Temporal scaling in C. elegans larval development

Abstract

Significance An enduring mystery of development is how its timing is controlled, particularly for development after birth, where timing is highly flexible and depends on environmental conditions, such as food availability and diet. We followed timing of cell- and organism-level events in individual Caenorhabditis elegans larvae developing from hatching to adulthood, uncovering widespread variations in event timing, both between isogenic individuals in the same environment and when changing conditions and genotypes. However, in almost all cases, we found that events occurred at the same time, when time was rescaled by the duration of development measured in each individual. This observation of “temporal scaling” poses strong constraints on models to explain timing of larval development.

Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans

“…Our observations of coupled growth and development are consistent with the observation that the temporal spacing of different morphologically defined events of C. elegans development scale proportionally among individuals 52 . Our model further suggests that the time between developmental events is determined by the rate of exponential growth of an individual.…”

“…According to this latter model, the coupling of growth and development is a continuous process that occurs throughout each larval stage, rather than a singular event occurring at the larval moult. Such continuous coupling is also consistent with proportional scaling of developmental events among individuals 52 and the temporal scaling of gene expression oscillations at reduced temperature 24 .…”

Critical slowing down may account for the robustness of development

“…From the limited data in Filina et al. ( 2 ) it appears that this is also valid for the developmental rate of C. elegans (defined as the inverse of the development duration T S ) ( Fig. 1 ).…”

“…In PNAS, Filina et al. ( 2 ) show that this is valid also in the development of Caenorhabditis elegans when the stage of development is defined relative to the overall developmental time, a property they call “temporal scaling.” We would like to point out here that this robustness could be a result of development occurring near a critical point, where all rates scale as θ − θ c , where θ is some external variable. Particularly, if development occurs near a critical temperature T c all developmental rates (growth rate, oscillatory frequencies, gene expression dynamics, etc.)…”

“… The developmental rate r of C. elegans (defined as the inverse of the developmental duration T S ) as a function of temperature [red points are data from Filina et al. ( 2 )] and a linear best fit (blue dots). Compare with the developmental rate of the fruit fly ( B. carambolae ) egg [brown points are data from Danjuma et al.…”