Evolutionary convergence of a neural mechanism in the cavefish lateral line system

  1. Elias T Lunsford
  2. Alexandra Paz
  3. Alex C Keene
  4. James C Liao  Is a corresponding author
  1. University of Florida, United States
  2. Florida Atlantic University, United States
  3. Texas A&M University, United States

Abstract

Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish.. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently-derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.

Data availability

Electrophysiology data generated and analysed during this study are included as a supplementary file ('Supplementary File 1').

Article and author information

Author details

  1. Elias T Lunsford

    Department of Biology, University of Florida, Saint Augustine, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3713-6994
  2. Alexandra Paz

    Department of Biological Sciences, Florida Atlantic University, Jupiter, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alex C Keene

    Texas A&M University, College Station, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. James C Liao

    Department of Biology, University of Florida, Saint Augustine, United States
    For correspondence
    jliao@whitney.ufl.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0181-6995

Funding

US-Israel Binational Science Foundation (SP#2018-190)

  • Alex C Keene

National Science Foundation (IOS165674)

  • Alex C Keene

National Institutes of Health (IR01GM127872)

  • Alex C Keene

National Institutes of Health (DC010809)

  • James C Liao

National Science Foundation (IOS1856237)

  • James C Liao

National Science Foundation (IOS2102891)

  • James C Liao

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

Ethics

Animal experimentation: All animals were handled according to protocols approved by the University of Florida or Florida Atlantic University Institutional Animal Care and Use Committee (IACUC201603267, IACUC202200000056). Animal health was assessed by monitoring blood flow throughout each experiment.

Reviewing Editor

  1. Matthieu Louis, University of California, Santa Barbara, United States

Publication history

  1. Received: January 27, 2022
  2. Accepted: June 15, 2022
  3. Accepted Manuscript published: June 16, 2022 (version 1)

Copyright

© 2022, Lunsford 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. Elias T Lunsford
  2. Alexandra Paz
  3. Alex C Keene
  4. James C Liao
(2022)
Evolutionary convergence of a neural mechanism in the cavefish lateral line system
eLife 11:e77387.
https://doi.org/10.7554/eLife.77387

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