COLLOQUIUM INTRODUCTION INTRODUCTION COLLOQUIUM

Gene regulatory networks and network models in development and Neil Shubina,1

The passion, energy, and intellectual rigor that the late Eric Davidson brought to science transformed fields and the of many scientists working in them. Key among his many contributions was developing a testable framework and global approach to un- derstanding the mechanics of regulation and development. For several decades, Davidson and his colleagues developed the tools, concepts, and ap- proaches that led to a conceptual revolution in our understanding of the role of circuits of interacting , regulatory elements, and factors in the differentiation of cells, tissues, and organs in both development and evolution. Indeed, one of the things Davidson was working on before his untimely passing in September 2015, was organizing a Sackler Colloquium highlighting progress in the field of gene regulatory networks and the potential directions for future research. The conference that emerged, led by Douglas Erwin, Ellen Rothenberg, and myself, brought to- gether a broad array of leaders and their students to identify key results, critical challenges, and exciting opportunities in the rapidly changing field, captured by the title of the conference: Gene Regulatory Networks and Network Models in Development and Evolution. One thing that is clear from the papers that follow is that the impact of thinking on gene networks in bioscience is truly broad and deep. The topics span a wide range, from the differentiation of germ cells (1), immunology (2, 3), and the molecular basis of cell- type differentiation (4–11), to paleontology (12, 13) and behavior (14). The central role of network thinking Eric Davidson (1937–2015), to whom the Sackler is revealed in the way it allows for both the design of Colloquium on Gene Regulatory Networks and Network testable experimental frameworks to probe complex Models in Development and Evolution is dedicated. biological processes and the conceptual framework for understanding biological mechanisms. By reveal- papers, as well as those who participated in the meet- ing the broad impact of gene regulatory networks, ing, supplies a fitting tribute to the person whose en- and the explanatory power that a rigorous approach ergy initiated the conference and catalyzed discovery to them contains, the work of the authors of these in the field at large.

aDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637 This paper results from the Arthur M. Sackler Colloquium of the National Academy of Sciences, “Gene Regulatory Networks and Network Models in Development and Evolution,” held April 12–14, 2016, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, CA. The complete program and video recordings of most presentations are available on the NAS website at www.nasonline. org/Gene_Regulatory_Networks. Author contributions: N.S. wrote the paper. The author declares no conflict of interest. 1Email: [email protected].

5782–5783 | PNAS | June 6, 2017 | vol. 114 | no. 23 www.pnas.org/cgi/doi/10.1073/pnas.1610618114 Downloaded by guest on September 28, 2021 1 Whittle CA, Extavour CG (2017) Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans. Proc Natl Acad Sci USA 114:5784–5791. 2 Collombet S, et al. (2017) Logical modeling of lymphoid and myeloid cell specification and transdifferentiation. Proc Natl Acad Sci USA 114:5792–5799. 3 Longabaugh WJR, et al. (2017) Bcl11b and combinatorial resolution of cell fate in the T-cell gene regulatory network. Proc Natl Acad Sci USA 114:5800–5807. 4 Pyrowolakis G, Veikkolainen V, Yakoby N, Shvartsman SY (2017) Gene regulation during eggshell patterning. Proc Natl Acad Sci USA 114:5808–5813. 5 Kirmizitas A, Meiklejohn S, Ciau-Uitz A, Stephenson R, Patient R (2017) Dissecting BMP signaling input into the gene regulatory networks driving specification of the blood stem cell lineage. Proc Natl Acad Sci USA 114:5814–5821. 6 Hamey FK, et al. (2017) Reconstructing blood stem cell regulatory network models from single-cell molecular profiles. Proc Natl Acad Sci USA 114:5822–5829. 7 Buckingham M (2017) Gene regulatory networks and cell lineages that underlie the formation of skeletal muscle. Proc Natl Acad Sci USA 114:5830–5837. 8 De Kumar B, et al. (2017) Dynamic regulation of Nanog and stem cell-signaling pathways by Hoxa1 during early neuro-ectodermal differentiation of ES cells. Proc Natl Acad Sci USA 114:5838–5845. 9 Zhu J, Palliyil S, Ran C, Kumar JP (2017) Drosophila Pax6 promotes development of the entire eye-antennal disc, thereby ensuring proper adult head formation. Proc Natl Acad Sci USA 114:5846–5853. 10 Cary GA, Cheatle Jarvela AM, Francolini RD, Hinman VF (2017) Genome-wide use of high- and low-affinity Tbrain binding sites during echinoderm development. Proc Natl Acad Sci USA 114:5854–5861. 11 Peter IS, Davidson EH (2017) Assessing regulatory information in developmental gene regulatory networks. Proc Natl Acad Sci USA 114:5862–5869. 12 Thompson JR, et al. (2017) Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins. Proc Natl Acad Sci USA 114:5870–5877. 13 Vergara HM, et al. (2017) Whole-organism cellular gene-expression atlas reveals conserved cell types in the ventral nerve cord of Platynereis dumerilii. Proc Natl Acad Sci USA 114:5878–5885. 14 Baran NM, McGrath PT, Streelman JT (2017) Applying gene regulatory network logic to the evolution of social behavior. Proc Natl Acad Sci USA 114:5886–5893.

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