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
中科院分区:
文献类型:
--
作者:
Goldsby HJ;Knoester DB;Ofria C;Kerr B
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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影响因子:
2
作者:
HAMILTON, WD
通讯作者:
HAMILTON, WD
DOI:
10.1073/pnas.0702723104
发表时间:
2007-05-22
影响因子:
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影响因子:
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通讯作者:
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影响因子:
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作者:
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