Phylogenetic analysis of symbiont transmission mechanisms reveal evolutionary patterns in thermotolerance and host specificity that enhance bleaching resistance among vertically transmitted Symbiodinium

Vertical transmission of Symbiodinium 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–Symbiodinium 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 Symbiodinium 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 Symbiodinium 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 Symbiodinium, 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 Symbiodinium may contribute to robust bleaching resistance among vertically transmitting corals that could reinforce the potential benefits of mixed-modes transmission.

关于珊瑚宿主代际间垂直传播Symbiodinium共生体的假设，认为其可能导致宿主与共生体生理机能的更优匹配，并形成对热应激通常更具抵抗力的全生物体。另一方面，水平传播，凭借其组装生理多样性关联的更大潜力以及能够对刺激作出替代共生体的能力，可能导致对热应激通常更具抵抗力的全生物体。尽管在珊瑚-共生体共生关系中，最普遍的传播方式是水平传播，但混合模式传播仅在垂直传播的珊瑚中发生，这允许在代际间维持高度专业化的关联以及暂时的关键关系。混合模式传播的这些优势可能有助于拯救本应易受影响的珊瑚，或相反，加强本应具有抵抗力的珊瑚，这取决于垂直传播的Symbiodinium谱系的其它属性。在此，我们探讨垂直传播的共生体是否倾向于具有更高的热耐受性和特异性。由于显著特征之间的关系可能被共享的进化历史模式高估或掩盖，我们推断出代表谱系A-F的97个Symbiodinium谱型的全新分子系统发育，以评估谱型传播模式、热耐受性和对珊瑚宿主的特异性之间的关系。热耐受性和特异性在Symbiodinium的进化历史中独立衍生多次，不能由谱系成员资格预测。随着热耐受性和特异性观察范围的扩大，谱型垂直传播的概率增加了超过200%，尽管谱型热耐受性与宿主特异性不相关。垂直传播的Symbiodinium具有更高的热耐受性和特异性，可能有助于垂直传播珊瑚中稳健的白化抵抗能力，从而强化混合模式传播的潜在益处。