增殖的抑制（DeSalvo 等人，2010 年；MaorLandaw 等人，2014 年；Poquita-Du 等人，2019 年）。例如，Kitchen 等人（2022 年）发现，热应力导致共生的 A. digitifera 幼虫细胞周期出现不可逆的永久性停滞，这种状态类似于细胞衰老。因此，我们的研究结果表明，在来自耐热成虫的幼虫体内，协同而强大的转录 HSR 可有效地将宿主细胞从胁迫中解救出来，从而有利于细胞周期的转换和分裂（图 6）。细胞分裂是真核生物更新、修复和生长组织的基本过程，宿主细胞周期调控被认为是控制共生体密度和维持刺丝胞动物共生的主要机制（Gorman 等，2022 年；Rivera & Davies，2021 年；Tivey 等，2020 年）。宿主细胞周期和有丝分裂加速的转录特征不仅意味着宿主细胞自我更新和更替的速度加快，还意味着维持共生的能力可能增强，这进一步反映在 A32 幼虫耐热性的增强和共生体数量的维持上。
4.3 Coordination between light harvesting, photoprotection and carbon fixation in algal symbionts 4.3 藻类共生体采光、光保护和碳固定之间的协调
Although the comparable symbiont densities of larvae in U32 and A32 denoted similar internal light fields, symbionts from heatacclimated adults experienced a longer exposure to high light due to adult bleaching. High light conditions usually lead to excessive light absorption by LHC and over excitation of PSII. NPQ is an important protective mechanism to dissipate the excess excitation energy, which is controlled by LHCSR proteins and the xanthophyll cycling kinetics in microalgae (Blommaert et al., 2017). Interestingly, symbionts in U32 upregulated LHC and LHCSR genes, which was consistent with the increased NPQ and values in U32, suggesting that the light energy absorbed by LHC antenna had greatly exceeded the capacity of photochemical reactions and LHCSR-dependent NPQ has been activated in U32 as a photoprotective mechanism to dissipate the excess excitation energy (Petroutsos et al., 2016). 虽然 U32 和 A32 中幼虫的共生体密度相当，表明其内部光场相似，但由于成虫漂白，热适生成虫的共生体暴露在强光下的时间更长。强光条件通常会导致 LHC 吸收过多的光，并导致 PSII 过度激发。NPQ 是消散过量激发能量的重要保护机制，它受 LHCSR 蛋白和微藻中黄绿素循环动力学的控制（Blommaert 等人，2017 年）。有趣的是，U32 中的共生体上调了 LHC 和 LHCSR 基因，这与 U32 中增加的 NPQ 和 值一致，表明 LHC 天线吸收的光能已大大超过了光化学反应的能力，依赖于 LHCSR 的 NPQ 在 U32 中被激活，作为一种光保护机制来耗散多余的激发能量（Petroutsos 等人，2016 年）。
In contrast, symbionts from heat-acclimated adults did not upregulate the LHC genes, suggesting a control of antenna size (Figure 6). This could help avoid excessive light absorption and reduce the kinetic constraints between rates of light capture and the downstream energy transfer and conversion, thus limiting the risk of photoinhibition and rendering photochemical reactions more efficient (Negi et al., 2020). Furthermore, symbionts in A32 upregulated the two key enzyme genes (VDE and ZEP) implicated in xanthophyll cycle (Figure 6), indicating faster xanthophyll cycling kinetics which could rapidly switch NPQ on and off for relaxation (Blommaert et al., 2017). Indeed, these transcriptomic signatures were manifested in higher but lower NPQ and of symbionts in A32. 与此相反，来自热适应性成虫的共生体没有上调 LHC 基因，这表明对触角大小的控制（图 6）。这有助于避免过度的光吸收，减少光捕获率与下游能量转移和转换率之间的动力学限制，从而限制光抑制的风险，提高光化学反应的效率（Negi 等人，2020 年）。此外，A32 中的共生体上调了与黄绿素循环有关的两个关键酶基因（VDE 和 ZEP）（图 6），这表明黄绿素循环动力学速度更快，可以快速开关 NPQ 以实现弛豫（Blommaert 等人，2017 年）。事实上，这些转录组特征在 A32 中表现为较高的 ，但较低的 NPQ 和共生体 。
Thermally-induced PSII photoinhibition and bleaching in symbiotic corals is primarily attributed to the perturbation of PSII protein D1 turnover rates and the impairment in PSII repair cycle (Warner et al., 1999). Unexpectedly, PSII protein D1 gene was upregulated by 5.7-fold in A32, suggesting a faster de novo synthesis and thus increased supply of newly synthesized D1 protein for the efficient repair of PSII reaction centres to evade photodamage and photoinhibition (Takahashi et al., 2009). Hence, symbiont in U32 and A32 mounted contrasting photoreception and photoprotective mechanisms, possibly as a result of the acclimation to differential in hospite light and temperature conditions while brooding within adults. 在共生珊瑚中，热引起的 PSII 光抑制和白化主要归因于 PSII 蛋白 D1 的周转率受到干扰和 PSII 修复周期受损（Warner 等人，1999 年）。意外的是，A32 中的 PSII 蛋白 D1 基因上调了 5.7 倍，这表明新合成的 D1 蛋白合成速度加快，从而增加了新合成的 D1 蛋白的供应量，以有效修复 PSII 反应中心，避免光损伤和光抑制（Takahashi 等人，2009 年）。因此，U32 和 A32 中的共生体具有截然不同的光感知和光保护机制，这可能是成虫育雏时适应不同光照和温度条件的结果。
Notably, symbionts in A32 also upregulated genes encoding transporters and enzymes associated with algal CCMs, including SLC4 inorganic carbon (Ci) transporters and those key enzymes (PEPCK, NADP-ME, and PPDK) involved in C4 pathway, thus indicating a certain degree of cooperation between algal and host CCMs in photosynthetic acquisition (Figure 6). Although the unicellular algae lack the typical Kranz anatomy (bundle sheath and mesophyll cells) for the spatial separation of fixation and release, the performance of a C4-like pathway and photosynthesis is commonly recognized in diatoms and dinoflagellates, including Symbiodiniaceae from cnidarians (Reinfelder et al., 2000; Tytler et al., 1986; Zhang et al., 2021). The co-upregulation of PEPCK and NADP-ME subtypes in suggests higher efficiency in the carboxylation process to enrich in the vicinity of Rubisco and suppress the oxygenase function of Rubisco and the photorespiratory activity (Timm & Hagemann, 2020). In turn, symbiont genes involved in Calvin cycle and starch synthesis exhibited higher expression in A32, while the key genes (such as PGLP and GLYK) implicated in the wasteful photorespiratory C2 pathway that competes with Calvin cycle were 值得注意的是，A32中的共生体还上调了编码与藻类CCM相关的转运体和酶的基因，包括SLC4无机碳（Ci）转运体和参与C4途径的关键酶（PEPCK、NADP-ME和PPDK），从而表明藻类和宿主CCM在光合 （图6）。虽然单细胞藻类缺乏典型的克兰兹（Kranz）解剖结构（束鞘和叶肉细胞）来实现 固定和释放的空间分离，但硅藻和甲藻，包括刺胞藻中的共生藻科（Symbiodiniaceae），通常都能实现类似 C4 的途径和光合作用（Reinfelder 等人，2000 年；Tytler 等人，1986 年；Zhang 等人，2021 年）。 中 PEPCK 和 NADP-ME 亚型的共同调控表明，羧化过程的效率更高，可富集 Rubisco 附近的 ，并抑制 Rubisco 的加氧酶功能和光呼吸活性（Timm 和 Hagemann，2020）。反过来，参与卡尔文循环和淀粉合成的共生基因在 A32 中表现出更高的表达量，而与卡尔文循环竞争的浪费光呼吸 C2 通路相关的关键基因（如 PGLP 和 GLYK）在 A32 中的表达量则较低。
downregulated in A32 compared to U32 (Figure 6). These findings point to greater capacity in carbon fixation and energy conversion in symbionts when thermal conditions of parental brooding and pelagic phase were correlated. Likewise, Buerger et al. (2020) found that artificially heat-evolved Symbiodiniaceae upregulated carbon fixation genes when hosted in coral larvae under heat stress. Overall, these photosynthesis-related transcriptional modifications suggest that after prior thermal acclimation, symbionts finetune photoreception, photoprotection and carbon fixation (Figure 6), thereby improving photosynthetic performance and yield under high temperature. 图 6）。这些发现表明，当亲代育雏和浮游阶段的热条件相关时，共生体的碳固定和能量转换能力更强。同样，Buerger 等人（2020 年）发现，人工热进化的共生藻寄居在热应力下的珊瑚幼虫体内时，碳固定基因会上调。总之，这些与光合作用相关的转录修饰表明，在事先进行热适应后，共生体会对光感知、光保护和碳固定进行微调（图 6），从而提高高温下的光合作用性能和产量。
Adult acclimation led to the downregulation of symbiont genes related to mitochondrial function and degradation pathways for key cellular energy substrates (Figure 6), indicating a decreased symbiont metabolic activity which could have contributed to depressed holobiont LEDR. Nonetheless, symbionts in A32 showed upregulation of genes involved in starch and lipid biosynthesis, suggesting opposing regulations of catabolic and anabolic processes under heat stress (Figure 6). Such a metabolic shift driven by adult acclimation is expected to result in increased conservation and greater pools of photosynthates in symbionts that could be available to the host. In contrast, symbionts in U32 upregulated repertoires of genes related to inorganic nitrogen cycling, amino acid biosynthesis and degradation, reflecting a higher dependence on amino acid metabolism to sustain energy requirement. Furthermore, in accordance with upregulation of nitrogen compound metabolic activity of symbionts in U32, host DEGs that were specifically downregulated in U32 had a corresponding enrichment in cellular amino acid catabolic process, suggesting that symbionts in U32 could have sequestered more nitrogen compounds for their own use instead of translocating them to the host, that is, less beneficial symbionts but still tightly-coupled metabolic integration. In line with Baker et al. (2018), our findings suggest that elevated temperature stimulates the selfish retention of nutrients by algal symbionts and promotes symbiont parasitism in larvae from control adults. 成体适应导致与线粒体功能和关键细胞能量底物降解途径有关的共生体基因下调（图 6），表明共生体代谢活动减少，这可能是导致全生物体发光二级管减少的原因之一。然而，A32 中的共生体显示出参与淀粉和脂质生物合成的基因上调，这表明热胁迫下分解代谢和合成代谢过程的调控是相反的（图 6）。这种由成虫适应性驱动的新陈代谢转变预计会导致共生体中可用于宿主的光合产物的保存和储备增加。与此相反，U32 中的共生体上调了与无机氮循环、氨基酸生物合成和降解相关的基因重组，这反映了共生体更依赖氨基酸代谢来维持能量需求。此外，与 U32 中共生体氮化合物代谢活性的上调一致，在 U32 中被特异性下调的宿主 DEGs 在细胞氨基酸分解代谢过程中也有相应的富集，这表明 U32 中的共生体可能螯合了更多的氮化合物供自身使用，而不是将其转运给宿主，即共生体的获益较少，但代谢整合仍然紧密耦合。与贝克等人（2018）的观点一致，我们的研究结果表明，温度升高会刺激藻类共生体自私地保留营养物质，并促进共生体在对照成虫幼体中的寄生。
