Sørensen Megan E S, Wood A Jamie, Cameron Duncan D, Brockhurst Michael A
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK.
Department of Biology, University of York, York YO10 5DD, UK.
Curr Biol. 2021 Sep 13;31(17):3721-3728.e4. doi: 10.1016/j.cub.2021.06.034. Epub 2021 Jul 12.
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.
伙伴切换在共生进化中起着重要作用，它能实现局部适应以及从共生关系的破裂中恢复过来。由于基因组间的上位性，伙伴切换后的共生关系可能拥有新的表型组合，但也可能因其缺乏近期的协同进化历史而表现出低适应性。在此，我们研究了草履虫 - 小球藻共生关系中基因组间上位性的结构和机制，并测试补偿进化是否能够挽救最初适应性较低的伙伴切换后的共生关系。通过结合代谢组学的伙伴切换实验，我们发现了基因组间上位性的证据，即在黑暗或高光照环境中，低适应性与共生体应激反应的升高有关，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所致。在高光条件下的实验进化表明，最初适应性较低的伙伴切换后的非本地宿主 - 共生体配对能够迅速适应，在不到50个宿主世代的时间内获得了与本地宿主 - 共生体配对相当的适应性。补偿进化采取了两种替代途径：要么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佳表现，要么藻类共生体自身进化出对光合作用和光保护特征的更高投入，以更好地减轻光应激。这些发现表明，伙伴切换与快速补偿进化相结合，可以使共生关系在不断变化的环境中实现恢复和局部适应。
