Genomic responses to increased temperature and pollinator selection in Brassica rapa L.

Summary

Rapid environmental change reshapes both abiotic stress and biotic interactions, yet it remains unclear how these combined forces structure plants’ genomic adaptation. In particular, the joint influence of temperature and pollinator identity, two ecological axes undergoing simultaneous global shifts, has rarely been quantified at genomic resolution.
We resequenced Brassica rapa L. plants after a six-generation evolution experiment, combining two temperature regimes (ambient vs hot) with three pollination treatments (bumblebee, butterfly, and mixed bumblebee–butterfly), and glasshouse control, to assess how these factors shape genomic responses.
Using multiple complementary statistics (allele-frequency trajectories, F
ST outliers, Cochran–Mantel–Haenszel tests, and local score analyses), we found that adaptive genomic responses differed sharply among pollinators and temperatures: warming strengthened selection in community-level pollination, yielding the clearest signals in the hot-generalised treatment; bumblebee pollination showed strong but drift-obscured genomic change; and butterfly treatments exhibited minimal genomic response.
Our findings demonstrate that pollinator identity and temperature interact nonadditively to produce distinct, highly context-dependent adaptive trajectories. This work highlights the importance of accounting for demographic variation and ecological complexity when predicting evolutionary responses to climate-driven shifts in species interactions.

摘要

剧烈的气候变化同时影响着非生物以及生物间的互作关系,然而植物基因组如何响应这些因素的协同效应,目前仍不明确。特别是温度和传粉者类型这两个正经历全球性变化的生态轴,它们的联合作用很少在开花植物的基因组上得到量化研究。
基于此,我们以油菜Brassica rapa L. 人工选育的快速代际品种(两月种子-种子生长周期)为材料,进行了一项持续六代的演化实验,结合两种温度处理(常温与高温)和三种传粉处理(单一熊蜂传粉、单一蝴蝶传粉以及蝴蝶幼虫的植食性拮抗阶段、熊蜂-蝴蝶混合传粉+蝴蝶幼虫阶段),并以温室条件下人工授粉作为对照。随后对所有植株进行了初代以及演化后的全基因组重测序,以量化植物基因组响应不同环境因素的选择压。
通过运用多种互补的统计方法(包括起始种群-演化后种群等位基因频率动态变化、FST离群值分析、Cochran–Mantel–Haenszel检验以及Local-score分析),我们发现油菜基因组的适应性响应在不同传粉者和温度处理间存在显著差异:高温强化了混合传粉处理下的选择压力,使得高温-混和传粉处理组产生了最清晰的基因组信号;单一熊蜂传粉处理表现出全基因组水平强烈的变化,但由于有限的有效种群大小,难以区分遗传漂变的作用,掩盖了大部分的选择压下的基因组信号;而蝴蝶传粉处理则显示出微弱的基因组响应。
我们的结果表明,不同的传粉者与温度以非线性叠加的方式相互作用,产生了截然不同且高度依赖于具体情境的适应性演化轨迹。本研究强调,在预测由气候变化驱动的物种间相互作用所引发的适应性演化响应时,必须将有效种群统计变化大小和生态复杂性纳入考量。

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