Evolution of neuronal cell types, development and circuitry in the insect visual system: breaking down behavioural evolution into its constituent elements

Informations projet

BehaEvoDevo

N° de convention de subvention: 949500

DOI

10.3030/949500

Date de signature de la CE 30 Octobre 2020

Date de début 1 Septembre 2021

Date de fin 31 Août 2026

Financé au titre de

• EXCELLENT SCIENCE - European Research Council (ERC)

Coût total

€ 1 632 647,00

Contribution de l’UE

€ 1 632 647,00

Coordonné par

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE CNRS
France

Periodic Reporting for period 3 - BehaEvoDevo (Evolution of neuronal cell types, development and circuitry in the insect visual system: breaking down behavioural evolution into its constituent elements)

Période du rapport: 2024-09-01 au 2026-02-28

Résumé du contexte et des objectifs généraux du projet

Animals live in different environments and they have to adapt their behaviors to their specific needs. A large part of neuroscience research aims to understand how the brain works to output complex behaviors. However, the brain is not an engineering feat, rather it is the product of millions of years of animal evolution. To fully comprehend how the brain works, we need to understand how it develops and how these developmental mechanisms have evolved during animal evolution. This is the goal of BehaEvoDevo, i.e. to understand how neuronal circuits and behaviors evolve from a cell-type specific perspective, using the intricate visual system of insects as a prime model for exploration.

Among insects, the fruit fly Drosophila stands as a well-documented exemplar, offering a rich literature regarding neuronal cell type composition, developmental processes, neural circuitry, and resultant behaviors. Leveraging our expertise in this system, we aim to address three overarching questions: a) How does the composition of brain cells vary across different species of animals? By scrutinizing the cellular landscape of diverse insect species, we can discern patterns of divergence and convergence, shedding light on the evolutionary trajectory of neural architecture. b) How do the mechanisms orchestrating neuronal development evolve, and what impact do they have on the diversity of neurons? Through comparative analyses, we seek to uncover the evolutionary dynamics shaping the emergence and differentiation of neuronal populations, thereby illuminating the roots of neural diversity. c) How do neuronal circuits evolve and how does this affect behaviors? By dissecting the neural circuits governing behaviors in various insects, we aim to unravel the intricacies of evolutionary divergence in behavioral control mechanisms.

Travail effectué depuis le début du projet jusqu’à la fin de la période considérée dans le rapport et principaux résultats atteints jusqu’à présent

To address these questions, we are using state-of-the-art methodologies, including single-cell sequencing and advanced genetic tools tailored for Drosophila, while also innovating techniques for genetic manipulation and circuit analysis in non-model insects. By juxtaposing cell composition, neuronal development, and circuit architecture across phylogenetically diverse insects, we aim to uncover the fundamental principles driving the evolution of behavioral diversity. Furthermore, we aim to establish a comprehensive framework for understanding how developmental processes shape behaviors and provide a roadmap for cross-species comparisons within the insect kingdom and beyond.

Along these lines, we have generated single-cell sequencing data from different insects that differ in the environments that they inhabit and, hence, in their behaviors. These data allow us to discover the neuronal cell types that occupy these insect brains. We are using state-of-the-art bioinformatic tools to compare cell type composition, as well as the their developmental mechanisms. We have, so far, established the appropriate pipelines for the anaysis of such data and have discovered potentially new cell types, as well as differences in the underlying neurodevelopmental mechanisms that we are currently confirming by immunostaining.

Finally, by studying a specific neurodevelopmental mechanism, called temporal patterning, we proposed a model whereby temporal patterning predated spatial patterning. We proposed that temporal patterning was potentially already present in single-celled organisms, which can pattern themselves in time (but not in space). As more complex organisms evolved, these temporal sequences could have been used to pattern the more complex tissues in space.

Progrès au-delà de l’état des connaissances et impact potentiel prévu (y compris l’impact socio-économique et les conséquences sociétales plus larges du projet jusqu’à présent)

This project relies on the unique advantage of the system we are studying, the visual system of insects. One of the main insect model organisms, Drosophila melanogaster, has been studied extensively and we currently have a full catalog of neuronal cell types, an extremely detailed description of the developmental mechanisms that generate these cell types, a full map of the connectivity between these neuronal cell types, and, finally, a fair description of the role of these cell types in different behaviors. The above allow us to perform a comprehensive comparison of visual system composition, development, and circuitry in species that span the entire phylogenetic tree of insects and come up with complete models of how circuits and behaviors evolve.

In the second half of this project, we will complete the comparison of the different insect visual systems at the level of neuronal type composition and neuronal development to understand how new neuronal types evolve. At the same time, we plan to progress in mapping the new neiuronal cell types and their circuitry in the brain and link it with different visually-guided behaviors.