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Metachronal waves in the flagellar beating of Volvox and their hydrodynamic origin.


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Authors

Brumley, Douglas R 
Polin, Marco 
Pedley, Timothy J 
Goldstein, Raymond E  ORCID logo  https://orcid.org/0000-0003-2645-0598

Abstract

Groups of eukaryotic cilia and flagella are capable of coordinating their beating over large scales, routinely exhibiting collective dynamics in the form of metachronal waves. The origin of this behavior--possibly influenced by both mechanical interactions and direct biological regulation--is poorly understood, in large part due to a lack of quantitative experimental studies. Here we characterize in detail flagellar coordination on the surface of the multicellular alga Volvox carteri, an emerging model organism for flagellar dynamics. Our studies reveal for the first time that the average metachronal coordination observed is punctuated by periodic phase defects during which synchrony is partial and limited to specific groups of cells. A minimal model of hydrodynamically coupled oscillators can reproduce semi-quantitatively the characteristics of the average metachronal dynamics, and the emergence of defects. We systematically study the model's behaviour by assessing the effect of changing intrinsic rotor characteristics, including oscillator stiffness and the nature of their internal driving force, as well as their geometric properties and spatial arrangement. Our results suggest that metachronal coordination follows from deformations in the oscillators' limit cycles induced by hydrodynamic stresses, and that defects result from sufficiently steep local biases in the oscillators' intrinsic frequencies. Additionally, we find that random variations in the intrinsic rotor frequencies increase the robustness of the average properties of the emergent metachronal waves.

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Keywords

eukaryotic flagella, metachronal waves, microhydrodynamics, synchronization, Flagella, Hydrodynamics, Models, Biological, Volvox

Journal Title

J R Soc Interface

Conference Name

Journal ISSN

1742-5689
1742-5662

Volume Title

12

Publisher

The Royal Society
Sponsorship
European Research Council (247333)
Wellcome Trust (097855/Z/11/Z)
This work was supported in part by the EPSRC (M.P.), ERC Advanced Investigator grant 247333 and a Senior Investigator Award from the Wellcome Trust.