Most importantly, our study revealed the upregulation of many transporter genes for various nutrients and metabolites in both host and symbionts from A32. The upregulation of nutrient transporters has been widely observed in cnidarian hosts when becoming symbiotic as well as symbionts transiting from the free-living to an endosymbiotic state, indicating active nutritional fluxes between the cnidarian hosts and symbionts after symbiosis establishment (Bellantuono et al., 2019; Lehnert et al., 2014; Maor-Landaw et al., 2020; Mohamed et al., 2020). Although many of these differentially expressed transporter genes in our study have not yet been characterized with regard to their subcellular localizations and specific functions, we found several host and symbiont genes that are specifically implicated in transporting sugar, lipids, and monocarboxylates from symbionts to the host. Specifically, the upregulation of transporters such as ABC transporters, SLC5s, NPC1, SLC16s and SWEET1 suggests that the coral host is actively receiving and incorporating nutrients from symbionts (Figure 6), which together with the alterations of symbiont metabolic status indicates a positive feedback loop in interpartner metabolic interactions after adult acclimation. Maintaining high rates of nutrient translocation and transfer in coral holobiont is crucial to the stability of symbiosis and potentially thermal bleaching resilience (Rädecker et al., 2021), and this principle held true for A32 larvae with transcriptional signals of enhanced photosynthate transfer and higher bleaching tolerance. Collectively, our findings suggest that heat acclimation could facilitate host-symbiont pairings in nutrient translocation and support the symbiotic relationship in larval P. damicornis holobiont under heat stress (Figure 6). 最重要的是，我们的研究揭示了 A32 宿主和共生体中多种营养物质和代谢物转运体基因的上调。营养物质转运体的上调已在成为共生体的刺胞动物宿主以及从自由生活状态过渡到内共生状态的共生体中被广泛观察到，这表明共生体建立后，刺胞动物宿主与共生体之间的营养通量活跃（Bellantuono 等人，2019 年；Lehnert 等人，2014 年；Maor-Landaw 等人，2020 年；Mohamed 等人，2020 年）。尽管在我们的研究中，许多差异表达的转运体基因尚未确定其亚细胞定位和特定功能，但我们发现了几个与从共生体向宿主转运糖类、脂类和单羧酸盐有关的宿主和共生体基因。具体来说，ABC 转运体、SLC5s、NPC1、SLC16s 和 SWEET1 等转运体的上调表明，珊瑚宿主正在积极接收和吸收共生体的营养物质（图 6），这与共生体代谢状态的改变一起表明，成体适应后，伙伴间的代谢相互作用形成了正反馈回路。在珊瑚全生物体中保持较高的营养物质转译和转移率对于共生的稳定性和潜在的热白化复原力至关重要（Rädecker 等人，2021 年），这一原则在 A32 幼虫身上也得到了验证，其转录信号表明光合作用转移增强，白化耐受力提高。总之，我们的研究结果表明，热适应可以促进宿主-共生体在营养物质转运方面的配对，并支持热胁迫下大菱鲆幼虫全共生体的共生关系（图 6）。
4.5 | Summary and implications for coral resilience under future warming 4.5 | 总结及未来气候变暖对珊瑚复原力的影响
Overall, we showed that heat acclimation of the brooding coral . damicornis rapidly shifted the thermal reaction norms of their larval offspring and resulted in higher survivorship, bleaching resistance and better photochemical performance of endosymbionts in heat-exposed larvae from heat-acclimated adults. RNA-seq analysis revealed strong effects of heat acclimation on the transcriptomic landscapes of the host and symbionts in larvae under heat stress. Specifically, larvae from heat-acclimated adults exhibited higher baseline expression and greater plasticity in host genes involved in cellular stress response, cell cycle, and nutrient transporting upon heat exposure, which could be the key to heat tolerance and symbiosis maintenance. After heat acclimation, endosymbionts coordinated light harvesting, photoprotection and carbon fixation to optimize photochemical efficiency and photosynthetic yield under heat stress. Furthermore, thermal stress renders symbionts less beneficial to their coral host in larvae from control parents, as indicated by the upregulation of symbiont amino acid metabolism and the concomitant downregulation of amino acid catabolic process in the host. In contrast, adult heat acclimation modified the catabolic and anabolic pathways for energy substrates in symbionts, and facilitated the nutrient transfer from symbionts to the host, thus favouring a functional symbiosis in larvae from heat-acclimated parents. These findings reveal the adaptive transcriptional changes of the host and symbionts due to parental and/or developmental thermal acclimation (Figure 6). 总之，我们的研究表明，育雏珊瑚 . damicornis 的热适应迅速改变了其幼体后代的热反应规范，并导致热暴露幼体的存活率更高、抗白化能力更强以及内生共生体的光化学性能更好。RNA-seq分析显示，热适应对热胁迫下幼虫宿主和共生体的转录组景观有很大影响。具体而言，来自热螯合成虫的幼虫表现出更高的基线表达量，并且在暴露于热环境时，涉及细胞应激反应、细胞周期和营养运输的宿主基因具有更大的可塑性，这可能是耐热性和共生关系维持的关键。经过热适应后，内生共生体会协调采光、光保护和碳固定，以优化热胁迫下的光化学效率和光合产量。此外，在对照亲本的幼虫体内，热胁迫会降低共生体对珊瑚宿主的益处，这表现在共生体氨基酸代谢的上调和宿主体内氨基酸分解代谢过程的下调。相反，成虫的热适应改变了共生体中能量底物的分解代谢和合成代谢途径，促进了共生体向宿主的营养转移，从而有利于热适应亲本幼虫的功能性共生。这些发现揭示了宿主和共生体因亲本和/或发育过程中的热适应而发生的适应性转录变化（图 6）。
The observed plasticity and resilience of larvae after parental preconditioning could be direct consequences of host and symbiont acclimation to heat stress while developing within parental polyps. Given that the in situ thermal pulse and the resultant preconditioning events associated with marine heatwaves will become more frequent under climate change, our findings suggest that adaptive plasticity might have great potential to fuel resilience by complementing genetic adaptation to facilitate population persistence, at least for the fast-brooding coral species studied here. 观察到的幼虫在亲本预处理后的可塑性和恢复力可能是寄主和共生体在亲本息肉中发育时适应热应力的直接结果。鉴于在气候变化的情况下，与海洋热浪相关的原地热脉冲和由此产生的预处理事件将变得更加频繁，我们的研究结果表明，适应性可塑性可能具有很大的潜力，通过补充遗传适应来促进种群的持久性，至少对本文研究的快速萌发珊瑚物种是如此。
However, the increased frequency of heat waves may also greatly undermine and even reverse this beneficial effect. Notably, the improved thermal tolerance of larval offspring after parental and/ or developmental acclimation was accompanied by consistent reductions in holobiont metabolism, suggesting a status of metabolic depression and thus potential tradeoffs. Nevertheless, whether this metabolic depression is a prerequisite for the enhanced heat tolerance and if this tradeoff is consistent across life stages and different species remain unknown. Although this metabolic depression induced by acclimation may allow temporal tolerance of high-temperature conditions in larvae, the reduced metabolic activity could be maladaptive in the long term and translate into negative repercussions for organismal performance characteristics, such as larval settlement, post-settlement growth, reproductive maturation, and fecundity. Consequently, our results also highlight the importance of curbing carbon emissions and dealing with the root cause of climate change to safeguard the future of reef corals and the reef ecosystems. 然而，热浪频率的增加也可能会大大削弱甚至逆转这种有利影响。值得注意的是，经过亲代和/或发育适应后，幼虫后代的耐热性提高的同时，全生物体的新陈代谢也在持续降低，这表明存在代谢抑制的情况，因此可能存在权衡。然而，这种新陈代谢抑制是否是增强耐热性的先决条件，以及这种权衡在不同生命阶段和不同物种之间是否一致，仍然是未知数。虽然适应性诱导的代谢抑制可能使幼虫暂时耐受高温条件，但代谢活动的降低可能会产生长期的不适应，并对生物体的表现特征（如幼虫定居、定居后生长、生殖成熟和繁殖力）产生负面影响。因此，我们的研究结果也凸显了遏制碳排放和应对气候变化根源的重要性，以保护珊瑚礁珊瑚和珊瑚礁生态系统的未来。
ACKNOWLEDGEMENTS 致谢
This work was supported by the National Key Research and Development Program (2021YFF0502804 and 2021YFC3100504), National Natural Science Foundation of China (42106115 and 41906097), and Science and Technology Planning Project of Guangdong Province, China (2020B1212060058). Dr Lei Jiang was supported by Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou) (SMSEGL20SC01) as a visiting scholar in HKB, HKUST. 本研究得到国家重点研发计划（2021YFF0502804 和 2021YFC3100504）、国家自然科学基金（42106115 和 41906097）和广东省科技计划项目（2020B1212060058）的资助。蒋磊博士作为访问学者获得南方海洋科学与工程广东实验室（广州）（SMSEGL20SC01）的支持。
AUTHOR CONTRIBUTIONS 作者贡献
Lei Jiang and Hui Huang designed the research. Lei Jiang and ChengYue Liu conducted the experiments and collected the samles. Lei Jiang, Cheng-Yue Liu, Guoxin Cui, Manuel Aranda, Pei-Yuan Qian and Hui Huang performed the analyses and drafted the manuscript. Lin-Tao Huang, Xiao-Lei Yu, You-Fang Sun, Hao-Ya Tong, Guo-Wei Zhou, Xiang-Cheng Yuan, Yi-Si Hu and Wen-Liang Zhou contributed to lab analysis and reviewed the manuscript. All authors critically revised the manuscript and gave final consent for publication. 蒋磊和黄慧设计了该研究。蒋磊和刘成月进行了实验并收集了样本。蒋磊、刘成跃、崔国新、Manuel Aranda、钱培元和黄辉进行了分析并起草了手稿。黄林涛、于晓雷、孙友芳、佟浩亚、周国伟、袁湘成、胡怡思和周文亮参与了实验室分析并审阅了稿件。所有作者对稿件进行了严格修改，并最终同意发表。
CONFLICT OF INTEREST 利益冲突
On behalf of all authors, the corresponding authors state that there is no conflict of interest. 通讯作者代表所有作者声明不存在利益冲突。
DATA AVAILABILITY STATEMENT 数据可用性声明
All data sets associated with this study are included in the manuscript and the electronic Supporting Information. The RNA-seq raw data have been submitted to NCBI under the BioProject accession numbers: PRJNA839911. 本研究的所有相关数据集均包含在手稿和电子版辅助信息中。RNA-seq 原始数据已提交给 NCBI，生物项目编号为PRJNA839911.
