Lipid membranes are a ubiquitous structure in biology and would have been an essential component of the first cells. In the absence of evolved cellular machinery, early membranes had to be capable of growth, division, and solute transport by intrinsic physical processes. We have used a combination of spectroscopic and physical methods to characterize the phase properties of fatty acids and related single-chain lipids, which have been proposed to serve a role as primitive membrane lipids. We found that low concentration vesicle solution feature significant amounts of coexisting micelles, while high concentration solutions were predominantly lamellar (vesicles). This concentration-dependent equilibrium allowed us to drive the growth of pre-existing vesicles by gentle solution evaporation, which raises the lipid concentration thus favoring lamellar incorporation. This phenomenon could have provided a mechanism for early cell membrane growth driven entirely by environmental fluctuations.We have also characterized a very different growth mechanism that relies on the inter-vesicle exchange of monomers, which occurs rapidly for single chain lipids. Small amounts of double-chain lipids, such as phospholipids, drive the growth of fatty acid vesicles and the concurrent shrinkage of neighboring vesicles with fewer or no phospholipids. This phenomenon would have provided a direct selective advantage of the adoption of phospholipid-based membranes, a critical step in early cellular evolution. We have found that such a putative transition in lipid composition is accompanied by changes in the physical properties of the membrane, most notably a decrease in membrane fluidity and permeability. These findings support a model in which early cell membranes, composed of single-chain lipids, had the intrinsic permeability to allow for passive solute transport. The subsequent evolution of less permeable, phospholipid membranes would have then allowed for the adoption of protein-based transport machinery and internalized metabolite synthesis.