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An Explanatory Evo-Devo Model for the Developmental Hourglass[Version 1; Peer Review: 1 Approved, 2 Approved with Reservations]

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An Explanatory Evo-Devo Model for the Developmental Hourglass[Version 1; Peer Review: 1 Approved, 2 Approved with Reservations] F1000Research 2014, 3:156 Last updated: 16 MAY 2019 RESEARCH ARTICLE An explanatory evo-devo model for the developmental hourglass [version 1; peer review: 1 approved, 2 approved with reservations] Saamer Akhshabi1, Shrutii Sarda2, Constantine Dovrolis1, Soojin Yi3 1School of Computer Science, Georgia Institute of Technology, Atlanta, GA, 30332, USA 2Center for Bioinformatics and Computational Biology, University of Maryland, College Park, MD, 20740, USA 3School of Biology, Georgia Institute of Technology, Atlanta, GA, 30332, USA First published: 08 Jul 2014, 3:156 ( Open Peer Review v1 https://doi.org/10.12688/f1000research.4583.1) Latest published: 18 Dec 2014, 3:156 ( https://doi.org/10.12688/f1000research.4583.2) Reviewer Status Abstract Invited Reviewers The "developmental hourglass'' describes a pattern of increasing 1 2 3 morphological divergence towards earlier and later embryonic development, separated by a period of significant conservation across distant species (the "phylotypic stage''). Recent studies have found version 2 report report evidence in support of the hourglass effect at the genomic level. For published instance, the phylotypic stage expresses the oldest and most conserved 18 Dec 2014 transcriptomes. However, the regulatory mechanism that causes the hourglass pattern remains an open question. Here, we use an evolutionary version 1 model of regulatory gene interactions during development to identify the published report report report conditions under which the hourglass effect can emerge in a general 08 Jul 2014 setting. The model focuses on the hierarchical gene regulatory network that controls the developmental process, and on the evolution of a population Marcel Quint, Leibniz Institute of Plant under random perturbations in the structure of that network. The model 1 predicts, under fairly general assumptions, the emergence of an hourglass Biochemistry, Halle, Germany pattern in the structure of a temporal representation of the underlying gene Hajk-Georg Drost, Martin Luther University regulatory network. The evolutionary age of the corresponding genes also Halle–Wittenberg, Halle, Germany follows an hourglass pattern, with the oldest genes concentrated at the hourglass waist. The key behind the hourglass effect is that developmental 2 Dmitri Krioukov, Northeastern University, regulators should have an increasingly specific function as development Boston, MA, USA progresses. Analysis of developmental gene expression profiles from Drosophila melanogaster and Arabidopsis thaliana provide consistent 3 Gourab Ghoshal, Harvard University, results with our theoretical predictions. Cambridge, MA, USA Any reports and responses or comments on the article can be found at the end of the article. Page 1 of 36 F1000Research 2014, 3:156 Last updated: 16 MAY 2019 Corresponding authors: Constantine Dovrolis ([email protected]), Soojin Yi ([email protected]) Competing interests: No competing interests were disclosed. Grant information: This work was supported by the National Science Foundation (Grant No. 0831848 to C.D.). Any opinions, findings and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation (NSF). Copyright: © 2014 Akhshabi S et al. This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication). How to cite this article: Akhshabi S, Sarda S, Dovrolis C and Yi S. An explanatory evo-devo model for the developmental hourglass [version 1; peer review: 1 approved, 2 approved with reservations] F1000Research 2014, 3:156 ( https://doi.org/10.12688/f1000research.4583.1) First published: 08 Jul 2014, 3:156 (https://doi.org/10.12688/f1000research.4583.1) Page 2 of 36 F1000Research 2014, 3:156 Last updated: 16 MAY 2019 Introduction The model predicts that the evolutionary process shapes the DGENs The evolutionary mechanism of conservation during embryogen- of a population in the form of an hourglass, under fairly general esis, and its connection to the gene regulatory networks that control assumptions. Specifically, the number of genes at each developmen- development, are fundamental questions in systems biology1–3. Sev- tal stage follows an hour-glass pattern, with the smallest number at eral models have been presented in the context of morphological, the “waist” of the hourglass. The main condition for the appearance of molecular, and genetic developmental patterns. The most widely the hourglass pattern is that the DGEN should