Ainsworth, T. D., Wasmund, K., Ukani, L., Seneca, F., Yellowlees, D., Miller, D., & Leggat, W. (2011). Defining the tipping point. A complex cellular life/death balance in corals in response to stress. Scientific Reports, 1(1), 160. Ainsworth, T. D., Wasmund, K., Ukani, L., Seneca, F., Yellowlees, D., Miller, D., & Leggat, W. (2011).确定临界点。珊瑚应对压力时复杂的细胞生死平衡。科学报告》，1（1），160。
Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L., & Knowlton, N. (2018). Climate change promotes parasitism in a coral symbiosis. The ISME Journal, 12(3), 921-930. https://doi.org/10.1038/s4139 6-018-0046-8 Baker, D. M., Freeman, C. J., Wong, J. C. Y., Fogel, M. L., & Knowlton, N. (2018).气候变化促进珊瑚共生中的寄生。ISME 期刊，12（3），921-930。https://doi.org/10.1038/s4139 6-018-0046-8
Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor-Knowles, N., & Palumbi, S. R. (2013). Genomic basis for coral resilience to climate change. Proceedings of the National Academy of Sciences, 110(4), 1387-1392. https://doi.org/10.1073/pnas. 1210224110 Barshis, D. J., Ladner, J. T., Oliver, T. A., Seneca, F. O., Traylor-Knowles, N., & Palumbi, S. R. (2013)。珊瑚抵御气候变化的基因组基础。美国国家科学院院刊》，110（4），1387-1392。https://doi.org/10.1073/pnas. 1210224110
Bellantuono, A. J., Dougan, K. E., Granados-Cifuentes, C., & RodriguezLanetty, M. (2019). Free-living and symbiotic lifestyles of a thermotolerant coral endosymbiont display profoundly distinct transcriptomes under both stable and heat stress conditions. Molecular Ecology, 28(24), 5265-5281. https://doi.org/10.1111/mec. 15300 Bellantuono, A. J., Dougan, K. E., Granados-Cifuentes, C., & RodriguezLanetty, M. (2019).一种耐热珊瑚内共生体的自由生活方式和共生生活方式在稳定和热应力条件下显示出截然不同的转录组。分子生态学》，28（24），5265-5281。https://doi.org/10.1111/mec。15300
Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O., & Rodriguez-Lanetty, M. (2012). Coral thermal tolerance: Tuning gene expression to resist thermal stress. PLoS One, 7(11), e50685. https://doi.org/10.1371/journal.pone. 0050685 Bellantuono, A. J., Granados-Cifuentes, C., Miller, D. J., Hoegh-Guldberg, O., & Rodriguez-Lanetty, M. (2012).珊瑚的耐热性：调整基因表达以抵御热应力。PLoS One, 7(11), e50685. https://doi.org/10.1371/journal.pone.0050685
Bellworthy, J., Menoud, M., Krueger, T., Meibom, A., & Fine, M. (2019). Developmental carryover effects of ocean warming and acidification in corals from a potential climate refugium, the Gulf of Aqaba. The Journal of Experimental Biology, 222(1), jeb186940. https://doi. org/10.1242/jeb. 186940 Bellworthy, J., Menoud, M., Krueger, T., Meibom, A., & Fine, M. (2019)。海洋变暖和酸化对亚喀巴湾潜在气候避难所珊瑚的发育传导效应。The Journal of Experimental Biology, 222(1), jeb186940. https://doi. org/10.1242/jeb.186940
Blommaert, L., Huysman, M. J. J., Vyverman, W., Lavaud, J., & Sabbe, K. (2017). Contrasting NPQ dynamics and xanthophyll cycling in a motile and a non-motile intertidal benthic diatom. Limnology and Oceanography, 62(4), 1466-1479. https://doi.org/10.1002/ Ino. 10511 Blommaert, L., Huysman, M. J. J., Vyverman, W., Lavaud, J., & Sabbe, K. (2017).运动型和非运动型潮间带底栖硅藻的 NPQ 动态和黄绿素循环对比。Limnology and Oceanography, 62(4), 1466-1479. https://doi.org/10.1002/ Ino.10511
Brener-Raffalli, K., Vidal-Dupiol, J., Adjeroud, M., Rey, O., Romans, P., Bonhomme, F., Pratlong, M., Haguenauer, A., Pillot, R., Feuillassier, L., Claereboudt, M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D., Mitta, G., Toulza, E., & Toulza, E. (2022). Gene expression plasticity and frontloading promote thermotolerance in Pocillopora corals. Peer Community Journal, 2. https://doi.org/10.24072/pcjou rnal. 79 Brener-Raffalli, K., Vidal-Dupiol, J., Adjeroud, M., Rey, O., Romans, P., Bonhomme, F., Pratlong, M., Haguenauer, A., Pillot, R.., Feuillassier, L., Claereboudt, M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D., M.、Feuillassier, L., Claereboudt, M., Magalon, H., Gélin, P., Pontarotti, P., Aurelle, D., Mitta, G., Toulza, E., & Toulza, E. (2022).基因表达可塑性和前负荷促进 Pocillopora 珊瑚的耐热性。Peer Community Journal, 2. https://doi.org/10.24072/pcjou rnal.79
Brown, B. E., Dunne, R. P., Edwards, A. J., Sweet, M. J., & Phongsuwan, N. (2015). Decadal environmental "memory" in a reef coral? Marine Biology, 162(2), 479-483. https://doi.org/10.1007/s0022 7-014-2596-2 Brown, B. E., Dunne, R. P., Edwards, A. J., Sweet, M. J., & Phongsuwan, N. (2015).珊瑚礁的十年环境 "记忆"？海洋生物学》，162（2），479-483。https://doi.org/10.1007/s0022 7-014-2596-2
Buerger, P., Alvarez-Roa, C., Coppin, C. W., Pearce, S. L., Chakravarti, L. J., Oakeshott, J. G., Edwards, O. R., & van Oppen, M. J. H. (2020). Heat-evolved microalgal symbionts increase coral bleaching tolerance. Science Advances, 6(20), eaba2498. https://doi.org/10.1126/ sciadv.aba2498 Buerger, P., Alvarez-Roa, C., Coppin, C. W., Pearce, S. L., Chakravarti, L. J., Oakeshott, J. G., Edwards, O. R., & van Oppen, M. J. H. (2020).热进化的微藻类共生体提高了珊瑚的漂白耐受性。科学进展》，6（20），eaba2498。https://doi.org/10.1126/ sciadv.aba2498
Castillo, K. D., & Helmuth, B. S. T. (2005). Influence of thermal history on the response of Montastraea annularis to short-term temperature exposure. Marine Biology, 148(2), 261-270. https://doi. org/10.1007/s00227-005-0046-x Castillo, K. D., & Helmuth, B. S. T. (2005).海洋生物学》，148（2），261-270。海洋生物学》，148（2），261-270。https://doi. org/10.1007/s00227-005-0046-x
Chen, S., Zhou, Y., Chen, Y., & Gu, J. (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34(17), i884-i890. https://doi. org/10.1093/bioinformatics/bty560 Chen, S., Zhou, Y., Chen, Y., & Gu, J. (2018). Fastp: an ultra-fast all-in-one FASTQ preprocessor.生物信息学》，34（17），i884-i890。https://doi. org/10.1093/bioinformatics/bty560
Chevin, L.-M., & Hoffmann, A. A. (2017). Evolution of phenotypic plasticity in extreme environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1723), 20160138. https:// doi.org/10.1098/rstb.2016.0138 Chevin, L.-M., & Hoffmann, A. A. (2017).极端环境中表型可塑性的进化。Philosophical Transactions of the Royal Society B: Biological Sciences, 372(1723), 20160138. https:// doi.org/10.1098/rstb.2016.0138
Chung, D. J., & Schulte, P. M. (2015). Mechanisms and costs of mitochondrial thermal acclimation in a eurythermal killifish (Fundulus heteroclitus). Journal of Experimental Biology, 218(11), 1621-1631. https:// doi.org/10.1242/jeb. 120444 Chung, D. J., & Schulte, P. M. (2015)。欧热鳉（Fundulus heteroclitus）线粒体热适应的机制和代价。实验生物学杂志》，218（11），1621-1631。https:// doi.org/10.1242/jeb.120444
Cleves, P. A., Krediet, C. J., Lehnert, E. M., Onishi, M., & Pringle, J. R. (2020). Insights into coral bleaching under heat stress from analysis Cleves, P. A., Krediet, C. J., Lehnert, E. M., Onishi, M., & Pringle, J. R. (2020).分析热应力下珊瑚白化的启示
of gene expression in a sea anemone model system. Proceedings of the National Academy of Sciences, 117(46), 28906-28917. https:// doi.org/10.1073/pnas. 2015737117 海葵模型系统中的基因表达。美国国家科学院院刊》，117（46），28906-28917。https:// doi.org/10.1073/pnas.
