Nonlinear instability in flagellar dynamics: A novel modulation mechanism in sperm migration?

Hermes Gadelha; E. A. Gaffney; D. J. Smith; J. C. Kirkman-Brown

doi:10.1098/rsif.2010.0136

Nonlinear instability in flagellar dynamics: A novel modulation mechanism in sperm migration?

Hermes Gadelha^*, E. A. Gaffney, D. J. Smith, J. C. Kirkman-Brown

^*Corresponding author for this work

Mathematics

Research output: Contribution to journal › Article › peer-review

Abstract

Throughout biology, cells and organisms use flagella and cilia to propel fluid and achieve motility. The beating of these organelles, and the corresponding ability to sense, respond to and modulate this beat is central to many processes in health and disease. While the mechanics of flagellum-fluid interaction has been the subject of extensive mathematical studies, these models have been restricted to being geometrically linear or weakly nonlinear, despite the high curvatures observed physiologically. We study the effect of geometrical nonlinearity, focusing on the spermatozoon flagellum. For a wide range of physiologically relevant parameters, the nonlinear model predicts that flagellar compression by the internal forces initiates an effective buckling behaviour, leading to a symmetry-breaking bifurcation that causes profound and complicated changes in the waveform and swimming trajectory, as well as the breakdown of the linear theory. The emergent waveform also induces curved swimming in an otherwise symmetric system, with the swimming trajectory being sensitive to head shape - no signalling or asymmetric forces are required. We conclude that nonlinear models are essential in understanding the flagellar waveform in migratory human sperm; these models will also be invaluable in understanding motile flagella and cilia in other systems.

Original language	English
Pages (from-to)	1689-1697
Number of pages	9
Journal	Interface
Volume	7
Issue number	53
DOIs	https://doi.org/10.1098/rsif.2010.0136
Publication status	Published - 6 Dec 2010

Keywords

Asymmetric waveforms
Buckling instability
Internally driven filaments
Nonlinear flagellar dynamics
Sperm motility
Symmetry breaking

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10.1098/rsif.2010.0136

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title = "Nonlinear instability in flagellar dynamics: A novel modulation mechanism in sperm migration?",

abstract = "Throughout biology, cells and organisms use flagella and cilia to propel fluid and achieve motility. The beating of these organelles, and the corresponding ability to sense, respond to and modulate this beat is central to many processes in health and disease. While the mechanics of flagellum-fluid interaction has been the subject of extensive mathematical studies, these models have been restricted to being geometrically linear or weakly nonlinear, despite the high curvatures observed physiologically. We study the effect of geometrical nonlinearity, focusing on the spermatozoon flagellum. For a wide range of physiologically relevant parameters, the nonlinear model predicts that flagellar compression by the internal forces initiates an effective buckling behaviour, leading to a symmetry-breaking bifurcation that causes profound and complicated changes in the waveform and swimming trajectory, as well as the breakdown of the linear theory. The emergent waveform also induces curved swimming in an otherwise symmetric system, with the swimming trajectory being sensitive to head shape - no signalling or asymmetric forces are required. We conclude that nonlinear models are essential in understanding the flagellar waveform in migratory human sperm; these models will also be invaluable in understanding motile flagella and cilia in other systems.",

keywords = "Asymmetric waveforms, Buckling instability, Internally driven filaments, Nonlinear flagellar dynamics, Sperm motility, Symmetry breaking",

author = "Hermes Gadelha and Gaffney, {E. A.} and Smith, {D. J.} and Kirkman-Brown, {J. C.}",

year = "2010",

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PY - 2010/12/6

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N2 - Throughout biology, cells and organisms use flagella and cilia to propel fluid and achieve motility. The beating of these organelles, and the corresponding ability to sense, respond to and modulate this beat is central to many processes in health and disease. While the mechanics of flagellum-fluid interaction has been the subject of extensive mathematical studies, these models have been restricted to being geometrically linear or weakly nonlinear, despite the high curvatures observed physiologically. We study the effect of geometrical nonlinearity, focusing on the spermatozoon flagellum. For a wide range of physiologically relevant parameters, the nonlinear model predicts that flagellar compression by the internal forces initiates an effective buckling behaviour, leading to a symmetry-breaking bifurcation that causes profound and complicated changes in the waveform and swimming trajectory, as well as the breakdown of the linear theory. The emergent waveform also induces curved swimming in an otherwise symmetric system, with the swimming trajectory being sensitive to head shape - no signalling or asymmetric forces are required. We conclude that nonlinear models are essential in understanding the flagellar waveform in migratory human sperm; these models will also be invaluable in understanding motile flagella and cilia in other systems.

AB - Throughout biology, cells and organisms use flagella and cilia to propel fluid and achieve motility. The beating of these organelles, and the corresponding ability to sense, respond to and modulate this beat is central to many processes in health and disease. While the mechanics of flagellum-fluid interaction has been the subject of extensive mathematical studies, these models have been restricted to being geometrically linear or weakly nonlinear, despite the high curvatures observed physiologically. We study the effect of geometrical nonlinearity, focusing on the spermatozoon flagellum. For a wide range of physiologically relevant parameters, the nonlinear model predicts that flagellar compression by the internal forces initiates an effective buckling behaviour, leading to a symmetry-breaking bifurcation that causes profound and complicated changes in the waveform and swimming trajectory, as well as the breakdown of the linear theory. The emergent waveform also induces curved swimming in an otherwise symmetric system, with the swimming trajectory being sensitive to head shape - no signalling or asymmetric forces are required. We conclude that nonlinear models are essential in understanding the flagellar waveform in migratory human sperm; these models will also be invaluable in understanding motile flagella and cilia in other systems.

KW - Asymmetric waveforms

KW - Buckling instability

KW - Internally driven filaments

KW - Nonlinear flagellar dynamics

KW - Sperm motility

KW - Symmetry breaking

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Nonlinear instability in flagellar dynamics: A novel modulation mechanism in sperm migration?

Abstract

Keywords

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