Varieties of Living Things: Life at the Intersection of Lineage and Metabolism

Abstract

We address three fundamental questions: What does it mean for an entity to be living? What is the role of inter-organismic collaboration in evolution? What is a biological individual? Our central argument is that life arises when lineage-forming entities collaborate in metabolism. By conceiving of metabolism as a collaborative process performed by functional wholes, which are associations of a variety of lineage-forming entities, we avoid the standard tension between reproduction and metabolism in discussions of life-a tension particularly evident in discussions of whether viruses are alive. Our perspective assumes no sharp distinction between life and non-life, and does not equate life exclusively with cellular or organismal status. We reach this conclusion through an analysis of the capabilities of a spectrum of biological entities, in which we include the pivotal case of viruses as well as prions, plasmids, organelles, intracellular and extracellular symbionts, unicellular and multicellular life-forms. The usual criterion for classifying many of the entities of our continuum as non-living is autonomy. This emphasis on autonomy is problematic, however, because even paradigmatic biological individuals, such as large animals, are dependent on symbiotic associations with many other organisms. These composite individuals constitute the metabolic wholes on which selection acts. Finally, our account treats cooperation and competition not as polar opposites but as points on a continuum of collaboration. We suggest that competitive relations are a transitional state, with multi-lineage metabolic wholes eventually outcompeting selfish competitors, and that this process sometimes leads to the emergence of new types or levels of wholes. Our view of life as a continuum of variably structured collaborative systems leaves open the possibility that a variety of forms of organized matter-from chemical systems to ecosystems-might be usefully understood as living entities. KEYWORDS Living • Non-living • Collaboration • Lineage Formation • Metabolic Whole • Autonomy It would seem that 60 years after Erwin Schrödinger wrote his book 'What is Life?' we should be able to answer the question. However, Nature never ceases to challenge the limits of our imagination.-M. Y. Galperin (2005, 149) This essay will not attempt to provide a definition that answers Schrödinger's question. We shall instead address it by describing a spectrum of biological entities that illustrates why no sharp dividing line between living and non-living things is likely to be useful. The more positive goal of these reflections will be to offer a flexible view of life that does in fact make good sense of why particular organizations of matter can be