Abstract
Development is a process precisely coordinated in both space and time. Spatial precision has been quantified in a number of developmental systems, and such data have contributed significantly to our understanding of, for example, morphogen gradient interpretation. However, comparatively little quantitative analysis has been performed on timing and temporal coordination during development. Here, we use Drosophila to explore the temporal robustness of embryonic development within physiologically normal temperatures. We find that development is temporally very precise across a wide range of temperatures in the three Drosophila species investigated. However, we find temperature dependence in the timing of developmental events. A simple model incorporating history dependence can explain the developmental temporal trajectories. Interestingly, history dependence is temperature-specific, with either effective negative or positive feedback at different temperatures. We also find that embryos are surprisingly robust to shifting temperatures during embryogenesis. We further identify differences between tropical and temperate species, potentially due to different mechanisms regulating temporal development that depend on the local environment. Our data show that Drosophila embryonic development is temporally robust across a wide range of temperatures. This robustness shows interesting species-specific differences that are suggestive of different sensitivity to temperature fluctuations between Drosophila species.
Highlights
Multicellular organism development is characterized by the ability to complete morphogenesis with little variation between individuals
If temporal variability in embryonic development is largely due to random variations, we expect the error in timing to increase with developmental time
Our results show that Drosophila temporal development is highly robust across three different species and a wide range of temperatures
Summary
Multicellular organism development is characterized by the ability to complete morphogenesis with little variation between individuals. Quantitative experiments on patterning processes early in embryogenesis have shed light on this level of reproducibility [1,2,3,4]. Coarse gradients are subsequently refined to reach a pattern resolved at the single-cell level [5]. The spatial precision of patterning often remains unaffected in the face of environmental fluctuations within typical physiological ranges. The fly wing vein patterning operates at the physical limit (i.e. at the single-cell level) and that this limit is robust to a wide temperature range [6]. Events during embryogenesis must be tightly coordinated temporally. Exploring temporal reproducibility is essential to gain insights into how development is coordinated and how organisms respond to environmental changes
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