To understand the emergence of Darwinian evolution, it is necessary to identify physical mechanisms that enabled primitive cells to compete with one another. Whereas all modern cell membranes are composed primarily of diacyl or dialkyl glycerol phospholipids, the first cell membranes are thought to have self-assembled from simple, single-chain lipids synthesized in the environment. We asked what selective advantage could have driven the transition from primitive to modern membranes, especially during early stages characterized by low levels of membrane phospholipid. Here we demonstrate that surprisingly low levels of phospholipids can drive protocell membrane growth during competition for single-chain lipids. Growth results from the decreasing fatty acid efflux from membranes with increasing phospholipid content. The ability to synthesize phospholipids from single-chain substrates would have therefore been highly advantageous for early cells competing for a limited supply of lipids. We show that the resulting increase in membrane phospholipid content would have led to a cascade of new selective pressures for the evolution of metabolic and transport machinery to overcome the reduced membrane permeability of diacyl lipid membranes. The evolution of phospholipid membranes could thus have been a deterministic outcome of intrinsic physical processes and a key driving force for early cellular evolution.origin of life | ribozymes | coevolution T he first cell membranes are likely to have formed from simple, single-chain lipids such as short-chain fatty acids and their derivatives that were present in the prebiotic environment (1, 2). Membranes composed of such amphiphiles are permeable to polar nutrients such as nucleotides (3) and feature the dynamic properties necessary for spontaneous growth and division (2, 4). The high permeability of fatty-acid-based membranes is consistent with a heterotrophic model for early cells, in which chemical building blocks are synthesized in the environment and passively diffuse across the cell membrane to participate in replication. All modern cells synthesize phospholipids (or sulfolipids in rare exceptions; refs. 5 and 6) with two hydrophobic chains as their primary membrane lipids. Phospholipid membranes prevent the rapid permeation of ions and polar molecules, allowing modern cells to retain internally synthesized metabolites and to control all import and export. The evolution of phospholipid membranes must have therefore mirrored the emergence of metabolic and transport machinery during early cellular evolution.This transition from single-chain lipids to phospholipids had to be gradual, both to allow for the coevolution of metabolic and transport machinery and because of the initial inefficiency of nascent catalysts (e.g., ribozymes). Hence, the selective advantage associated with phospholipid synthesis had to apply to small differences in phospholipid content in order to drive this transition. What selective advantage could be conferred by the low levels of phospholipid that mus...