gradually get sparser as discussed model is the “developmental hourglass”, which places development progresses, with general-purpose regulatory genes at the strongest conservation across species in the “phylotypic stage”. the earlier developmental stages and highly specialized regulatory The first observations supporting the hourglass model go back to genes at the later stages. Another model prediction is that the evolu- von Baer when he noticed that there exists a mid-developmental tionary age of DGEN genes also follows an hourglass pattern, with stage in which embryos of different animals look similar4. On the the oldest genes concentrated at the waist. other hand, the “developmental funnel” model of conservation pre- dicts increasing diversification as development progresses5,6. We have examined the aforementioned predictions using transcrip- tome data from the development of Drosophila melanogaster and Recently, the hourglass model has come under new light. Multiple Arabidopsis thaliana. This data is insufficient to reconstruct the studies have observed the hourglass pattern across diverse biologi- complete DGEN of these species but it allows to estimate the num- cal processes, including transcriptome divergence7–11, transcrip- ber of genes at each developmental stage, given an activity variation tome age7,12,13, molecular interaction14, and evolutionary selective threshold. Under a wide range of this threshold, the inferred DGEN constraints10,14,15. Despite these observations the genomic basis and shape follows an hourglass pattern, the waist of that hourglass even the existence of the developmental hourglass effect have been roughly coincides with the previously reported phylotypic stage for the subject of an intense debate1,6,13,16–21. More importantly, the under- these species, and the age of the corresponding genes follows the lying mechanism that can shape the developmental process in the predicted hourglass pattern. hourglass or funnel forms is still unknown. Developmental gene execution networks We aim to understand the conditions under which the hourglass As a first-order approximation, a regulatory gene can be modeled effect can emerge in a general setting, based on an abstract model in one of several discrete functional states22. In the simplest case, a for the evolution of embryonic development. The model focuses regulatory gene can act as a binary switch (“on” and “off”) but in on a hierarchical network that represents the temporal “execution” general a gene may have more than two functional states. The tran- of the underlying Gene Regulatory Network (GRN) during devel- sition of a regulatory gene X from one functional state to another is opment. Each layer of the network corresponds to a developmen- often (but not always) caused by one or more upstream regulators tal stage. The nodes at each layer represent regulatory genes (i.e., of X that go through a functional state transition before X. We use genes encoding transcription factors or signaling molecules) that the term transitioning gene to refer to a regulatory gene that goes undergo significant activity change at that corresponding stage. The through a functional state transition at a given developmental time edges from genes at one layer to genes at the next layer represent anywhere at the developing embryo. regulatory interactions that cause those activity changes. We refer to this hierarchical network as Developmental Gene Execution A DGEN is a directed and acyclic network; see Figure 1a for an Network (DGEN) to distinguish it from the corresponding GRN. abstract example. The vertical direction refers to developmental A DGEN is subject to evolutionary perturbations (e.g., gene dele- time, from the zygote at the top to the developed organism at the tions, rewiring, duplication) that may be lethal, or that may impede bottom. In the horizontal direction we can represent different spa- development, for the corresponding organism. tial domains, even though this is not necessary and it is not done in a b Relative position 1 Increasing specificity A DL B RW 2 C RF 3 ... Developmental stage L DF Figure 1. An abstract DGEN. (A) The circles denote state-transitioning genes, edges represent directed regulatory interactions, and colored boxes refer to spatial domains that form during development. If regulatory genes become increasingly function-specific as development progresses, the network gradually becomes sparser in that direction. (B) Evolutionary perturbations on a DGEN’s structure: Gene A is deleted (DL), while gene B is rewired (RW) losing an outgoing edge. This RW event causes the regulatory failure (RF) of gene C, which then causes a cascade of five more RF events. This cascade causes
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