Abstract
BackgroundExtensive variation in early gap gene expression in the Drosophila blastoderm is reduced over time because of gap gene cross regulation. This phenomenon is a manifestation of canalization, the ability of an organism to produce a consistent phenotype despite variations in genotype or environment. The canalization of gap gene expression can be understood as arising from the actions of attractors in the gap gene dynamical system.ResultsIn order to better understand the processes of developmental robustness and canalization in the early Drosophila embryo, we investigated the dynamical effects of varying spatial profiles of Bicoid protein concentration on the formation of the expression border of the gap gene hunchback. At several positions on the anterior-posterior axis of the embryo, we analyzed attractors and their basins of attraction in a dynamical model describing expression of four gap genes with the Bicoid concentration profile accounted as a given input in the model equations. This model was tested against a family of Bicoid gradients obtained from individual embryos. These gradients were normalized by two independent methods, which are based on distinct biological hypotheses and provide different magnitudes for Bicoid spatial variability. We showed how the border formation is dictated by the biological initial conditions (the concentration gradient of maternal Hunchback protein) being attracted to specific attracting sets in a local vicinity of the border. Different types of these attracting sets (point attractors or one dimensional attracting manifolds) define several possible mechanisms of border formation. The hunchback border formation is associated with intersection of the spatial gradient of the maternal Hunchback protein and a boundary between the attraction basins of two different point attractors. We demonstrated how the positional variability for hunchback is related to the corresponding variability of the basin boundaries. The observed reduction in variability of the hunchback gene expression can be accounted for by specific geometrical properties of the basin boundaries.ConclusionWe clarified the mechanisms of gap gene expression canalization in early Drosophila embryos. These mechanisms were specified in the case of hunchback in well defined terms of the dynamical system theory.
Highlights
Extensive variation in early gap gene expression in the Drosophila blastoderm is reduced over time because of gap gene cross regulation
In this paper we extend the dynamical analysis to multiple Bcd gradients, revealing additional dynamical mechanisms which work in a coordinated manner to reduce variance
For the median Bcd profile, the gap gene expression patterns generated by Eqs. (2) from 35% to 71% embryo length (EL) occur in the same order and locations as those generated by the full model equations (1)
Summary
Extensive variation in early gap gene expression in the Drosophila blastoderm is reduced over time because of gap gene cross regulation. This phenomenon is a manifestation of canalization, the ability of an organism to produce a consistent phenotype despite variations in genotype or environment. Development is surprisingly robust to environmental stress, intrinsic fluctuations, and genetic variability in populations. These facts, together with the observation that cell type is a discrete rather than continuous property, led C. Waddington will buffer the phenotypic consequences of these variations. Even under larger changes over evolutionary time, the tendency of the system to stay close to the valley floors will preserve and buffer developmental pathways in the face of evolutionary change
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