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

Abstract

Author SummaryCells 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.