Abstract
All forms of life are confronted with environmental and genetic perturbations, making phenotypic robustness an important characteristic of life. Although development has long been viewed as a key component of phenotypic robustness, the underlying mechanism is unclear. Here we report that the determinative developmental cell lineages of two protostomes and one deuterostome are structured such that the resulting cellular compositions of the organisms are only modestly affected by cell deaths. Several features of the cell lineages, including their shallowness, topology, early ontogenic appearances of rare cells, and non-clonality of most cell types, underlie the robustness. Simple simulations of cell lineage evolution demonstrate the possibility that the observed robustness arose as an adaptation in the face of random cell deaths in development. These results reveal general organizing principles of determinative developmental cell lineages and a conceptually new mechanism of phenotypic robustness, both of which have important implications for development and evolution.
Highlights
Phenotypic robustness, often referred to as canalization, is the phenomenon that a phenotypic trait is invariant in the face of environmental or genetic perturbations [1,2,3,4,5,6,7]
Even in largely regulative embryos, one finds determinative development [20], where the developmental process and cell fate are fixed. Especially those of mollusks [21], annelids [22], tunicates [23], and nematodes [24,25], determinative development is extensively observed [20]. How do these species deal with environmental or genetic perturbations in ontogenesis? To answer this question, we investigate the ontogenic robustness of three invertebrates dominated by determinative development, using developmental cell lineages that describe the exact genealogical relations of all cells of an individual embryo or adult
It is widely believed that development plays an important role in the phenotypic robustness of organisms to environmental and genetic perturbations
Summary
Phenotypic robustness, often referred to as canalization, is the phenomenon that a phenotypic trait is invariant in the face of environmental or genetic perturbations [1,2,3,4,5,6,7]. The genetic basis of phenotypic robustness has been of longstanding interest, and several underlying mechanisms have been elucidated [2,3,5]. Functional redundancy in genetic systems is another cause of robustness because it renders the phenotype of an organism relatively invariant to the loss of a genetic component. Such redundancies are known to exist at both the individual gene level (e.g., between duplicate genes) [11] and the systems level (e.g., between alternative metabolic pathways) [5,12]. Other proposed mechanisms of robustness include expression regulation via transcriptional regulatory networks [16], posttranscriptional regulation by microRNA [17,18], and certain feedback/feed-forward circuits in signaling among cells [19]
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