Abstract Eukaryotes exhibit a complex and dynamic internal meshwork of membranes—the endomembrane system —used to insert membrane proteins, ingest food, and digest cells and macromolecules. Verbal models explaining the origin of endomembranes abound, but explicit quantitative considerations of fitness are lacking. A wealth of quantitative data on vesicle sizes, local protein abundances, protein residence times at functional loci, nutrient transporter rates, membrane protein insertion rates, etc., have been made available in the past couple of decades. Drawing on these data allows for the derivation of two biologically-grounded analytical models of endomembrane evolution that quantify organismal fitness: 1) vesicle-based uptake of nutrient molecules— pinocytosis , and 2) vesicle-based insertion of membrane proteins— proto-endoplasmic reticulum . Surprisingly, pinocytosis doesn’t provide a net fitness gain under biologically sensible parameter ranges. Explaining why it is primarily used for protein, and not small molecule, uptake in contemporary organisms. The proto-endoplasmic reticulum does provide net fitness gains, making it the more likely candidate for initiating the origin of the endomembrane system. With modifications, the approach developed here can be used to understand the present-day endomembrane system and to further flesh out the cell-level fitness landscape of endomembranes and illuminate the origin of the eukaryotic cell.
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