Systematic comparison of sea urchin and sea star developmental gene regulatory networks explains how novelty is incorporated in early development

Gregory A Cary,Olga Zueva,Brenna S Mccauley,Joseph Pattinato,William Longabaugh,Veronica F Hinman

doi:10.1038/s41467-020-20023-4

Abstract

The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. Morphology is the output of development, therefore phenotypic evolution arises from changes to the topology of the gene regulatory networks (GRNs) that control the highly coordinated process of embryogenesis. A particular challenge in understanding the origins of animal diversity lies in determining how GRNs incorporate novelty while preserving the overall stability of the network, and hence, embryonic viability. Here we assemble a comprehensive GRN for endomesoderm specification in the sea star from zygote through gastrulation that corresponds to the GRN for sea urchin development of equivalent territories and stages. Comparison of the GRNs identifies how novelty is incorporated in early development. We show how the GRN is resilient to the introduction of a transcription factor, pmar1, the inclusion of which leads to a switch between two stable modes of Delta-Notch signaling. Signaling pathways can function in multiple modes and we propose that GRN changes that lead to switches between modes may be a common evolutionary mechanism for changes in embryogenesis. Our data additionally proposes a model in which evolutionarily conserved network motifs, or kernels, may function throughout development to stabilize these signaling transitions.

Highlights

The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution
It initiates with early asymmetries that activate highly coordinated cascades of gene regulatory interactions known as a gene regulatory network (GRN)
We demonstrate that the change in upstream regulation between sea urchin and sea stars that results in co-expression of delta and hesC at blastula stage allows for lateral inhibition (LI) regulatory interactions in sea stars, compared to the inductive mechanism used in sea urchins (Fig. 2h)

Summary

Introduction

The extensive array of morphological diversity among animal taxa represents the product of millions of years of evolution. The GRN for the specification of sea urchin endomesoderm is the most comprehensive, experimentally derived GRN known to date[9,10,11] It explains how vegetal-most micromeres express signaling molecules, including Delta, needed to specify the adjacent macromere cells to endomesoderm, how micromeres ingress as mesenchyme, and are specified to form a biomineralized skeleton. Temporal model, including primary and published data, is hosted on a web server (grns.biotapestry.org/ PmEndomes), which allows for further and more fine-grained exploration (Supplementary Fig. 2) This GRN was produced using the same experimental approaches as those used to generate the sea urchin network[20] to allow for a meaningful comparison. We show how bimodal switches in signaling pathways permit an evolutionary transition in regulatory network topology, and how such a transition is buffered by the presence of conserved regulatory kernels

Methods

Results

Conclusion