Crowder, C. M., Liang, W.-L., Weis, V. M., & Fan, T.-Y. (2014). Elevated temperature alters the lunar timing of planulation in the brooding coral Pocillopora damicornis. PLoS One, 9(10), e107906. https://doi. org/10.1371/journal.pone. 0107906 Crowder, C. M., Liang, W.-L., Weis, V. M., & Fan, T.-Y.(2014).温度升高会改变育雏珊瑚 Pocillopora damicornis 的月经排卵时间。https://doi. org/10.1371/journal.pone.0107906
Cumbo, V. R., Fan, T. Y., & Edmunds, P. J. (2013). Effects of exposure duration on the response of Pocillopora damicornis larvae to elevated temperature and high . Journal of Experimental Marine Biology and Ecology, 439, 100-107. https://doi.org/10.1016/j. jembe.2012.10.019 Cumbo, V. R., Fan, T. Y., & Edmunds, P. J. (2013)。暴露持续时间对 Pocillopora damicornis 幼虫对高温和高 的反应的影响 .实验海洋生物学与生态学杂志》，439, 100-107. https://doi.org/10.1016/j. jembe.2012.10.019
Cunning, R., Bay, R. A., Gillette, P., Baker, A. C., & Traylor-Knowles, N. (2018). Comparative analysis of the Pocillopora damicornis genome highlights role of immune system in coral evolution. Scientific Reports, 8(1), 16134. https://doi.org/10.1038/s41598-018-34459 Cunning, R., Bay, R. A., Gillette, P., Baker, A. C., & Traylor-Knowles, N. (2018).Pocillopora damicornis 基因组的比较分析凸显了免疫系统在珊瑚进化中的作用。Scientific Reports, 8(1), 16134. https://doi.org/10.1038/s41598-018-34459
DeMerlis, A., Kirkland, A., Kaufman, M. L., Mayfield, A. B., Formel, N., Kolodziej, G., Manzello, D. P., Lirman, D., Traylor-Knowles, N., & Enochs, I. C. (2022). Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress. Coral Reefs, 41, 435-445. https://doi.org/10.1007/ s00338-022-02232-z DeMerlis, A., Kirkland, A., Kaufman, M. L., Mayfield, A. B., Formel, N., Kolodziej, G., Manzello, D. P., Lirman, D., Traylor-Knowles, N., & Enochs, I. C. (2022)。Pre-exposure to a variable temperature treatment improves the response of Acropora cervicornis to acute thermal stress.Coral Reefs, 41, 435-445. https://doi.org/10.1007/ s00338-022-02232-z
DeSalvo, M. K., Sunagawa, S., Voolstra, C. R., & Medina, M. (2010). Transcriptomic responses to heat stress and bleaching in the Elkhorn coral Acropora palmata. Marine Ecology Progress Series, 402, 97-113. DeSalvo, M. K., Sunagawa, S., Voolstra, C. R., & Medina, M. (2010).Transcriptomic responses to heat stress and bleaching in the Elkhorn coral Acropora palmata.Marine Ecology Progress Series, 402, 97-113.
Dixon, G. B., Davies, S. W., Aglyamova, G. V., Meyer, E., Bay, L. K., & Matz, M. V. (2015). Genomic determinants of coral heat tolerance across latitudes. Science, 348(6242), 1460-1462. https://doi.org/10.1126/ science. 1261224 Dixon, G. B., Davies, S. W., Aglyamova, G. V., Meyer, E., Bay, L. K., & Matz, M. V. (2015).不同纬度珊瑚耐热性的基因组决定因素。Science, 348(6242), 1460-1462. https://doi.org/10.1126/ science.1261224
Donelson, J. M., Munday, P. L., McCormick, M. I., & Pitcher, C. R. (2012). Rapid transgenerational acclimation of a tropical reef fish to climate change. Nature Climate Change, 2(1), 30-32. https://doi. org/10.1038/nclimate1323 Donelson, J. M., Munday, P. L., McCormick, M. I., & Pitcher, C. R. (2012).热带珊瑚鱼对气候变化的快速跨代适应。https://doi. org/10.1038/nclimate1323
Donelson, J. M., Salinas, S., Munday, P. L., & Shama, L. N. S. (2018). Transgenerational plasticity and climate change experiments: Where do we go from here? Global Change Biology, 24(1), 13-34. https://doi.org/10.1111/gcb. 13903 Donelson, J. M., Salinas, S., Munday, P. L., & Shama, L. N. S. (2018).跨代可塑性与气候变化实验：我们何去何从？全球变化生物学》，24（1），13-34。https://doi.org/10.1111/gcb。13903
Ernst, J., & Bar-Joseph, Z. (2006). STEM: A tool for the analysis of short time series gene expression data. BMC Bioinformatics, 7(1), 191. https://doi.org/10.1186/1471-2105-7-191 Ernst, J., & Bar-Joseph, Z. (2006).STEM: A tool for the analysis of short time series gene expression data.BMC Bioinformatics, 7(1), 191. https://doi.org/10.1186/1471-2105-7-191
Fan, T. Y., Li, J. J., le, S. X., & Fang, L. S. (2002). Lunar periodicity of larval release by pocilloporid corals in southern Taiwan. Zoological Studies, 41(3), 288-294. Fan, T. Y., Li, J. J., le, S. X., & Fang, L. S. (2002).台湾南部桡足类珊瑚释放幼虫的月相周期性。Zoological Studies, 41(3), 288-294.
Galanto, N., Sartor, C., Moscato, V., Lizama, M., & Lemer, S. (2022). Effects of elevated temperature on reproduction and larval settlement in Leptastrea purpurea. Coral Reefs, 41, 293-302. https://doi. org/10.1007/s00338-022-02241-y Galanto, N., Sartor, C., Moscato, V., Lizama, M., & Lemer, S. (2022)。温度升高对 Leptastrea purpurea 繁殖和幼虫沉降的影响。Coral Reefs, 41, 293-302. https://doi. org/10.1007/s00338-022-02241-y
Gorman, L. M., Konciute, M. K., Cui, G., Oakley, C. A., Grossman, A. R., Weis, V. M., Aranda, M., & Davy, S. K. (2022). Symbiosis with dinoflagellates alters cnidarian cell-cycle gene expression. Cellular Microbiology, 2022, 3330160. https://doi. org/10.1155/2022/3330160 Gorman, L. M., Konciute, M. K., Cui, G., Oakley, C. A., Grossman, A. R., Weis, V. M., Aranda, M., & Davy, S. K. (2022).与甲藻的共生改变了刺胞动物细胞周期基因的表达。细胞微生物学》，2022，3330160。https://doi. org/10.1155/2022/3330160
Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., ... Regev, A. (2011). Full-length transcriptome assembly from RNA-seq data without a reference genome. Nature Biotechnology, 29(7), 644-652. https:// doi.org/10.1038/nbt. 1883 Grabherr, M. G., Haas, B. J., Yassour, M., Levin, J. Z., Thompson, D. A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R.. Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren、Zeng, Q., Chen, Z., Mauceli, E., Hacohen, N., Gnirke, A., Rhind, N., di Palma, F., Birren, B. W., Nusbaum, C., Lindblad-Toh, K., ...Regev, A. (2011).无参考基因组的 RNA-seq 数据全长转录组组装。https:// doi.org/10.1038/nbt.1883
Hackerott, S., Martell, H. A., & Eirin-Lopez, J. M. (2021). Coral environmental memory: Causes, mechanisms, and consequences for future reefs. Trends in Ecology & Evolution, 36(11), 1011-1023. https://doi. org/10.1016/j.tree.2021.06.014 Hackerott, S., Martell, H. A., & Eirin-Lopez, J. M. (2021).珊瑚环境记忆：原因、机制及对未来珊瑚礁的影响。https://doi. org/10.1016/j.tree.2021.06.014
Hawkins, T. D., & Warner, M. E. (2017). Warm preconditioning protects against acute heat-induced respiratory dysfunction and delays bleaching in a symbiotic sea anemone. Journal of Experimental Biology, 220(6), 969-983. https://doi.org/10.1242/jeb. 150391 Hawkins, T. D., & Warner, M. E. (2017).温暖预处理保护共生海葵免受急性热诱导的呼吸功能障碍并延迟白化。实验生物学杂志》，220（6），969-983。https://doi.org/10.1242/jeb。150391
Hetz, C. (2012). The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nature Reviews Molecular Cell Biology, 13(2), 89-102. https://doi.org/10.1038/nrm3270 Hetz, C. (2012).未折叠蛋白反应：在 ER 压力及其他情况下控制细胞命运的决定。Nature Reviews Molecular Cell Biology, 13(2), 89-102. https://doi.org/10.1038/nrm3270
Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W., & Dove, S. (2017). Coral reef ecosystems under climate change and ocean acidification. Frontiers in Marine Science, 4(158). https://doi.org/10.3389/ fmars. 2017.00158 Hoegh-Guldberg, O., Poloczanska, E. S., Skirving, W., & Dove, S. (2017).气候变化和海洋酸化下的珊瑚礁生态系统。海洋科学前沿》，4（158）。https://doi.org/10.3389/ fmars.2017.00158
Howells, E. J., Abrego, D., Liew, Y. J., Burt, J. A., Meyer, E., & Aranda, M. (2021). Enhancing the heat tolerance of reef-building corals to future warming. Science Advances, 7(34), eabg6070. https://doi. org/10.1126/sciadv.abg6070 Howells, E. J., Abrego, D., Liew, Y. J., Burt, J. A., Meyer, E., & Aranda, M. (2021).增强造礁珊瑚对未来变暖的耐热性。Science Advances, 7(34), eabg6070. https://doi. org/10.1126/sciadv.abg6070
