Selfish metabolism

2008 Wiley Periodicals, Inc. Complexity 7: 7–13, 2008 E volutionary biology has traditionally made much of the concept of selfishness. Charles Darwin reduced adaptation (and to a less satisfying degree, speciation) to the heritable variation and competition among individuals. As understanding of the genetic control of heredity and morphogenesis has become more sophisticated, Richard Dawkins has advocated displacing selfishness somewhat, from the organism to its genes. This perspective makes many mathematical aspects of the population genetics of kin selection, viral infection, and genomic imprinting intuitive and natural; though it perhaps underemphasizes the difficulty of apportioning evolutionary credit among genes that act in concert during development. Certain proposals for the RNA world as a first chemical stage of life have even gone so far as to attempt to keep the self while possibly doing away with the cell. Tiny, selfish RNAs in solution or on surfaces are imagined to have competed with one another for replicating potential and raw materials from a transient primordial mixture of organics, much as modern viruses compete with a cell’s host genome for consumption of the cell’s metabolic resources. In all these scenarios, selfishness brings together two very different notions. One is a kind of greediness, in which existing states of order compete to increase their own instantiation at the expense of others. The other is a notion of individuality, whether of the organism, gene, or self-replicating RNA molecule. In Darwin’s theory of evolution, and for many practical applications to modern life, the two are indeed tightly coupled. However, this need not always be so (even today), as evolutionary theorists are coming to recognize whenever viral and host genes define two co-present and incommensurable notions of self, or when they consider that the parentally imprinted haplotype in a diploid organism is both genetically incomplete to make a cell, and yet has an identity that spans multiple generations of organisms. Moreover, certain areas of biology do not seem adequately captured in this selfish paradigm at all. Ecology concerns robust and richly ordered networks of relations, which are not properties of any of the individuals or taxa per se. And it doesn’t help to try to envision ecosystems (Gaia notwithstanding) as super-organisms, because ecosystems don’t obey the mathematics of simple Mendelian heredity and they don’t compete; they pass through sequential forms of relatednesses in a sort of noisy succession. The greedy but non-individualistic nature of ecosystems becomes especially salient if we try to understand the origin of life, because many of the most universal and robust properties of life are more easily visible at the ecosystem level of aggregation than at the level of individual organisms. Perhaps the most striking such universal is the network of reactions that we call core metabolism. As with many familiar concepts in biology, our understanding of what metabolism is continues to change. For most of the past 60 years metabolism has been understood in biochemistry to refer to the metabolic pathways chart first developed by Donald Nicholson in 1955 and constantly updated since that time. Much of the original chart was based on the physiology of humans and HAROLD J. MOROWITZ, ERIC SMITH, AND VIJAYASARATHI SRINIVASAN