The evolutionary origin of somatic cells under the dirty work hypothesis.

The evolutionary origin of somatic cells under the dirty work hypothesis.
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DOI:
10.1371/journal.pbio.1001858
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发表时间:
2014-05
期刊:
影响因子:
9.8
通讯作者:
Kerr B
Kerr B
中科院分区:
生物学1区
文献类型:
--
作者:
Goldsby HJ;Knoester DB;Ofria C;Kerr B

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数字生物体的实验进化表明,与执行有价值的代谢工作相关的诱变副作用可以在多细胞生物体中产生生殖体分化。生殖分工是多细胞生物体的一个标志。然而,产生所描绘的生殖细胞和体细胞的进化压力仍然不清楚。在这里,我们提出一个假设,即与执行代谢工作相关的突变后果有利于这种分化。我们提出了用实验进化的计算形式收集的证据来支持这一假说。我们的数字有机体作为未分化的多细胞个体开始每一次实验,并可以进化出提高其繁殖率的计算功能。当这些功能与适度的诱变效应相关时,我们观察到多细胞生物体内生殖分工的演变。具体地说,一部分细胞将自己从多细胞后代的繁殖体中剔除,同时执行不成比例的大量突变工作,因此被归类为胞体。因此,其他细胞能够扮演细菌的角色,保持静止,从而保护它们的遗传信息。我们分析了成功分化的多细胞生物体的谱系,发现它们表现出意想不到的进化轨迹:细胞首先表现出将代谢工作集中到生殖细胞子集(我们称之为“伪体细胞”)的发育模式,然后进化以消除这些细胞的繁殖潜力,从而将它们转化为实际的体细胞。我们还证明,体细胞的进化使表型策略成为可能,否则未分化的生物不易获得这些表型策略,尽管这些新表型特征的表达通常包括负面副作用,如衰老。生物体内的细胞如果能够成长为一个全新的后代有机体,则被归类为“生殖细胞”,如果它们对身体的功能做出贡献,但本身无法产生后代,则被归类为“胞体”。从进化论的角度来看,重要的是要问为什么以及如何界定多细胞生物体的细胞的繁殖潜力。在这里,我们提出了“肮脏工作假说”,该假说认为生殖体分化是一种适应,允许破坏细胞DNA的代谢工作。Soma有能力完成这项“肮脏的工作”,而生殖细胞必须为未来的多细胞后代保持其DNA的纯净。我们使用数字生物来提供支持这一假说的实验证据,并提出了一条意想不到的进化轨迹:多细胞生物首先进化,在更复杂的发育模式出现之前,将破坏性的代谢工作限制在一个细胞子集(我们将其标记为“伪胞体”),从而允许与适当胞体的生殖分工。最后,我们证明,体细胞允许有机体进化出有价值的功能,否则这些功能对细胞的破坏太大;然而,它们伴随着快速衰老的副作用。类似的压力可能在其他情况下产生了生殖分工,例如在真社会昆虫群体中生殖女王和不育工蚁的分化。
Experimental evolution of digital organisms suggests that mutagenic side effects associated with performing valuable metabolic work can produce germ-soma differentiation in multicellular organisms. Reproductive division of labor is a hallmark of multicellular organisms. However, the evolutionary pressures that give rise to delineated germ and somatic cells remain unclear. Here we propose a hypothesis that the mutagenic consequences associated with performing metabolic work favor such differentiation. We present evidence in support of this hypothesis gathered using a computational form of experimental evolution. Our digital organisms begin each experiment as undifferentiated multicellular individuals, and can evolve computational functions that improve their rate of reproduction. When such functions are associated with moderate mutagenic effects, we observe the evolution of reproductive division of labor within our multicellular organisms. Specifically, a fraction of the cells remove themselves from consideration as propagules for multicellular offspring, while simultaneously performing a disproportionately large amount of mutagenic work, and are thus classified as soma. As a consequence, other cells are able to take on the role of germ, remaining quiescent and thus protecting their genetic information. We analyze the lineages of multicellular organisms that successfully differentiate and discover that they display unforeseen evolutionary trajectories: cells first exhibit developmental patterns that concentrate metabolic work into a subset of germ cells (which we call “pseudo-somatic cells”) and later evolve to eliminate the reproductive potential of these cells and thus convert them to actual soma. We also demonstrate that the evolution of somatic cells enables phenotypic strategies that are otherwise not easily accessible to undifferentiated organisms, though expression of these new phenotypic traits typically includes negative side effects such as aging. Cells within an organism are categorized as “germ” if they are able to grow into a whole new offspring organism or as “soma” if they contribute to the body's functionality but cannot produce an offspring themselves. From an evolutionary perspective, it is important to ask why and how a multicellular organism would demarcate the reproductive potential of its cells. Here we propose the “dirty work hypothesis,” which argues that germ–soma differentiation is an adaptation to allow metabolic work that damages a cell's DNA. Soma can afford to perform this “dirty work,” while germ cells must keep their DNA pristine for future multicellular offspring. We use digital organisms to provide experimental evidence in support of this hypothesis and present an unexpected evolutionary trajectory: multicellular organisms first evolve to confine damaging metabolic work to a subset of cells (which we label “pseudo-soma”) before more complex developmental patterns arise that allow for reproductive division of labor with a proper soma. Finally, we demonstrate that somatic cells allow organisms to evolve valuable functions that are otherwise too damaging to cells; however, they come with the side effect of rapid aging. Similar pressures may have produced reproductive division of labor in other contexts, such as the differentiation of reproductive queens and sterile workers in eusocial insect colonies.
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发表时间: 1964-01-01
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