1. Developmental Biology
  2. Physics of Living Systems

Rolling controls sperm navigation in response to the dynamic rheological properties of the environment

  1. Meisam Zaferani
  2. Farhad Javi
  3. Amir Mokhtare
  4. Peilong Li
  5. Alireza Abbaspourrad  Is a corresponding author
  1. Cornell University, United States
https://doi.org/10.7554/eLife.68693
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  1. Meisam Zaferani
  2. Farhad Javi
  3. Amir Mokhtare
  4. Peilong Li
  5. Alireza Abbaspourrad
(2021)
Rolling controls sperm navigation in response to the dynamic rheological properties of the environment
eLife 10:e68693.
https://doi.org/10.7554/eLife.68693
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Abstract

Mammalian sperm rolling around their longitudinal axes is a long-observed component of motility, but its function in the fertilization process, and more specifically in sperm migration within the female reproductive tract, remains elusive. While investigating bovine sperm motion under simple shear flow and in a quiescent microfluidic reservoir and developing theoretical and computational models, we found that rolling regulates sperm navigation in response to the rheological properties of the sperm environment. In other words, rolling enables a sperm to swim progressively even if the flagellum beats asymmetrically. Therefore, a rolling sperm swims stably along the nearby walls (wall-dependent navigation) and efficiently upstream under an external fluid flow (rheotaxis). By contrast, an increase in ambient viscosity and viscoelasticity suppresses rolling, consequently, non-rolling sperm are less susceptible to nearby walls and external fluid flow and swim in two-dimensional diffusive circular paths (surface exploration). This surface exploration mode of swimming is caused by the intrinsic asymmetry in flagellar beating such that the curvature of a sperm’s circular path is proportional to the level of asymmetry. We found that the suppression of rolling is reversible and occurs in sperm with lower asymmetry in their beating pattern at higher ambient viscosity and viscoelasticity. Consequently, the rolling component of motility may function as a regulatory tool allowing sperm to navigate according to the rheological properties of the functional region within the female reproductive tract.

Data availability

All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. All data related to this paper are deposited in https://doi.org/10.5061/dryad.ngf1vhhtd

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Article and author information

Author details

  1. Meisam Zaferani

    Department of Food Science, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.

  2. Farhad Javi

    Food Science, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.

  3. Amir Mokhtare

    Department of Food Science, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Peilong Li

    Food Science, Cornell University, Ithaca, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Alireza Abbaspourrad

    Food Science, Cornell University, Ithaca, United States
    For correspondence
    alireza@cornell.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5617-9220

Funding

Cornell University

  • Alireza Abbaspourrad

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Raymond E Goldstein, University of Cambridge, United Kingdom

Version history

  1. Received: March 23, 2021
  2. Accepted: August 3, 2021
  3. Accepted Manuscript published: August 4, 2021 (version 1)
  4. Version of Record published: August 25, 2021 (version 2)

Copyright

© 2021, Zaferani et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Meisam Zaferani
  2. Farhad Javi
  3. Amir Mokhtare
  4. Peilong Li
  5. Alireza Abbaspourrad
(2021)
Rolling controls sperm navigation in response to the dynamic rheological properties of the environment
eLife 10:e68693.
https://doi.org/10.7554/eLife.68693

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