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The evolutionary scaling of cellular traits imposed by the drift barrier

Significance Owing to internal homeostatic mechanisms, cellular traits may experience long periods of stable selective pressures. Nonetheless, drift and mutation still conspire to generate significant variation in mean phenotypes among phylogenetic lineages. Provided there are classes of mutations with sufficiently small effects, even in the face of constant selection, variation in genetic effective population sizes will result in gradients of mean phenotypes with respect to organism size across the tree of life. Mutation is an important determinant of such patterns, even in the absence of directional bias. Thus, a substantial amount of variation in cellular features may be a simple consequence of lineage-specific differences in the power of drift rather than a reflection of adaptive divergence. Owing to internal homeostatic mechanisms, cellular traits may experience long periods of stable selective pressures, during which the stochastic forces of drift and mutation conspire to generate variation. However, even in the face of invariant selection, the drift barrier defined by the genetic effective population size, which is negatively associated with organism size, can have a substantial influence on the location and dispersion of the long-term steady-state distribution of mean phenotypes. In addition, for multilocus traits, the multiplicity of alternative, functionally equivalent states can draw mean phenotypes away from selective optima, even in the absence of mutation bias. Using a framework for traits with an additive genetic basis, it is shown that 1) optimal phenotypic states may be only rarely achieved; 2) gradients of mean phenotypes with respect to organism size (i.e., allometric relationships) are likely to be molded by differences in the power of random genetic drift across the tree of life; and 3) for any particular set of population-genetic conditions, significant variation in mean phenotypes may exist among lineages exposed to identical selection pressures. These results provide a potentially useful framework for understanding numerous aspects of cellular diversification and illustrate the risks of interpreting such variation in a purely adaptive framework.