Partner switching plays an important role in the evolution of symbiosis, enabling local adaptation and recovery from the breakdown of symbiosis. Because of intergenomic epistasis, partner-switched symbioses may possess novel combinations of phenotypes but may also exhibit low fitness due to their lack of recent coevolutionary history. Here, we examine the structure and mechanisms of intergenomic epistasis in the Paramecium-Chlorella symbiosis and test whether compensatory evolution can rescue initially low fitness partner-switched symbioses. Using partner-switch experiments coupled with metabolomics, we show evidence for intergenomic epistasis wherein low fitness is associated with elevated symbiont stress responses either in dark or high irradiance environments, potentially owing to mismatched light management traits between the host and symbiont genotypes. Experimental evolution under high light conditions revealed that an initially low fitness partner-switched non-native host-symbiont pairing rapidly adapted, gaining fitness equivalent to the native host-symbiont pairing in less than 50 host generations. Compensatory evolution took two alternative routes: either hosts evolved higher symbiont loads to mitigate for their new algal symbiont’s poor performance, or the algal symbionts themselves evolved higher investment in photosynthesis and photoprotective traits to better mitigate light stress. These findings suggest that partner switching combined with rapid compensatory evolution can enable the recovery and local adaptation of symbioses in response to changing environments.

合作伙伴转换在共生关系的演变中发挥着重要作用，使局部适应和从共生关系的崩溃中恢复。由于基因组间的上位性，伴侣转换的共生体可能具有新的表型组合，但由于缺乏最近的共同进化历史，它们也可能表现出低适应度。在这里，我们研究了草履虫-小球藻中基因组上位性的结构和机制共生并测试补偿性进化是否可以拯救最初低适应度的伙伴转换共生体。使用结合代谢组学的伙伴转换实验，我们展示了基因组间上位性的证据，其中低适应度与在黑暗或高辐照度环境中升高的共生体应激反应相关，这可能是由于宿主和共生体基因型之间的光管理特征不匹配。高光条件下的实验进化表明，最初低适应度的伙伴转换的非本地宿主-共生体配对迅速适应，在不到 50 代宿主中获得相当于本地宿主-共生体配对的适应度。补偿性进化采取了两条替代路线：任一宿主进化出更高的共生体负荷以减轻其新藻类共生体的不良性能，或者藻类共生体本身对光合作用和光保护性状进行了更高的投资，以更好地减轻光胁迫。这些发现表明，伴侣转换与快速补偿进化相结合，可以使共生体恢复和局部适应，以应对不断变化的环境。