The evolution of developmental system drift in axial specification in Spiralia
Lead Research Organisation:
Queen Mary University of London
Department Name: Sch of Biological & Behavioural Sciences
Abstract
Similar organs in different animals often form slightly differently during development in the egg or the mother's womb. For example, humans and fishes have a spine on their backs, made of vertebrae with a nerve running through them. Yet, how cells behave and how the core units that comprise our genetic information--the genes--interact during the development of the spine in these animals are not entirely identical. This is paradoxical because the common expectation is that differences in how equivalent organs form should result in changes in how they look at birth. The phenomenon by which similar organs form through varying mechanisms is called 'developmental system drift', and researchers do not fully understand why and how it happens.
Animals as diverse as mussels, snails and earthworms look alike at the very first steps of their development. Indeed, we have shown that, in many cases, they use similar molecules and signals to define the blueprint of their adult morphology while they develop in their eggs. However, we have also found that different worms can use two distinct signals to define the organs that form along the body axis that goes from their backs to their bellies, the so-called dorsoventral axis. Our project wants to use this puzzling observation as a study system to investigate the process of 'developmental system drift' and, thereby, solve a fundamental and long-standing knowledge gap in Evolution and Developmental Biology.
In this project, we will investigate how changes in the formation of the back-to-belly axis in marine segmented worms originated. We will do this by applying advanced methodologies that allow recording the activity of genes at the level of individual cells. We will use these techniques in two worms that form the back-to-belly axis differently and perturb their development with chemical drugs to reconstruct how their genes interact during the critical phase of forming that body axis. By comparing the two species, we will identify similarities and differences at the level of single genes and single cells during their development, thereby inferring the changes in gene activity and regulation that cause 'developmental system drift' during the development of these species. Moreover, we will study the formation of the back-to-belly axis in a new species of worm to test the hypothesis that changes in the signals controlling this axis correlate with transitions to a mode of reproduction that relies on molecules that the mother deposits into the eggs.
Together, our project will establish new methods and species for the study of animal development and produce unparalleled datasets that will reveal the principles underpinning 'developmental system drift', a widespread and fundamental phenomenon in animals. We will thus generate new concepts, predictions and approaches that will likely apply to many other animals, providing a better understanding of the rules that govern the most critical phase of our lives.
Animals as diverse as mussels, snails and earthworms look alike at the very first steps of their development. Indeed, we have shown that, in many cases, they use similar molecules and signals to define the blueprint of their adult morphology while they develop in their eggs. However, we have also found that different worms can use two distinct signals to define the organs that form along the body axis that goes from their backs to their bellies, the so-called dorsoventral axis. Our project wants to use this puzzling observation as a study system to investigate the process of 'developmental system drift' and, thereby, solve a fundamental and long-standing knowledge gap in Evolution and Developmental Biology.
In this project, we will investigate how changes in the formation of the back-to-belly axis in marine segmented worms originated. We will do this by applying advanced methodologies that allow recording the activity of genes at the level of individual cells. We will use these techniques in two worms that form the back-to-belly axis differently and perturb their development with chemical drugs to reconstruct how their genes interact during the critical phase of forming that body axis. By comparing the two species, we will identify similarities and differences at the level of single genes and single cells during their development, thereby inferring the changes in gene activity and regulation that cause 'developmental system drift' during the development of these species. Moreover, we will study the formation of the back-to-belly axis in a new species of worm to test the hypothesis that changes in the signals controlling this axis correlate with transitions to a mode of reproduction that relies on molecules that the mother deposits into the eggs.
Together, our project will establish new methods and species for the study of animal development and produce unparalleled datasets that will reveal the principles underpinning 'developmental system drift', a widespread and fundamental phenomenon in animals. We will thus generate new concepts, predictions and approaches that will likely apply to many other animals, providing a better understanding of the rules that govern the most critical phase of our lives.
Technical Summary
Developmental system drift (DSD) is the phenomenon by which homologous phenotypes develop through divergent molecular mechanisms. Although DSD is widespread in animal embryos, how it arises is poorly understood. Our work in segmented worms (i.e., annelids) has shown a striking case of DSD affecting dorsoventral (DV) development in embryos with spiral cleavage, a highly conserved developmental mode ancestral to many marine invertebrates. While BMP is the ancestral pathway specifying the DV axis in annelids, certain species have independently transitioned to using Activin/Nodal. This project will use genome-scale, single-cell approaches to compare species that use BMP (Owenia fusiformis) with those that use Activin/Nodal (Capitella teleta) and, thereby, reveal the principles and consequences of DSD in animal development. We will test the hypothesis that the co-option of central nodes of a conserved DV gene regulatory network underpins DSD in axial patterning in annelids. To do so, we will (i) generate an unprecedented single-cell transcriptomic and regulatory atlas of annelid gastrulae to prove whether BMP and Activin/Nodal activate similar (or different) gene networks; (ii) determine the genetic programmes that control DV development, to reveal whether BMP and Activin/Nodal promote similar repertoires of homologous cell types during larval formation; and (iii) study the annelid Spirobranchus lamarcki to assess whether the axial role of BMP is generally conserved and test the link between DSD in axial patterning and transitions to autonomous development in spiral cleavage. Together, our project will use an excellent study system to advance our knowledge of the mechanisms that control animal embryogenesis and the crucial early steps of axial patterning, transforming our views of spiral cleavage and the forces that promote DSD in animal development.