Howells, E. J., Abrego, D., Meyer, E., Kirk, N. L., & Burt, J. A. (2016). Host adaptation and unexpected symbiont partners enable reef-building corals to tolerate extreme temperatures. Global Change Biology, 22(8), 2702-2714. https://doi.org/10.1111/gcb. 13250 Howells, E. J., Abrego, D., Meyer, E., Kirk, N. L., & Burt, J. A. (2016).宿主适应和意想不到的共生伙伴使造礁珊瑚能够耐受极端温度。全球变化生物学》，22（8），2702-2714。https://doi.org/10.1111/gcb。13250
Huang, Y., Niu, B., Gao, Y., Fu, L., & Li, W. (2010). CD-HIT suite: A web server for clustering and comparing biological sequences. Bioinformatics, 26(5), 680-682. https://doi.org/10.1093/bioin formatics/btq003 Huang, Y., Niu, B., Gao, Y., Fu, L., & Li, W. (2010)。CD-HIT suite：用于聚类和比较生物序列的网络服务器。生物信息学》，26（5），680-682。https://doi.org/10.1093/bioin formatics/btq003
Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., Heron, S. F., Hoey, A. S., Hoogenboom, M. O., Liu, G., McWilliam, M. J., Pears, R. J., Pratchett, M. S., Skirving, W. J., Stella, J. S., & Torda, G. (2018). Global warming transforms coral reef assemblages. Nature, 556(7702), 492-496. https://doi.org/10.1038/ s41586-018-0041-2 Hughes, T. P., Kerry, J. T., Baird, A. H., Connolly, S. R., Dietzel, A., Eakin, C. M., Heron, S. F., Hoey, A. S.., Hoogenboom, M. O., Liu, G., McWilliam, M. J., Pears, R. J., Pratchett, M. S., Skirving, W. J..、Hoogenboom, M. O., Liu, G., McWilliam, M. J., Pears, R. J., Pratchett, M. S., Skirving, W. J., Stella, J. S., & Torda, G. (2018).全球变暖改变珊瑚礁组合。自然》，556（7702），492-496。https://doi.org/10.1038/ s41586-018-0041-2
Iglesias-Prieto, R., Beltrán, V. H., Lajeunesse, T. C., Reyesbonilla, H., & Thomé, P. E. (2004). Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proceedings of the Royal Society of London Series B: Biological Sciences, 271(1549), 1757-1763. https://doi.org/10.1098/ rspb. 2004.2757 Iglesias-Prieto, R., Beltrán, V. H., Lajeunesse, T. C., Reyesbonilla, H., & Thomé, P. E. (2004).不同的藻类共生体解释了东太平洋优势珊瑚礁的垂直分布。https://doi.org/10.1098/ rspb.2004.2757
Innis, T., Allen-Waller, L., Brown, K. T., Sparagon, W., Carlson, C., Kruse, E., Huffmyer, A. S., Nelson, C. E., Putnam, H. M., & Barott, K. L. (2021). Marine heatwaves depress metabolic activity and impair cellular acid-base homeostasis in reef-building corals regardless of bleaching susceptibility. Global Change Biology, 27(12), 2728-2743. https://doi.org/10.1111/gcb. 15622 Innis, T., Allen-Waller, L., Brown, K. T., Sparagon, W., Carlson, C., Kruse, E., Huffmyer, A. S., Nelson, C. E., Putnam, H. M., & Barott, K. L. (2021)。海洋热浪抑制造礁珊瑚的新陈代谢活动并损害细胞的酸碱平衡，与漂白易感性无关。全球变化生物学》，27（12），2728-2743。https://doi.org/10.1111/gcb。15622
Isomura, N., & Nishihira, M. (2001). Size variation of planulae and its effect on the lifetime of planulae in three pocilloporid corals. Coral Reefs, 20(3), 309-315. https://doi.org/10.1007/s003380100180 Isomura, N., & Nishihira, M. (2001).珊瑚礁，20（3），309-315。Coral Reefs, 20(3), 309-315. https://doi.org/10.1007/s003380100180
Jiang, L., Guo, M.-L., Zhang, F., Zhang, Y.-Y., Zhou, G.-W., Lei, X.-M., Yuan, X.-C., Sun, Y.-F., Yuan, T., Cai, L., Lian, J.-S., Liu, S., Qian, P., & Huang, H. (2020). Impacts of elevated temperature and on the brooded larvae of Pocillopora damicornis from Luhuitou reef, China: Evidence for local acclimatization. Coral Reefs, 39, 331-344. https://doi.org/10.1007/s00338-020-01894-x Jiang, L., Guo, M.-L., Zhang, F., Zhang, Y.-Y., Zhou, G.-W., Lei, X.-M., Yuan, X.-C., Sun, Y.-F., Yuan, T., Cai, L., Lian, J.-S., Liu, S., Qian, P., & Huang, H. (2020).温度升高和 对中国芦花礁大疣梭子蟹育雏幼体的影响：当地适应的证据。珊瑚礁，39，331-344。https://doi.org/10.1007/s00338-020-01894-x。
Kenkel, C. D., & Matz, M. V. (2016). Gene expression plasticity as a mechanism of coral adaptation to a variable environment. Nature Ecology & Evolution, 1(1), 0014. https://doi.org/10.1038/s41559-016-0014 Kenkel, C. D., & Matz, M. V. (2016).基因表达可塑性是珊瑚适应多变环境的机制。Nature Ecology & Evolution, 1(1), 0014. https://doi.org/10.1038/s41559-016-0014
Kim, D., Langmead, B., & Salzberg, S. L. (2015). HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12(4), 357-360. https://doi.org/10.1038/nmeth. 3317 Kim, D., Langmead, B., & Salzberg, S. L. (2015)。HISAT：低内存需求的快速剪接对齐器。https://doi.org/10.1038/nmeth.3317
Kitchen, S. A., Jiang, D., Harii, S., Satoh, N., Weis, V. M., & Shinzato, C. (2022). Coral larvae suppress heat stress response during the onset of symbiosis decreasing their odds of survival. Molecular Ecology, 31(22), 5813-5830. https://doi.org/10.1111/mec. 16708 Kitchen, S. A., Jiang, D., Harii, S., Satoh, N., Weis, V. M., & Shinzato, C. (2022).珊瑚幼虫在共生开始时抑制热应激反应，降低其存活几率。分子生态学》，31（22），5813-5830。https://doi.org/10.1111/mec。16708
LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R., & Santos, S. R. (2018). Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Current Biology, 28(16), 2570-2580.e2576. https:// doi.org/10.1016/j.cub.2018.07.008 LaJeunesse, T. C., Parkinson, J. E., Gabrielson, P. W., Jeong, H. J., Reimer, J. D., Voolstra, C. R., & Santos, S. R. (2018).Symbiodiniaceae 的系统修订突显了珊瑚内共生体的古老性和多样性。Current Biology, 28(16), 2570-2580.e2576. https:// doi.org/10.1016/j.cub.2018.07.008
Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357-359. https://doi.org/10.1038/ nmeth. 1923 Langmead, B., & Salzberg, S. L. (2012).用 Bowtie 2 进行快速间隙读数比对。https://doi.org/10.1038/ nmeth.1923
Lehnert, E. M., Mouchka, M. E., Burriesci, M. S., Gallo, N. D., Schwarz J. A., & Pringle, J. R. (2014). Extensive differences in gene expression between symbiotic and Aposymbiotic cnidarians. G3 Genes|Genomes|Genetics, 4(2), 277-295. https://doi.org/10.1534/ g3.113.009084 Lehnert, E. M., Mouchka, M. E., Burriesci, M. S., Gallo, N. D., Schwarz J. A., & Pringle, J. R. (2014).共生和互生刺胞动物基因表达的广泛差异。G3 Genes|Genomes|Genetics, 4(2), 277-295. https://doi.org/10.1534/ g3.113.009084
Levy, G., Shaish, L., Haim, A., & Rinkevich, B. (2010). Mid-water rope nursery-Testing design and performance of a novel reef restoration instrument. Ecological Engineering, 36(4), 560-569. https:// doi.org/10.1016/j.ecoleng.2009.12.003 Levy, G., Shaish, L., Haim, A., & Rinkevich, B. (2010)。水中绳索育苗--新型珊瑚礁修复工具的设计与性能测试。生态工程，36（4），560-569。 https:// doi.org/10.1016/j.ecoleng.2009.12.003
Li, J., Long, L., Zou, Y., & Zhang, S. (2021). Microbial community and transcriptional responses to increased temperatures in coral Pocillopora damicornis holobiont. Environmental Microbiology, 23(2), 826-843. https://doi.org/10.1111/1462-2920.15168 Li, J., Long, L., Zou, Y., & Zhang, S. (2021).珊瑚 Pocillopora damicornis holobiont 对温度升高的微生物群落和转录反应。Environmental Microbiology, 23(2), 826-843. https://doi.org/10.1111/1462-2920.15168
Li, X., Liu, S., Huang, H., Huang, L., Jing, Z., & Zhang, C. (2012). Coral bleaching caused by an abnormal water temperature rise at Luhuitou fringing reef, Sanya Bay, China. Aquatic Ecosystem Health & Management, 15(2), 227-233. https://doi.org/10.1080/14634 988.2012 .687651 Li, X., Liu, S., Huang, H., Huang, L., Jing, Z., & Zhang, C. (2012).中国三亚湾鹿回头环礁水温异常升高导致的珊瑚白化。水生生态系统健康与管理，15（2），227-233。https://doi.org/10.1080/14634 988.2012 .687651
Liao, M.-L., Li, G.-Y., Wang, J., Marshall, D. J., Hui, T. Y., Ma, S.-Y., Zhang, Y.-M., Helmuth, B., & Dong, Y.-W. (2021). Physiological determinants of biogeography: The importance of metabolic depression to heat tolerance. Global Change Biology, 27(11), 2561-2579. https:// doi.org/10.1111/gcb. 15578 Liao, M.-L., Li, G.-Y., Wang, J., Marshall, D. J., Hui, T. Y., Ma, S.-Y., Zhang, Y.-M., Helmuth, B., & Dong, Y.-W.(2021).生物地理学的生理决定因素：代谢抑制对耐热性的重要性。https:// doi.org/10.1111/gcb.15578
