A small group of proteins that form core components of electron transfer complexes are consistently encoded by organellar genomes in multicellular organisms, suggesting functional constraint. These genomes are costly to maintain and vulnerable to mutation. We propose that they provide cell lineages with sensors of long-term redox damage, and of bioenergetic and genomic competence. This proposed adaptive function sets tonic retrograde signalling to the nucleus and anterograde responses influencing protective and cell death pathways. The nature of the proposed gain-of-function signalling mechanisms is unclear but could involve defective complex assembly. Organellar proteomes therefore provide cumulative feedback on bioenergetic and genomic status within cell lineages, selection of the energetically 'fittest' cells and a means of removing cells that compromise survival of the organism.