Evolutionary stalling and a limit on the power of natural selection to improve a cellular module

Evolutionary stalling and a limit on the power of natural selection to improve a cellular module
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进化停滞和自然选择改进蜂窝模块能力的限制

DOI:
10.1073/pnas.1921881117
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发表时间:
2019
影响因子:
11.1
通讯作者:
B. Kacar
B. Kacar
中科院分区:
综合性期刊1区
文献类型:
--
作者:
S. Venkataram;R. Monasky;Shohreh H Sikaroodi;S. Kryazhimskiy;B. Kacar

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重要意义细胞模块,如翻译机(TM),是适应性进化的关键单元,因为适应性取决于它们的性能。在快速进化的种群中,自然选择可能无法同时改进所有模块,因为不同模块中的适应性突变相互竞争。我们假设,尽管存在有益的突变,但某些模块的适应会停滞不前。我们在大肠杆菌实验种群的TM模块中经验性地证明了这种进化停滞。自然选择最初改善了TM,但在TM的性能完全恢复之前,它的重点转移到了其他细胞模块上。这项工作表明,选择重点的快速转移会减缓自然界中单个细胞成分的改善。细胞由执行重要生物学功能的分子模块组成。细胞模块是适应性进化的关键单位,因为生物体的健康状况取决于它们的表现。理论表明,在快速进化的种群中,例如许多微生物的种群,适应主要是由共同的有益突变驱动的,影响很大,而其他突变的行为好像它们实际上是中性的。因此,如果一个模块只能通过罕见和/或微弱的有益突变来改进,它的适应性进化将停滞不前。然而,这种进化停滞还没有得到经验证明,目前还不清楚这种停滞会在多大程度上限制自然选择改进模块的能力。在这里,我们经验地描述了自然选择如何改善翻译机器(TM),这是一个基本的细胞模块。我们用基因扰动的TM对大肠杆菌种群进行了1,000代的实验性进化。有严重TM缺陷的人群最初通过TM突变来适应,但TM适应在大约300代内停滞不前。我们估计,在我们的人群中,由残留的TM缺陷引起的遗传负荷在0.5%到19%之间。最后,我们发现有证据表明,上位性和有益突变池的枯竭都导致了进化停滞。我们的结果表明,尽管存在适应性突变,但自然选择可能不会完全优化细胞模块。
Significance Cellular modules, such as the translation machinery (TM), are key units of adaptive evolution because fitness depends on their performance. In rapidly evolving populations, natural selection may not be able to improve all modules simultaneously because adaptive mutations in different modules compete against each other. We hypothesize that adaptation in some modules would stall, despite the availability of beneficial mutations. We empirically demonstrate such evolutionary stalling in the TM module in experimental populations of Escherichia coli. Natural selection initially improved the TM, but its focus shifted away to other cellular modules before TM’s performance was fully restored. This work shows that rapid shifts in the focus of selection can slow down the improvement of individual cellular components in nature. Cells consist of molecular modules which perform vital biological functions. Cellular modules are key units of adaptive evolution because organismal fitness depends on their performance. Theory shows that in rapidly evolving populations, such as those of many microbes, adaptation is driven primarily by common beneficial mutations with large effects, while other mutations behave as if they are effectively neutral. As a consequence, if a module can be improved only by rare and/or weak beneficial mutations, its adaptive evolution would stall. However, such evolutionary stalling has not been empirically demonstrated, and it is unclear to what extent stalling may limit the power of natural selection to improve modules. Here we empirically characterize how natural selection improves the translation machinery (TM), an essential cellular module. We experimentally evolved populations of Escherichia coli with genetically perturbed TMs for 1,000 generations. Populations with severe TM defects initially adapted via mutations in the TM, but TM adaptation stalled within about 300 generations. We estimate that the genetic load in our populations incurred by residual TM defects ranges from 0.5 to 19%. Finally, we found evidence that both epistasis and the depletion of the pool of beneficial mutations contributed to evolutionary stalling. Our results suggest that cellular modules may not be fully optimized by natural selection despite the availability of adaptive mutations.
微生物生长阶段之间的权衡导致频率依赖和非传递选择。
DOI: 10.1098/rspb.2017.2459
发表时间: 2018
期刊: Proceedings. Biological sciences
影响因子: --
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期刊: PLOS GENETICS
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