Louis, Y. D., Bhagooli, R., Kenkel, C. D., Baker, A. C., & Dyall, S. D. (2017). Gene expression biomarkers of heat stress in scleractinian corals: Promises and limitations. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 191, 63-77. https:// doi.org/10.1016/j.cbpc.2016.08.007 Louis, Y. D., Bhagooli, R., Kenkel, C. D., Baker, A. C., & Dyall, S. D. (2017).硬骨珊瑚热应力的基因表达生物标志物：前景与局限。Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 191, 63-77. https:// doi.org/10.1016/j.cbpc.2016.08.007
Love, M. I., Huber, W., & Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 15(12), 550. https://doi.org/10.1186/s1305 9-014-0550-8 Love, M. I., Huber, W., & Anders, S. (2014)。使用 DESeq2 对 RNA-seq 数据的折叠变化和离散度进行有节制的估计。Genome Biology, 15(12), 550. https://doi.org/10.1186/s1305 9-014-0550-8
Maboloc, E. A., & Chan, K. Y. K. (2021). Parental whole life cycle exposure modulates progeny responses to ocean acidification in slipper limpets. Global Change Biology, 27(14), 3272-3281. https://doi. org/10.1111/gcb. 15647 Maboloc, E. A., & Chan, K. Y. K. (2021).父母整个生命周期的暴露调节舄类后代对海洋酸化的反应。Global Change Biology, 27(14), 3272-3281. https://doi. org/10.1111/gcb.15647
Majerova, E., Carey, F. C., Drury, C., & Gates, R. D. (2021). Preconditioning improves bleaching tolerance in the reef-building coral Pocillopora acuta through modulations in the programmed cell death pathways. Molecular Ecology, 30(14), 3560-3574. https://doi.org/10.1111/ mec. 15988 Majerova, E., Carey, F. C., Drury, C., & Gates, R. D. (2021)。Preconditioning improves bleaching tolerance in the reef-building coral Pocillopora acuta through modulations in the programmed cell death pathways.分子生态学》，30（14），3560-3574。https://doi.org/10.1111/ mec.15988
Maor-Landaw, K., Karako-Lampert, S., Ben-Asher, H. W., Goffredo, S., Falini, G., Dubinsky, Z., & Levy, O. (2014). Gene expression profiles during short-term heat stress in the red sea coral Stylophora pistillata. Global Change Biology, 20(10), 3026-3035. https://doi. org/10.1111/gcb. 12592 Maor-Landaw, K., Karako-Lampert, S., Ben-Asher, H. W., Goffredo, S., Falini, G., Dubinsky, Z., & Levy, O. (2014).红海珊瑚 Stylophora pistillata 短期热应力期间的基因表达谱。Global Change Biology, 20(10), 3026-3035. https://doi. org/10.1111/gcb.12592
Maor-Landaw, K., van Oppen, M. J. H., & McFadden, G. I. (2020), Symbiotic lifestyle triggers drastic changes in the gene expression of the algal endosymbiont Breviolum minutum (Symbiodiniaceae). Ecology and Evolution, 10(1), 451-466. https://doi.org/10.1002/ ece3.5910 Maor-Landaw, K., van Oppen, M. J. H., & McFadden, G. I. (2020)，共生生活方式引发藻类内共生体 Breviolum minutum（共生藻科）基因表达的剧烈变化。https://doi.org/10.1002/ ece3.5910
Marshall, D. J., & McQuaid, C. D. (2011). Warming reduces metabolic rate in marine snails: Adaptation to fluctuating high temperatures challenges the metabolic theory of ecology. Proceedings of the Royal Society B: Biological Sciences, 278(1703), 281-288. https://doi org/10.1098/rspb.2010.1414 Marshall, D. J., & McQuaid, C. D. (2011).变暖降低了海洋蜗牛的新陈代谢率：对高温波动的适应挑战了生态学的新陈代谢理论。Proceedings of the Royal Society B: Biological Sciences, 278(1703), 281-288. https://doi org/10.1098/rspb.2010.1414
McRae, C. J., Huang, W.-B., Fan, T.-Y., & Côté, I. M. (2021). Effects of thermal conditioning on the performance of Pocillopora acuta adult coral colonies and their offspring. Coral Reefs, 40(5), 1491-1503. https://doi.org/10.1007/s00338-021-02123-9 McRae, C. J., Huang, W.-B., Fan, T.-Y., & Côté, I. M. (2021).热调节对 Pocillopora acuta 成年珊瑚群及其后代表现的影响。Coral Reefs, 40(5), 1491-1503. https://doi.org/10.1007/s00338-021-02123-9
McRae, C. J., Keshavmurthy, S., Meng, P.-J., Rosset, S. L., Huang, W.B., Chen, C. A., Fan, T.-Y., & Côté, I. M. (2022). Variable responses to chronic and acute elevated temperature of three coral species from reefs with distinct thermal regimes. Marine Biology, 169(7), 97. https://doi.org/10.1007/s00227-022-04071-6 McRae, C. J., Keshavmurthy, S., Meng, P.-J., Rosset, S. L., Huang, W.B., Chen, C. A., Fan, T.-Y., & Côté, I. M. (2022)。来自不同热制度珊瑚礁的三种珊瑚物种对慢性和急性温度升高的不同反应。Marine Biology, 169(7), 97. https://doi.org/10.1007/s00227-022-04071-6
Middlebrook, R., Hoegh-Guldberg, O., & Leggat, W. (2008). The effect of thermal history on the susceptibility of reef-building corals to thermal stress. Journal of Experimental Biology, 211(7), 1050-1056. https://doi.org/10.1242/jeb. 013284 Middlebrook, R., Hoegh-Guldberg, O., & Leggat, W. (2008).热历史对造礁珊瑚易受热应力影响的影响。实验生物学杂志》，211（7），1050-1056。https://doi.org/10.1242/jeb。013284
Mohamed, A. R., Andrade, N., Moya, A., Chan, C. X., Negri, A. P., Bourne, D. G., Ying, H., Ball, E. E., & Miller, D. J. (2020). Dual RNAsequencing analyses of a coral and its native symbiont during the establishment of symbiosis. Molecular Ecology, 00, 1-17. https://doi. org/10.1111/mec. 15612 Mohamed, A. R., Andrade, N., Moya, A., Chan, C. X., Negri, A. P., Bourne, D. G., Ying, H., Ball, E. E., & Miller, D. J. (2020).共生建立过程中珊瑚及其原生共生体的双重 RNA 序列分析。分子生态学》，00, 1-17. https://doi. org/10.1111/mec.15612
Negi, S., Perrine, Z., Friedland, N., Kumar, A., Tokutsu, R., Minagawa, J., Berg, H., Barry, A. N., Govindjee, G., & Sayre, R. (2020). Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algaet. The Plant Journal, 103(2), 584-603. https://doi.org/10.1111/ tpj. 14751 Negi, S., Perrine, Z., Friedland, N., Kumar, A., Tokutsu, R., Minagawa, J., Berg, H., Barry, A. N., Govindjee, G., & Sayre, R. (2020).光对采光天线大小的调节可大幅提高绿藻的光合效率和生物量产量。植物学报》，103（2），584-603。https://doi.org/10.1111/ tpj.14751
Nielsen, D. A., Petrou, K., & Gates, R. D. (2018). Coral bleaching from a single cell perspective. The ISME Journal, 12(6), 1558-1567. https:// doi.org/10.1038/s41396-018-0080-6 Nielsen, D. A., Petrou, K., & Gates, R. D. (2018)。从单细胞角度看珊瑚漂白。https:// doi.org/10.1038/s41396-018-0080-6
Permata, W. D., Kinzie III, R. A., & Hidaka, M. (2000). Histological studies on the origin of planulae of the coral Pocillopora damicornis. Marine Ecology Progress Series, 200, 191-200. Permata, W. D., Kinzie III, R. A., & Hidaka, M. (2000).Histological studies on the origin of the planulae of the coral Pocillopora damicornis.Marine Ecology Progress Series, 200, 191-200.
Pernice, M., Dunn, S. R., Miard, T., Dufour, S., Dove, S., & Hoegh-Guldberg, O. (2011). Regulation of apoptotic mediators reveals dynamic responses to thermal stress in the reef building coral Acropora millepora. PLoS One, 6(1), e16095. https://doi.org/10.1371/journ al.pone. 0016095 Pernice, M., Dunn, S. R., Miard, T., Dufour, S., Dove, S., & Hoegh-Guldberg, O. (2011).凋亡介质的调节揭示了造礁珊瑚 Acropora millepora 对热应力的动态响应。PLoS One, 6(1), e16095. https://doi.org/10.1371/journ al.pone.0016095
Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T.-C., Mendell, J. T., & Salzberg, S. L. (2015). StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nature Biotechnology, 33(3), 290-295. https://doi.org/10.1038/nbt. 3122 Pertea, M., Pertea, G. M., Antonescu, C. M., Chang, T.-C., Mendell, J. T., & Salzberg, S. L. (2015).StringTie 实现了从 RNA-seq 读数重建转录组的改进。自然生物技术》，33（3），290-295。https://doi.org/10.1038/nbt。3122
Petroutsos, D., Tokutsu, R., Maruyama, S., Flori, S., Greiner, A., Magneschi, L., Cusant, L., Kottke, T., Mittag, M., Hegemann, P., Finazzi, G., & Minagawa, J. (2016). A blue-light photoreceptor mediates the feedback regulation of photosynthesis. Nature, 537(7621), 563-566. https://doi.org/10.1038/nature19358 Petroutsos, D., Tokutsu, R., Maruyama, S., Flori, S., Greiner, A., Magneschi, L., Cusant, L., Kottke, T., Mittag, M., Hegemann, P., Finazzi, G., & Minagawa, J. (2016)。蓝光光感受器介导光合作用的反馈调节。Nature, 537(7621), 563-566. https://doi.org/10.1038/nature19358
