PHD2023-22

PHD2023-22

Dynamics of hydraulic actuation of appendages in insects during metamorphosis

Host laboratory and collaborators

Joël Marthelot (IUSTI) / joel.marthelot@univ-amu.fr

Raphaël Clément (IBDM) / raphael.clement@univ-amu.fr

Yoël Forterre HDR (CNRS IUSTI) / yoel.forterre@univ-amu.fr

Abstract

While early wing morphogenesis in insects has been extensively studied [1], the process by which the wing expands during its transformation to its adult form is still poorly described. Such rapid organ-wide expansion is highly original in developmental biology. In a recent study, we characterized the kinematics of wings expansion in Drosophila melanogaster and proposed a mechanical model that well accounts for the planar expansion of the structure [2]. However, the dynamics of the deployement remains a completely open question. The coupling between the viscous flow and the elasticity of the structure limits actuation speed in soft structures [3]. The goal of the project is to develop a fundamental understanding of the fluid-structure interaction of appendage deployment in insects through a combination of theoretical analysis, numerical simulations and experiments on two models of insects: the wings of drosophila that unfold in a plane and the pronotal structures of Membracidae that exhibit complex and elaborate 3D morphologies mimicking structures in their environment to deceive predators [4].

Keywords

Morphogenesis, biomechanics, fluid-structure interaction

Objectives

The main objective of the proposed research is to build a fundamental understanding of the dynamics of rapid appendage expansion in insects during metamorphosis. The hypothesis is that hydraulic mechanisms limit the speed at which the structure can be expanded dictating the dynamic and timescale of structure deployment. This hypothesis will be tested by a series of experiments to measure hemoplymph flow in Drosophila wings and by macroscopic observations of the deployment of Membracidae pronotal structures.

Proposed approach (experimental / theoretical / computational)

In Drosophila melanogaster, we will characterize hemolymph flow in the wing during expansion with particle image velocimetry by injecting fluorescent microbeads into the Drosophila abdomen at the exit of the pupal phase. Hemolymph pressure in the fly will be measured simultaneously using microfluidic pressure probes developed at IUSTI to characterize plant cells. The expansion dynamics will be described theoretically using a fluid mechanics model based on viscous flows in poroelastic structures. This description will be validated and extended to the unfolding of structures that unfold in more complex three-dimensional geometries by observing the kinematics and characterizing the dynamics during the unfolding of pronotal structures in the Membracidae. This will provide a fundamental description of the processes limiting the hydaulic actuation of appendages in insects. In addition to providing a fundamental understanding of a spectacular example of rapid morphogenesis, the results will be relevant to the actuation and dynamics of soft structures with application in soft robotics.

Interdisciplinarity

The proposed research is interdisciplinary in nature, spanning organismic biology, mechanics, and materials science and will link traditionally disparate fields, providing the perspective of theoretical mechanics to the field of biology. The characterization of the hemolymph flow in the wing will be carried out at IBDM under the guidance of Raphaël Clément within the team Physical approach to cell dynamics and tissue morphogenesis. The measurement of hemolymph pressure using microfluidic probes will be carried out at IUSTI within the Biomechanics team under the guidance of Joël Marthelot and Yoël Forterre. The work on Drosophila will be complemented by the study of the expansion of pronotal structures in membracids, a non-model insect with unusual and dramatic features that have received very little attention in biological studies. Membracidae nymphs will be provided by collaborators in French Guiana.

Expected profile

Candidates with either Physics or Engineering backgrounds and research achievements in the
general area of biomechanics, soft/compliant mechanics or fluid mechanics are welcomed to
apply. The following areas of experimental expertise are particularly welcomed: biomechanics, rapid prototyping, micro-fabrication, material science and mechanical testing. A strong motivation to work at the interface between physics and biology is mandatory. In addition, an appreciation of theory, computation and scaling analysis is a plus.

Is this project the continuation of an existing project or an entirely new one? In the case of an existing project, please explain the links between the two projects

The project builds on the thesis of Simon Hadjaje who characterized the kinematics and developed a mechanical model of the Drosophila wing expansion. This mechanical description is a first fundamental step to describe the expansion dynamics which is still not understood and which is the objective of this project.

2 to 5 references related to the project

[1] MD Loza, and B Thompson “Forces shaping the Drosophila wing”. Mech. Dev. 144 (2017)
[2] S Hadjaje, I Andrade MJ Dalbe, R Clement, and J Marthelot “Wings deployment in Drosophila” (in prep).
[3] S Elbaz, and A Gat “Dynamics of viscous liquid within a closed elastic cylinder”. J Fluid Mech 758 (2014)
[4] A Haruhiko et al. Structure and development of complex helmet of treehoppers. Zoological Lett 6 (2020)

3 main publications from each PI over the last 5 years

Joël Marthelot

  • J Jones et al. “Bubble casting soft robotics” Nature 599, 229-233, 2021.
  • M Badaoui et al. “Capillary suction in templated Hele-Shaw cells” Adv Mater, 34:27, 2270200, 2022.
  • L Cai et al., “Instability mediated self-templating drop crystals” Science Advances, 8, eabq0828, 2022.

 

Raphaël Clement

  • S Genovese et al. “Coopted temporal patterning governs cellular hierarchy, heterogeneity and metabolism in Drosophila neuroblast tumors” Elife, 8, 2019.
  • B Dehapiot et al. “Assembly of a persistent apical actin network by the formin Frl/Fmnl tunes epithelial cell deformability” Nat Cell Biol 22, 7:791-802, 2020.
  • B Dehapiot et al. “RhoA-and Cdc42-induced antagonistic forces underlie symmetry breaking and spindle rotation in mouse oocytes” PLoS biology, 19(9), e3001376, 2021.

 

Yoël Forterre

  • A Bérut et al. “Gravisensors in plant cells behave like an active granular liquid” PNAS 115, 5123-5128, 2018.
  • N Levernier et al. “An integrative model of plant gravitropism linking statoliths position and auxin transport” Front Plant Sci 12 651928, 2021.
  • Y Forterre “Basic soft matter for plants”, in “Soft Matter in Plants: from Biophysics to biomimetics” eds. KH. Jensen, Y. Forterre, Royal Society of Chemistry, 2022.
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