A careful scrutiny of the dynamics of secretory compartments in the entire eukaryotic world reveals many common themes. The most fundamental theme is that the Golgi apparatus and related structures appear as compartments formed by the act of transporting cargo. The second common theme is the pivotal importance for endomembrane dynamics of shifting back and forth the equilibrium between full and perforated cisternae along the pathway. The third theme is the role of a continuous membrane flow in anterograde transfer of molecules from the endoplasmic reticulum through the Golgi apparatus. The last common theme is the self-regulatory balance between anatomical continuities and discontinuities of the endomembrane system. As this balance depends on secretory activity, it provides a source of morphological variability among cell types or, for a given cell type, according to environmental conditions. Beyond this first source of variability, it appears that divergent strategies pave the evolutionary routes in different eukaryotic kingdoms. These divergent strategies primarily affect the levels of stacking, of stabilization, and of clustering of the Golgi apparatus. They presumably underscore a trade-off between versatility and stability to adapt the secretory function to the degree of environmental variability. Nonequilibrium secretory structures would provide yeasts, and plants to a lesser extent, with the required versatility to cope with ever changing environments, by contrast to the stabler milieu intérieur of homeothermic animals.