Poquita-Du, R. C., Huang, D., Chou, L. M., Mrinalini, W., & Todd, P. A. (2019). Short term exposure to heat and sediment triggers changes in coral gene expression and photo-physiological performance. Frontiers in Marine Science, 6. https://doi.org/10.3389/ fmars.2019.00121 Poquita-Du, R. C., Huang, D., Chou, L. M., Mrinalini, W., & Todd, P. A. (2019).短期暴露于热量和沉积物会引发珊瑚基因表达和光生理表现的变化。https://doi.org/10.3389/ fmars.2019.00121
Putnam, H. M., Edmmunds, P. J., & Fan, T. Y. (2008). Effect of temperature on the settlement choice and photophysiology of larvae from the reef coral Stylophora pistillata. Biological Bulletin, 215(2), 135-142. Putnam, H. M., Edmmunds, P. J., & Fan, T. Y. (2008).温度对珊瑚虫幼虫定居选择和光生理学的影响。生物通报》，215（2），135-142。
Putnam, H. M., & Gates, R. D. (2015). Preconditioning in the reef-building coral Pocillopora damicornis and the potential for trans-generational acclimatization in coral larvae under future climate change conditions. Journal of Experimental Biology, 218(15), 2365. Putnam, H. M., & Gates, R. D. (2015).造礁珊瑚 Pocillopora damicornis 的预调节以及未来气候变化条件下珊瑚幼体跨代适应的潜力。实验生物学杂志》，218（15），2365。
Putnam, H. M., Ritson-Williams, R., Cruz, J. A., Davidson, J. M., & Gates, R. D. (2020). Environmentally-induced parental or developmental conditioning influences coral offspring ecological performance. Scientific Reports, 10(1), 13664. https://doi.org/10.1038/s41598020-70605-x Putnam, H. M., Ritson-Williams, R., Cruz, J. A., Davidson, J. M., & Gates, R. D. (2020).环境诱导的亲代或发育调节影响珊瑚后代的生态表现。Scientific Reports, 10(1), 13664. https://doi.org/10.1038/s41598020-70605-x
Rädecker, N., Pogoreutz, C., Gegner, H. M., Cárdenas, A., Roth, F., Bougoure, J., Guagliardo, P., Wild, C., Pernice, M., Raina, J.-B., Meibom, A., & Voolstra, C. R. (2021). Heat stress destabilizes symbiotic nutrient cycling in corals. Proceedings of the National Academy of Sciences, 118(5), e2022653118. https://doi.org/10.1073/ pnas. 2022653118 Rädecker, N., Pogoreutz, C., Gegner, H. M., Cárdenas, A., Roth, F., Bougoure, J., Guagliardo, P., Wild, C., Pernice, M., Raina, J.-B., Meibom, A., & Voolstra, C. R. (2021)。热应力破坏珊瑚共生营养循环的稳定性。美国国家科学院院刊》，118（5），e2022653118. https://doi.org/10.1073/ pnas. 2022653118
Reinfelder, J. R., Kraepiel, A. M. L., & Morel, F. M. M. (2000). Unicellular C4 photosynthesis in a marine diatom. Nature, 407(6807), 996-999. https://doi.org/10.1038/35039612 Reinfelder, J. R., Kraepiel, A. M. L., & Morel, F. M. M. (2000).海洋硅藻的单细胞 C4 光合作用。Nature, 407(6807), 996-999. https://doi.org/10.1038/35039612
Richter, K., Haslbeck, M., & Buchner, J. (2010). The heat shock response: Life on the verge of death. Molecular Cell, 40(2), 253-266. https:// doi.org/10.1016/j.molcel.2010.10.006 Richter, K., Haslbeck, M., & Buchner, J. (2010)。热休克反应：濒临死亡的生命。分子细胞》，40（2），253-266。https:// doi.org/10.1016/j.molcel.2010.10.006
Rivera, H. E., Aichelman, H. E., Fifer, J. E., Kriefall, N. G., Wuitchik, D. M., Wuitchik, S. J. S., & Davies, S. W. (2021). A framework for understanding gene expression plasticity and its influence on stress tolerance. Molecular Ecology, 30(6), 1381-1397. https://doi.org/10.1111/ mec. 15820 Rivera, H. E., Aichelman, H. E., Fifer, J. E., Kriefall, N. G., Wuitchik, D. M., Wuitchik, S. J. S., & Davies, S. W. (2021).理解基因表达可塑性及其对胁迫耐受性影响的框架。分子生态学》，30（6），1381-1397。https://doi.org/10.1111/ mec.15820
Rivera, H. E., Chen, C.-Y., Gibson, M. C., & Tarrant, A. M. (2021). Plasticity in parental effects confers rapid larval thermal tolerance in the estuarine anemone Nematostella vectensis. Journal of Experimental Biology, 224(5). https://doi.org/10.1242/jeb. 236745 Rivera, H. E., Chen, C.-Y., Gibson, M. C., & Tarrant, A. M. (2021).亲本效应的可塑性赋予河口海葵 Nematostella vectensis 幼虫快速耐热性。实验生物学杂志》，224（5）。https://doi.org/10.1242/jeb。236745
Rivera, H. E., & Davies, S. W. (2021). Symbiosis maintenance in the facultative coral, Oculina arbuscula, relies on nitrogen cycling, cell cycle modulation, and immunity. Scientific Reports, 11(1), 21226. https:// doi.org/10.1038/s41598-021-00697-6 Rivera, H. E., & Davies, S. W. (2021).面生珊瑚 Oculina arbuscula 的共生维持依赖于氮循环、细胞周期调节和免疫。https:// doi.org/10.1038/s41598-021-00697-6
Shama, L. N. S., Mark, F. C., Strobel, A., Lokmer, A., John, U., & Mathias Wegner, K. (2016). Transgenerational effects persist down the maternal line in marine sticklebacks: Gene expression matches physiology in a warming ocean. Evolutionary Applications, 9(9), 10961111. https://doi.org/10.1111/eva. 12370 Shama, L. N. S., Mark, F. C., Strobel, A., Lokmer, A., John, U., & Mathias Wegner, K. (2016)。海洋粘虫母系的传代效应持续存在：在变暖的海洋中基因表达与生理相匹配。进化应用》，9（9），10961111。https://doi.org/10.1111/eva。12370
Shama, L. N. S., Strobel, A., Mark, F. C., & Wegner, K. M. (2014). Transgenerational plasticity in marine sticklebacks: Maternal effects mediate impacts of a warming ocean. Functional Ecology, 28(6), 1482-1493. https://doi.org/10.1111/1365-2435.12280 Shama, L. N. S., Strobel, A., Mark, F. C., & Wegner, K. M. (2014).海洋粘虫的跨代可塑性：海洋变暖对母体影响的中介作用。Functional Ecology, 28(6), 1482-1493. https://doi.org/10.1111/1365-2435.12280
Silverstein, R. N., Cunning, R., & Baker, A. C. (2015). Change in algal symbiont communities after bleaching, not prior heat exposure, increases heat tolerance of reef corals. Global Change Biology, 21(1), 236-249. https://doi.org/10.1111/gcb. 12706 Silverstein, R. N., Cunning, R., & Baker, A. C. (2015).白化后藻类共生群落的变化（而非之前的热暴露）提高了珊瑚礁珊瑚的耐热性。全球变化生物学》，21（1），236-249。https://doi.org/10.1111/gcb。12706
Stoddart, J. A., & Black, R. (1985). Cycles of gametogenesis and planulation in the coral Pocillopora damicornis. Marine Ecology Progress Series, 23(2), 153-164. Stoddart, J. A., & Black, R. (1985).Cycles of gametogenesis and planulation in the coral Pocillopora damicornis.Marine Ecology Progress Series, 23(2), 153-164.
Takahashi, S., Whitney, S. M., & Badger, M. R. (2009). Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proceedings of the National Academy of Sciences, 106(9), 3237-3242. https://doi.org/10.1073/ pnas. 0808363106 Takahashi, S., Whitney, S. M., & Badger, M. R. (2009).培养的 Symbiodinium 物种对修复光损伤光合机械的不同热敏感性。美国国家科学院院刊》，106（9），3237-3242。https://doi.org/10.1073/ pnas. 0808363106
Takahashi, S., Yoshioka-Nishimura, M., Nanba, D., & Badger, M. R. (2012). Thermal acclimation of the symbiotic alga Symbiodinium spp. alleviates photobleaching under heat stress. Plant Physiology, 161(1), 477-485. https://doi.org/10.1104/pp.112.207480 Takahashi, S., Yoshioka-Nishimura, M., Nanba, D., & Badger, M. R. (2012).共生藻类共生藻的热适应减轻了热胁迫下的光漂白。植物生理学》，161（1），477-485。 https://doi.org/10.1104/pp.112.207480
Tchernov, D., Kvitt, H., Haramaty, L., Bibby, T. S., Gorbunov, M. Y., Rosenfeld, H., & Falkowski, P. G. (2011). Apoptosis and the selective survival of host animals following thermal bleaching in zooxanthellate corals. Proceedings of the National Academy of Sciences, 108(24), 9905-9909. https://doi.org/10.1073/pnas. 1106924108 Tchernov, D., Kvitt, H., Haramaty, L., Bibby, T. S., Gorbunov, M. Y., Rosenfeld, H., & Falkowski, P. G. (2011).动物贝类珊瑚热漂白后宿主动物的凋亡和选择性生存。美国国家科学院院刊》，108(24), 9905-9909. https://doi.org/10.1073/pnas. 1106924108
Timm, S., & Hagemann, M. (2020). Photorespiration-How is it regulated and how does it regulate overall plant metabolism? Journal of Experimental Botany, 71(14), 3955-3965. https://doi.org/10.1093/ jxb/eraa183 Timm, S., & Hagemann, M. (2020)。光呼吸--如何调节以及如何调节植物的整体新陈代谢？实验植物学杂志》，71（14），3955-3965。https://doi.org/10.1093/ jxb/eraa183
Tivey, T. R., Parkinson, J. E., Weis, V. M., Medina, M., & Ruby, E. G. (2020). Host and symbiont cell cycle coordination is mediated by symbiotic state, nutrition, and partner identity in a model cnidariandinoflagellate Symbiosis. mBio, 11(2), e02626-02619. https://doi. org Tivey, T. R., Parkinson, J. E., Weis, V. M., Medina, M., & Ruby, E. G. (2020).mBio, 11(2), e02626-02619. https://doi. org.
