From cell shape to organism shape: the cellular basis for the evolutionary origin of animal morphogenesis

Introduction

My work concerns a critical question: How did the cellular mechanisms underpinning animal morphogenesis first evolve? While the first multicellular ancestors of modern animals have left limited fossil traces, insights can be gained by studying their closest living relatives: the choanoflagellates.

Background

This group of microeukaryotes has several features of high relevance to animal origins, including:

• Temporal cell differentiation
• Facultative multicellularity
• A metazoan-like "developmental gene toolkit"

Importantly, they have become amenable to functional genetics in the past few years.

Research Focus

We will study the molecular and cellular mechanisms of three morphogenetic processes in choanoflagellates:

1. The formation of the "collar complex," a ring of microvilli surrounding the flagellum, which represents an example of complex single-cell morphogenesis and has been central to hypotheses about animal origins.
2. The molecular control of the differentiation of choanoflagellates into amoeboid cells under confinement, which I recently discovered and whose mechanisms remain unknown.
3. The cellular basis of adhesion and inversion in sheet colonies of the multicellular species Choanoeca flexa, which I recently co-discovered.

Methodology

These three processes will be characterized by multiomic approaches, which will allow unbiased comparisons with the growing dataset of molecular atlases for animal cell types.

We will perform:

• Knockout
• Chemical inhibition
• Fluorescent tagging of candidate genes identified by omics and/or known to play important roles in animals, including structural genes (such as those encoding cytoskeletal and adhesion proteins) and components of signaling pathways.

Analysis

Results will be analyzed in a rigorous phylogenetic framework. This project has the potential to answer long-standing questions on the pre-metazoan function of developmental genes and to inform the mechanistic basis of the transition from cell shape to organism shape in both development and evolution.