Morphogenesis and form · Article

Segment formation by oscillating dynamics versus gene expression transients

One uses a complex transient in gene expression. Ten Tusscher and Hogeweg compared evolved networks of both kinds and reported that the oscillating kind was more robust and more evolvable¹³. Grodstein and colleagues note that the clock-and-wavefront model typically requires a global clock⁷. They proposed a model whose measuring waves do not require a clock⁸. McMillen and Levin describe the vertebrate clock as a case of collective behaviour⁹.

Earliest held: 2011, Ten Tusscher KH, Hogeweg P
Most discussed in: Evolution of networks for body plan…, 2011
In the library: 44 passages in 8 works
Rewritten: 2026-11-04

Two network types

Ten Tusscher and Hogeweg (2011) studied evolved networks for body plan patterning and sorted them into two kinds. SS networks make both segments and domains from a complex gene expression time transient¹. SF networks use a similar transient to make domains, but rely on oscillatory dynamics to make regularly sized segments². They reported that SF networks are more robust and more evolvable³. Purely architectural methods found no difference in modularity between the two kinds. The authors left open whether SF networks are truly not more modular, or whether those methods miss some type of modularity³.

The clock in embryos

Pai and colleagues (2012) noted consistent differences in the timing of bilateral transcriptional waves that drive the segmentation clock of somitogenesis⁴. Herrera-Rincon and colleagues (2017) described the clock and wavefront model for Xenopus. In it, presomitic mesoderm cells oscillate between permissive and nonpermissive conditions for segmentation⁶. They listed Wnt, Shh, BMP, Fgf and Notch pathways as regulators of the clock, and asked whether innervation might help orchestrate somitogenesis⁶. Baluška and Levin (2016) said root apex transition zones, where cells oscillate in almost all their activities, resemble presomitic mesoderm clocks⁵.

Is a clock required

Grodstein, McMillen and Levin (2023) traced the clock-and-wavefront model to Cooke and Zeeman (1976). They said it typically requires a global clock, though some versions avoid this and have a reaction-diffusion flavour⁷. They wrote that many details of the segmentation clock remain unknown, including the reasons for its robustness. They proposed a model whose waves perform measurement and do not require a clock⁸. Their view differs from the clock-centred account.

Collective behaviour

McMillen and Levin (2024) used the clock as an example of collective behaviour. They cited earlier studies showing that presomitic mesoderm cells do not oscillate when cultured alone, but resume oscillating when cultured together⁹. They also cited prior grafting experiments showing that wild type cells grafted into non-cycling mutant fish express her1 without cycling it⁹.

SourcesEach quotation was checked word for word against the passage it opens.

SS networks generate both segments and domains from a complex gene expression time transient, whereas SF networks use a complex time transient to generate domains and oscillating dynamics to generate segments.Ten Tusscher KH, Hogeweg P, 2011 · Evolution of networks for body plan patterning; interplay of modularity… · open at passage 46
SF networks use a similar complex time transient to produce domains, while using oscillatory dynamics to produce regularly sized segments.Ten Tusscher KH, Hogeweg P, 2011 · Evolution of networks for body plan patterning; interplay of modularity… · open at passage 34
Furthermore, SF networks are more robust and more evolvable. Still, no differences in network modularity were found using frequently used, purely architectural methods.Ten Tusscher KH, Hogeweg P, 2011 · Evolution of networks for body plan patterning; interplay of modularity… · open at passage 46
consistent differences in the timing of highly dynamic bilateral transcriptional waves that drive the segmentation clock of somitogenesisPai VP, Vandenberg LN, Blackiston D, Levin M, 2012 · Neurally Derived Tissues in Xenopus laevis Embryos Exhibit a Consistent… · open at passage 4
These root apex transition zones resemble presomitic mesoderm segmentation clocks underlying vertebrate embryo segmentationBaluška F, Levin M, 2016 · On Having No Head: Cognition throughout Biological Systems · open at passage 34
the presomitic mesodermal cells dynamically oscillate between permissive and nonpermissive conditions for segmentation (clock)Herrera-Rincon C, Herrera-Rincon C, Pai VP, Moran KM…, 2017 · The brain is required for normal muscle and nerve patterning during early… · open at passage 4
It originated as the clock-and-wavefront model (Cooke and Zeeman, 1976; Tabin and Johnson, 2001) and typically requires a global clockGrodstein J, McMillen P, Levin M, 2023 · Closing the loop on morphogenesis: a mathematical model of morphogenesis by… · open at passage 19
Despite decades of research, many details of the segmentation clock–including reasons for its robustness–remain unknown.Grodstein J, McMillen P, Levin M, 2023 · Closing the loop on morphogenesis: a mathematical model of morphogenesis by… · open at passage 21
Similarly, pre-somitic mesoderm cells do not oscillate when cultured independently, but will resume oscillating when cultured collectivelyMcMillen P, Levin M, 2024 · Collective intelligence: A unifying concept for integrating biology across… · open at passage 25

Linked ideas

Segmentation and identity-domain patterning in body planspart of / contains

Covers segments and domains generally; this article concerns the two mechanisms, transient or oscillator, that can produce the segments.

Hox colinearity, somitogenesis clock and morphogen wavefrontrelated to

Treats the somitogenesis clock alongside Hox expression order; this article compares clock-based and transient-based routes to segments.

Evolvabilityrelated to

Ten Tusscher and Hogeweg reported that SF networks, with oscillating segment formation, were more evolvable than SS networks.

Modularity of developmental gene regulatory networksrelated to

The 2011 study asked whether SF networks are more modular and found no difference with architectural methods.

Turing patterns, reaction-diffusion and autocatalysisin tension with

Grodstein and colleagues note some clock models have a reaction-diffusion flavour, while their own model measures with waves and needs no clock.

Collective intelligence of cellsrelated to

McMillen and Levin cite the segmentation clock as collective behaviour, since cells oscillate together but not alone.

Evolution of segmentation and expression domains in body plan patterningrelated to

Both concern vertebrate segment formation. The passages describe the oscillator route (segmentation clock, clock-and-wavefront, Notch/hairy waves, one version without a global clock), but say nothing about transients or evolutionary models.

Evolution of modularity in regulatory networksrelated to

The passage tests whether modularity evolves in GRNs by selecting simulated networks for segmentation and differentiation. It never mentions oscillators or expression transients, so the link is only through segmentation.

Pleiotropy and its reduction by modularityrelated to

Passage links segmentation dynamics (B) to modularity (A): different expression dynamics suggested SF networks might be more modular, but architectural scores showed both non-modular. Pleiotropy is not mentioned.

Where it is discussedPassages matching segmentation clock, oscillating dynamics, gene expression time transient, segments and domains

2011	Evolution of networks for body plan patterning; interplay of modularity… · Ten Tusscher KH, Hogeweg P	31
2024	Collective intelligence: A unifying concept for integrating biology across… · McMillen P, Levin M	3
2022	Information Theory as an Experimental Tool for Integrating Disparate… · McMillen P, Walker SI, Levin M	3
2023	Closing the loop on morphogenesis: a mathematical model of morphogenesis by… · Grodstein J, McMillen P, Levin M	3
2012	Neurally Derived Tissues in Xenopus laevis Embryos Exhibit a Consistent… · Pai VP, Vandenberg LN, Blackiston D…	1
2017	The brain is required for normal muscle and nerve patterning during early… · Herrera-Rincon C, Herrera-Rincon C, Pai…	1
2013	Root apex transition zone as oscillatory zone · Baluška F, Mancuso S	1
2016	On Having No Head: Cognition throughout Biological Systems · Baluška F, Levin M	1