Torda, G., Donelson, J. M., Aranda, M., Barshis, D. J., Bay, L., Berumen, M. L., Bourne, D. G., Cantin, N., Foret, S., Matz, M., Miller, D. J., Moya, A., Putnam, H. M., Ravasi, T., van Oppen, M. J. H., Thurber, R. V., Vidal-Dupiol, J., Voolstra, C. R., Watson, S.-A., ... Munday, P. L. (2017). Rapid adaptive responses to climate change in corals. Nature Climate Change, 7(9), 627-636. https://doi.org/10.1038/ nclimate3374
Tytler, E. M., Trench, R. K., & Smith, D. (1986). Activities of enzymes in -carboxylation reactions and of catalase in cell-free preparations from the symbiotic dinoflagellates Symbiodinium Spp. from a coral, a clam, a zoanthid and two sea anemones. Proceedings of the Royal Society of London. Series B. Biological Sciences, 228(1253), 483-492. https://doi.org/10.1098/rspb.1986.0065 Tytler, E. M., Trench, R. K., & Smith, D. (1986)。 -羧化反应中酶的活性以及来自珊瑚、蛤蜊、zoanthid 和两种海葵的共生双鞭毛藻的无细胞制备物中过氧化氢酶的活性。伦敦皇家学会论文集》。生物科学》，228(1253)，483-492。 https://doi.org/10.1098/rspb.1986.0065
Voolstra, C. R., Suggett, D. J., Peixoto, R. S., Parkinson, J. E., Quigley, K. M., Silveira, C. B., Sweet, M., Muller, E. M., Barshis, D. J., Bourne, D. G., & Aranda, M. (2021). Extending the natural adaptive capacity of coral holobionts. Nature Reviews Earth & Environment, 2(11), 747762. https://doi.org/10.1038/s43017-021-00214-3 Voolstra, C. R., Suggett, D. J., Peixoto, R. S., Parkinson, J. E., Quigley, K. M., Silveira, C. B., Sweet, M., Muller, E. M., Barshis, D. J., Bourne, D. G., & Aranda, M. (2021).Extending the natural adaptive capacity of coral holobionts.Nature Reviews Earth & Environment, 2(11), 747762. https://doi.org/10.1038/s43017-021-00214-3
Walter, P., & Ron, D. (2011). The unfolded protein response: From stress pathway to homeostatic regulation. Science, 334(6059), 1081-1086. Walter, P., & Ron, D. (2011)。未折叠蛋白反应：从应激途径到平衡调节。科学》，334（6059），1081-1086。
Warner, M. E., Fitt, W. K., & Schmidt, G. W. (1999). Damage to photosystem II in symbiotic dinoflagellates: A determinant of coral bleaching. Proceedings of the National Academy of Sciences, 96(14), 80078012. https://doi.org/10.1073/pnas.96.14.8007 Warner, M. E., Fitt, W. K., & Schmidt, G. W. (1999).共生甲藻光系统 II 的损伤：珊瑚白化的决定因素。美国国家科学院院刊》，96（14），80078012。https://doi.org/10.1073/pnas.96.14.8007。
Weis, V. M. (2008). Cellular mechanisms of cnidarian bleaching: Stress causes the collapse of symbiosis. Journal of Experimental Biology, 211(19), 3059-3066. Weis, V. M. (2008).刺胞动物白化的细胞机制：压力导致共生关系崩溃。实验生物学杂志》，211（19），3059-3066。
Wong, J. M., Johnson, K. M., Kelly, M. W., & Hofmann, G. E. (2018). Transcriptomics reveal transgenerational effects in purple sea urchin embryos: Adult acclimation to upwelling conditions alters the response of their progeny to differential pCO2 levels. Molecular Ecology, 27(5), 1120-1137. https://doi.org/10.1111/ mec. 14503 Wong, J. M., Johnson, K. M., Kelly, M. W., & Hofmann, G. E. (2018).转录组学揭示了紫色海胆胚胎的跨代效应：成体对上升流条件的适应改变了其后代对不同 pCO2 水平的反应。分子生态学》，27（5），1120-1137。https://doi.org/10.1111/ mec.14503
Wong, K. H., Goodbody-Gringley, G., de Putron, S. J., Becker, D. M., Chequer, A., & Putnam, H. M. (2021). Brooded coral offspring physiology depends on the combined effects of parental press and pulse thermal history. Global Change Biology, 27(13), 3179-3195. https:// doi.org/10.1111/gcb. 15629 Wong, K. H., Goodbody-Gringley, G., de Putron, S. J., Becker, D. M., Chequer, A., & Putnam, H. M. (2021).繁殖的珊瑚后代生理机能取决于亲本压力和脉冲热历史的综合影响。Global Change Biology, 27(13), 3179-3195. https:// doi.org/10.1111/gcb.15629
Wuitchik, D. M., Almanzar, A., Benson, B. E., Brennan, S., Chavez, J. D., Liesegang, M. B., Reavis, J. L., Reyes, C. L., Schniedewind, M. K., Trumble, I. F., & Davies, S. W. (2021). Characterizing environmental stress responses of aposymbiotic Astrangia poculata to divergent thermal challenges. Molecular Ecology, 30(20), 5064-5079. https:// doi.org/10.1111/mec. 16108 Wuitchik, D. M., Almanzar, A., Benson, B. E., Brennan, S., Chavez, J. D., Liesegang, M. B., Reavis, J. L., Reyes, C. L., Schniedewind, M. K., Trumble, I. F., & Davies, S. W. (2021).Characterizing environmental stress responses of aposymbiotic Astrangia poculata to divergent thermal challenges.https:// doi.org/10.1111/mec.16108
Xiang, T., Jinkerson, R. E., Clowez, S., Tran, C., Krediet, C. J., Onishi, M., Cleves, P. A., Pringle, J. R., & Grossman, A. R. (2017). Glucoseinduced trophic shift in an endosymbiont dinoflagellate with physiological and molecular consequences. Plant Physiology, 176(2), 1793-1807. https://doi.org/10.1104/pp.17.01572 Xiang, T., Jinkerson, R. E., Clowez, S., Tran, C., Krediet, C. J., Onishi, M., Cleves, P. A., Pringle, J. R., & Grossman, A. R. (2017).内共生甲藻中葡萄糖诱导的营养转变及其生理和分子后果。植物生理学》，176（2），1793-1807。https://doi.org/10.1104/pp.17.01572。
Yakovleva, I. M., Baird, A. H., Yamamoto, H. H., Bhagooli, R., Nonaka, M., & Hidaka, M. (2009). Algal symbionts increase oxidative damage and death in coral larvae at high temperatures. Marine Ecology Progress Series, 378, 105-112. Yakovleva, I. M., Baird, A. H., Yamamoto, H. H., Bhagooli, R., Nonaka, M., & Hidaka, M. (2009).Algal symbionts increase oxidative damage and death in coral larvae at high temperature.Marine Ecology Progress Series, 378, 105-112.
Yellowlees, D., Rees, T. A. V., & Leggat, W. (2008). Metabolic interactions between algal symbionts and invertebrate hosts. Plant, Cell & Environment, 31(5), 679-694. https://doi. org/10.1111/j.1365-3040.2008.01802.x Yellowlees, D., Rees, T. A. V., & Leggat, W. (2008).藻类共生体与无脊椎动物宿主之间的代谢相互作用。植物、细胞与环境，31（5），679-694。https://doi. org/10.1111/j.1365-3040.2008.01802.x
Yin, J., Zhou, M., Lin, Z., Li, Q. Q., & Zhang, Y.-Y. (2019). Transgenerational effects benefit offspring across diverse environments: A metaanalysis in plants and animals. Ecology Letters, 22(11), 1976-1986. https://doi.org/10.1111/ele. 13373 Yin, J., Zhou, M., Lin, Z., Li, Q. Q., & Zhang, Y.-Y.(2019).跨代效应在不同环境中对后代的益处：动植物的荟萃分析。Ecology Letters, 22(11), 1976-1986. https://doi.org/10.1111/ele.13373
Yu, G., Wang, L.-G., Han, Y., & He, Q.-Y. (2012). clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS. A Journal of Integrative Biology, 16(5), 284-287. https://doi. org/10.1089/omi.2011.0118 Yu, G., Wang, L.-G., Han, Y., & He, Q.-Y. (2012.)。(clusterProfiler：用于比较基因簇间生物学主题的 R 软件包。OMICS.综合生物学杂志》，16（5），284-287。 https://doi. org/10.1089/omi.2011.0118
Yu, X., Yu, K., Huang, W., Liang, J., Qin, Z., Chen, B., Yao, Q., & Liao, Z. (2020). Thermal acclimation increases heat tolerance of the scleractinian coral Acropora pruinosa. Science of the Total Environment, 733, 139319. https://doi.org/10.1016/j.scitotenv.2020.139319 Yu, X., Yu, K., Huang, W., Liang, J., Qin, Z., Chen, B., Yao, Q., & Liao, Z. (2020)。热适应提高硬骨鱼类珊瑚 Acropora pruinosa 的耐热性。总体环境科学》，733, 139319。https://doi.org/10.1016/j.scitotenv.2020.139319。
Zhang, H., Zhou, Y., Liu, T.-Q., Yin, X.-J., Lin, L., Lin, Q., & Wang, D.Z. (2021). Initiation of efficient C4 pathway in response to low Zhang, H., Zhou, Y., Liu, T.-Q., Yin, X.-J., Lin, L., Lin, Q., & Wang, D.Z. (2021)。高效 C4 通路的启动以应对低
ambient during the bloom period of a marine dinoflagellate. Environmental Microbiology, 23(6), 3196-3211. https://doi. org/10.1111/1462-2920.15545 海洋甲藻绽放期间的环境 。环境微生物学》，23（6），3196-3211。https://doi. org/10.1111/1462-2920.15545
Zhang, Y.-Y. (2015). Recovery capacity of Pocillopora damicornis on Luhuitou reef, Sanya. [Ph.D. thesis]. University Of Chinese Academy of Sciences. (In Chinese with English abstract). Zhang, Y.-Y.(2015).三亚鹿回头礁大鸨的恢复能力。[中国科学院大学。］中国科学院大学。(中文，有英文摘要）。
SUPPORTING INFORMATION 佐证资料
Additional supporting information can be found online in the Supporting Information section at the end of this article. 其他辅助信息可在本文末尾的 "辅助信息 "部分在线查阅。
How to cite this article: Jiang, L., Liu, C.-Y., Cui, G., Huang, L.-T., Yu, X.-L., Sun, Y.-F., Tong, H.-Y., Zhou, G.-W., Yuan, X.-C., Hu, Y.-S., Zhou, W.-L., Aranda, M., Qian, P.-Y., & Huang, H. (2023). Rapid shifts in thermal reaction norms and tolerance of brooded coral larvae following parental heat acclimation. Molecular Ecology, 32, 1098-1116. https://doi.org/10.1111/ mec. 16826 本文引用方式Jiang, L., Liu, C.-Y., Cui, G., Huang, L.-T., Yu, X.-L., Sun, Y.-F., Tong, H.-Y., Zhou, G.-W., Yuan, X.-C., Hu, Y.-S., Zhou, W.-L., Aranda, M., Qian, P.-Y., & Huang, H. (2023).亲代热适应后育雏珊瑚幼体热反应规范和耐受性的快速转变。分子生态学》，32，1098-1116。https://doi.org/10.1111/ mec.16826
