A fool to do your dirty work?

Abstract

Much of life on Earth owes its spectacular success to a rather important evolutionary transition—from single-celled organisms to multicellularity—which has occurred independently in many lineages, enabling the differentiation of cells to perform the highly specialized functions that we see in living fungi, plants, and animals. However, whereas all clones of single-celled organisms have a relatively equal chance of dividing and propagating their genes, most multicellular organisms entrust the propagation of their genes to a few select germline cells amidst a sea of non-reproductive somatic cells. At this point, the fitness of individual cells and the fitness of the entire organism become decoupled. Anytime complexity increases through evolution, one must ask how selection at the lower level of organization (i.e., the individual cell) doesn’t disrupt the integration at higher levels of organization (i.e., a multicellular organism) by favoring selfishness. There are some general evolutionary hypotheses that have been offered to explain why and how multicellularity and the division of labor between somatic and germline cells evolved, as well as the conditions under which these developments would be expected. Clearly, organisms with differentiated cells can experience many fitness advantages, such as the ability to grow larger and exploit novel resources. And along with these advantages come costs, such as the energy and materials that must be allocated towards growth and maintenance, rather than reproduction. However, there are more subtle, but no less important, constraints on an organism’s ability to acquire resources, grow, metabolize, and reproduce that might also influence the evolution of cellular differentiation. One idea that has been suggested, but not yet fully developed, is that the evolution of multicellular organisms with separate somatic and reproductive cells might be influenced by constraints on the preservation of genetic information. Most of the ‘‘work’’ performed by a cell—that is, the production and use of energy—takes place in the mitochondria and chloroplasts (in eukaryotes) or across membranes (in prokaryotes). As a byproduct of this work, reactive oxygen species such as hydrogen peroxide are generated. In turn, these byproducts can create oxidative stress in a cell, one result of which can be mutations to that cell’s DNA. Here, the idea of the so-called ‘‘dirty work’’ hypothesis is that the advent of cellular differentiation allows the organism to separate the energetically costly and potentially mutagenic processes into their somatic cells, while protecting their genomes within germline cells that need perform little work. While this and other theories about the evolution of multicellularity and cellular differentiation are intriguing, empirical evidence is less forthcoming. Some studies in yeasts and cellular slime molds, among others, have provided a few clues. But the time scales necessary to observe and manipulate the processes driving the evolution of cellular differentiation are typically prohibitive. Unless, that is, one could reproduce the evolutionary process in a realistic, but tractable way. That is just what Goldsby et al. did in this issue of PLOS Biology. To explore the role of the dirty work hypothesis in the differentiation of somatic and germline cells, Goldsby et al. performed a series of evolutionary experiments on populations of digital organisms. What’s a digital organism? In this case, digital organisms have a genome that comprises a fully functional computer program. These genetic programs can process numbers that flow into and out of their habitat to perform computational logic functions (e.g., AND, NOT, XOR) which order to gain resources. These genomes mutate at some defined probability, and the organisms differentially survive and reproduce as a function of their ability to acquire resources (i.e., when enough functions are executed). With this basic framework in hand, any number of evolutionary questions can be investigated simply by defining the parameters in which the digital organisms interact. In this case, the authors explored whether and how these simple multicellular individuals make the transition to having non-reproducing somatic cells and reproductive germline cells. They established a series of evolutionary experiments