Phylogenetic analysis of symbiont transmission mechanisms reveal evolutionary patterns in thermotolerance and host specificity that enhance bleaching resistance among vertically transmitted <i>Symbiodinium</i>
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Vertical transmission of <i>Symbiodinium</i> symbionts between generations of coral hosts has been hypothesized to result in superior matches between host and symbiont physiologies, and to form holobionts that are generally more resistant to thermal stress. Alternatively, horizontal transmission, with its greater potential for assembling physiologically diverse associations as well as being capable of substituting symbionts in response to stimuli, may result in holobionts that are generally more resistant to thermal stress. While the most common mode of transmission among Scleractinia–<i>Symbiodinium</i> symbioses is horizontal, mixed-modes transmission only occurs in vertically transmitting corals, allowing the maintenance of highly specialized associations across generations as well as transiently critical relationships. These advantages of mixed-modes transmission may serve to rescue otherwise susceptible corals, or alternatively, reinforce otherwise resistant corals, depending upon the other attributes of vertically transmitted <i>Symbiodinium</i> phylotypes. Here we ask if vertically transmitted symbionts tend to be more thermotolerant and specific. Because significant relationships between traits can be overestimated or obscured by patterns of shared evolutionary history, we inferred a novel molecular phylogeny for 97 <i>Symbiodinium</i> phylotypes representing clades A–F to evaluate the relationship between phylotype transmission-mode, thermotolerance and specificity to coral hosts. Thermotolerance and specificity have been independently derived multiple times during the evolutionary history of <i>Symbiodinium</i>, and cannot be predicted by clade membership. The probability of phylotype transmission being predominantly vertical increased by more than 200% across the observed ranges of increase of thermotolerance and specificity, even though phylotype thermotolerance is not correlated with host specificity. Higher thermotolerance and specificity of vertically transmitted <i>Symbiodinium</i> may contribute to robust bleaching resistance among vertically transmitting corals that could reinforce the potential benefits of mixed-modes transmission.
珊瑚宿主世代间的虫黄藻（Symbiodinium）垂直传播，此前被假说认为可促成宿主与共生体生理适配性的优化，并形成总体上更耐受热胁迫的全共生体（holobiont）。与之相对，水平传播模式凭借其在组装生理多样化共生关联上的更大潜力，以及可响应环境刺激替换共生体的特性，或也能形成总体耐受热胁迫能力更强的全共生体。尽管石珊瑚目（Scleractinia）-虫黄藻共生体系中最主流的传播模式为水平传播，但混合传播模式仅存在于垂直传播型珊瑚中，使其既能跨世代维持高度特化的共生关联，也能维系瞬时性的关键共生关系。混合传播模式的此类优势，或可拯救原本易受胁迫的珊瑚，或是强化原本具备抗逆性的珊瑚，具体取决于垂直传播的虫黄藻系统型（phylotype）的其他属性。本研究旨在探究垂直传播的共生体是否往往具备更强的耐热性与宿主特异性。由于性状间的显著关联可能因共享演化历史的模式被高估或掩盖，我们为涵盖A-F演化支（clade）的97个虫黄藻系统型构建了全新的分子系统发育树，以评估系统型传播模式、耐热性与珊瑚宿主特异性之间的关联。在虫黄藻的演化历史中，耐热性与宿主特异性已被多次独立演化获得，且无法通过其所属演化支进行预测。即便虫黄藻系统型的耐热性与宿主特异性并无关联，但在耐热性与特异性的观测增长范围内，以垂直传播为主的系统型出现概率提升了200%以上。垂直传播的虫黄藻所具备的更高耐热性与宿主特异性，或可增强垂直传播型珊瑚的抗白化能力，进而强化混合传播模式的潜在优势。
