An inverse relationship between temperature during ontogeny and final body size is widespread in ectotherms, but poorly understood. Evidence suggests that within organs, this "temperature-size rule" (TSR) may also apply to cell size with no change in numbers. So how closely do reductions in size and number of cells and other repeated structures correlate with size reduction at higher levels of organization? We examine this in the context of a proposal that size and/or number changes at various organizational levels are adaptive responses to temperature- and size-dependent oxygen supply. We subjected two clones of the modular colonial bryozoan, Celleporella hyalina, to orthogonal combinations of two temperatures and two oxygen concentrations during ontogeny, observing effects on sizes of colonies and larvae, and sizes and numbers of cells, tentacles, and modules (autozooids). We found that the size:number responses varied among cell types and among structures at different levels of organization, with the inverse temperature-size relationship applying only to larval parenchymal cells and colony modules. Using our findings and other evidence we propose a unifying adaptive hypothesis that predicts how temperature affects the sizes of mitochondria, cells, organs, modules and organisms, and their relationships with processes that determine the functional capacity of aerobic metabolism.