Cycles upon cycles—Temperature scaling of medaka development

How organisms develop in dynamic environmental conditions is a fundamental question. We asked how day-night temperature cycles impact embryonic axis elongation and segmentation, itself a cyclic process linked to the segmentation clock, using the Japanese rice fish medaka. We developed an unbiased dimensional reduction approach, based on Singular Value Decomposition, to reliably identify the dynamic modes of segmentation clock oscillations across all temperature conditions. We reveal that the two major dynamic modes show opposite temperature sensitivities: While the temporal oscillation (mode 1) varies strongly with temperature, the spatial phase gradient (mode 2) appears largely temperature invariant. In addition, we found developmental parameters with intermediate, subscaled temperature responses, such as axis elongation. We used theoretical modeling to understand how dynamic modes emerge from the underlying local oscillation dynamics and axis elongation. We then exposed embryos to circadian and ultradian temperature cycles to reveal dynamic response patterns of oscillations and axis elongation, and found how these responses are integrated into morphological features. Combined, our theoretical–experimental results support a model in which the dynamic integration of temporal (i.e. segmentation clock related) and spatial (i.e. axis elongation) processes, in particular their subscaled temperature response patterns, quantitatively compensate each other to yield a robust, temperature-invariant axis patterning outcome.