Morphogenic machines evolve more rapidly than the signals that pattern them: lessons from amphibians

Shook, David; Keller, Ray

doi:10.1002/jez.b.21204

Cited by 20 publications

(17 citation statements)

References 205 publications

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“…Lastly, on the tissue scale the classical processes of secondary induction may serve to signal the success of a particular tissue movement or elicit further morphogenetic movements. The molecular and cellular scale processes that provide feedback from the mechanical processes of morphogenesis are poorly understood and their resolution will provide deeper insights into many larger questions in evolution as well as the nature of disease liability and birth defects 42,95–97 .…”

Section: Mechanics Feedback and Robust Programs Of Developmentmentioning

confidence: 99%

The interplay between cell signalling and mechanics in developmental processes

2013

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Force and stress production within embryos and organisms are crucial physical processes that direct morphogenesis. In addition, there is mounting evidence that biomechanical cues created by these processes guide cell behaviors and cell fates. Here we review key roles for biomechanics during development to directly shape tissues, provide positional information for cell fate decisions, and enable robust programs of development. Several recently identified molecular mechanisms suggest how cells and tissues might coordinate their responses to biomechanical cues. Lastly, we outline long-term challenges in integrating biomechanics with genetic analysis of developing embryos.

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Section: Mechanics Feedback and Robust Programs Of Developmentmentioning

confidence: 99%

The interplay between cell signalling and mechanics in developmental processes

2013

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“…Thus, it is likely that the spatial distribution of the cells that receive these signals depends on how morphogenetic mechanisms move them, and on how they move and deform the signalling territories (thus affecting, over time, the spatial distribution of the cells that receive a signal). As such, vertebrate gastrulation probably uses strong morphodynamic mechanisms (Shook and Keller, 2008).…”

Section: Type E: Vertebratesmentioning

confidence: 99%

“…Except for mammals, this variation seems to involve, mainly, the amount of yolk. This does not necessarily have dramatic effects on adult morphology (del Pino and Elinson, 1983;del Pino, 1989;del Pino and Loor-Vela, 1990), although the morphogenetic movements involved can be quite different (Shook and Keller, 2008).…”

Section: Type E: Vertebratesmentioning

confidence: 99%

Morphological evolution and embryonic developmental diversity in metazoa

Salazar‐Ciudad

2010

Development

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SummaryMost studies of pattern formation and morphogenesis in metazoans focus on a small number of model species, despite the fact that information about a wide range of species and developmental stages has accumulated in recent years. By contrast, this article attempts to use this broad knowledge base to arrive at a classification of developmental types through which metazoan body plans are generated. This classification scheme pays particular attention to the diverse ways by which cell signalling and morphogenetic movements depend on each other, and leads to several testable hypotheses regarding morphological variation within and between species, as well as metazoan evolution. Key words: Pattern formation, Morphogenesis, Body plan evolution, Evolution of development, Mechanisms of development IntroductionThe conservation of developmental processes, especially that of genes and gene expression patterns (Gilbert, 2006; Carroll, 2001), has traditionally received a lot of attention in evolutionary developmental biology. Differences at the level of genes and gene interactions among metazoan groups have also been studied (Lynch and Wagner, 2008). However, few studies have integrated the available information about different stages of development to understand the commonalities and differences in the overall process of development among metazoa. Earlier work identified gross developmental similarities and differences between metazoan groups that led to their classification into three types of development (Davidson, 1991;Davidson et al., 1995;Wray, 2000). These similarities in development are suggested to relate to similarities in the body plan or in the life cycle of the different species.This article introduces a classification scheme that incorporates the information about additional species and about later stages of development that has accumulated since the publication of these previous reviews. I also propose new hypotheses about the relationship between signalling and morphogenetic movements in the classification of developmental types. Particular attention is given to the distinction between morphostatic and morphodynamic developmental mechanisms (Salazar-Ciudad et al., 2003). In morphostatic mechanisms, major signalling events occur before the onset of morphogenetic movements, whereas in morphodynamic mechanisms, cell signalling and morphogenetic mechanisms occur at the same time or in a closely interlinked manner (Fig. 1). Previous work (Salazar-Ciudad and Jernvall, 2004) suggests that this distinction has important implications for our understanding of developmental dynamics and for how development affects evolution. However, this previous work focused on individual developmental mechanisms that act only between specific developmental stages. Here, the focus is not on specific stages, but instead on the entire period of development. Thus, the previous classifications are revised to take into account the diversity of events in metazoa over the course of development. On the basis of the relative timing and of...

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“…Although all pattern transformations in development can be said to be done by developmental mechanisms a specifi c pattern transformation can be equally realisable by different developmental mechanisms. Indeed, it has been extensively shown that different developmental mechanisms underlie very similar morphologies in different species (Müller 2007;Shook and Keller 2008) or even in the same individual (Catala et al 1995). On the other hand a developmental mechanism does not always produce the same pattern transformation.…”

Section: Variational Propertiesmentioning

confidence: 98%

Looking at the origin of phenotypic variation from pattern formation gene networks

Salazar‐Ciudad¹

2009

J Biosci

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This article critically reviews some widespread views about the overall functioning of development. Special attention is devoted to views in developmental genetics about the superstructure of developmental gene networks. According to these views gene networks are hierarchic and multilayered. The highest layers partition the embryo in large coarse areas and control downstream genes that subsequently subdivide the embryo into smaller and smaller areas. These views are criticized on the bases of developmental and evolutionary arguments. First, these views, although detailed at the level of gene identities, do not incorporate morphogenetic mechanisms nor do they try to explain how morphology changes during development. Often, they assume that morphogenetic mechanisms are subordinate to cell signaling events. This is in contradiction to the evidence reviewed herein. Experimental evidence on pattern formation also contradicts the view that developmental gene networks are hierarchically multilayered and that their functioning is decodable from promoter analysis. Simple evolutionary arguments suggest that, indeed, developmental gene networks tend to be non-hierarchic. Re-use leads to extensive modularity in gene networks while developmental drift blurs this modularity. Evolutionary opportunism makes developmental gene networks very dependent on epigenetic factors.

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Morphogenic machines evolve more rapidly than the signals that pattern them: lessons from amphibians

Cited by 20 publications

References 205 publications

The interplay between cell signalling and mechanics in developmental processes

The interplay between cell signalling and mechanics in developmental processes

Morphological evolution and embryonic developmental diversity in metazoa

Looking at the origin of phenotypic variation from pattern formation gene networks

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