Transgenerational effects persist down the maternal line in marine sticklebacks: gene expression matches physiology in a warming ocean

Transgenerational effects can buffer populations against environmental change, yet little is known about underlying mechanisms, their persistence, or the influence of environmental cue timing. We investigated mitochondrial respiratory capacity (MRC) and gene expression of marine sticklebacks that experienced acute or developmental acclimation to simulated ocean warming (21°C) across three generations. Previous work showed that acute acclimation of grandmothers to 21°C led to lower (optimised) offspring MRCs. Here, developmental acclimation of mothers to 21°C led to higher, but more efficient offspring MRCs. Offspring with a 21°Cx17°C grandmother-mother environment mismatch showed metabolic compensation: their MRCs were as low as offspring with a 17°C thermal history across generations. Transcriptional analyses showed primarily maternal but also grandmaternal environment effects: genes involved in metabolism and mitochondrial protein biosynthesis were differentially expressed when mothers developed at 21°C, whereas 21°C grandmothers influenced genes involved in hemostasis and apoptosis. Genes involved in mitochondrial respiration all showed higher expression when mothers developed at 21° and lower expression in the 21°Cx17°C group, matching the phenotypic pattern for MRCs. Our study links transcriptomics to physiology under climate change, and demonstrates that mechanisms underlying transgenerational effects persist across multiple generations with specific outcomes depending on acclimation type and environmental mismatch between generations.

跨代效应可缓冲种群应对环境变化的压力，但目前学界对其潜在作用机制、效应持续性，以及环境线索（environmental cue）的作用时机仍缺乏深入认知。本研究以历经三代急性驯化或发育驯化至模拟海洋变暖（21℃）环境的海棘鱼为研究对象，对其线粒体呼吸容量（mitochondrial respiratory capacity, MRC）与基因表达展开了探究。既往研究表明，祖母代接受21℃急性驯化后，其后代的线粒体呼吸容量更低，但处于优化后的水平。本研究发现，母代在21℃环境中进行发育驯化后，其后代的线粒体呼吸容量更高，但代谢效率更为优异。当祖母与母代的环境存在21℃×17℃的不匹配时，后代会出现代谢补偿现象：其线粒体呼吸容量与历代均处于17℃热环境的后代相当。转录组分析结果显示，环境效应主要源自母代，同时也受祖母代环境的影响：当母代在21℃环境下发育时，参与代谢与线粒体蛋白质生物合成的基因会出现差异表达；而祖母代处于21℃环境时，则会影响参与止血与细胞凋亡的基因的表达。所有参与线粒体呼吸作用的基因，在母代于21℃环境发育时均呈现更高的表达量，而在21℃×17℃组中表达量更低，这与线粒体呼吸容量的表型变化规律一致。本研究将转录组学与气候变化下的生理特征建立了关联，并证实跨代效应的潜在机制可在多代间延续，且最终的具体效应取决于驯化类型以及代际间的环境不匹配程度。