Cavefish brain atlases reveal functional and anatomical convergence across independently evolved populations

James B. Jaggard, Evan Lloyd, Anders Yuiska, Adam Patch, Yaouen Fily, Johanna E. Kowalko, Lior Appelbaum, Erik R. Duboue, Alex C. Keene

Research output: Contribution to journalArticlepeer-review

33 Scopus citations

Abstract

Environmental perturbation can drive behavioral evolution and associated changes in brain structure and function. The Mexican fish species, Astyanax mexicanus, includes eyed river-dwelling surface populations and multiple independently evolved populations of blind cavefish. We used whole-brain imaging and neuronal mapping of 684 larval fish to generate neuroanatomical atlases of surface fish and three different cave populations. Analyses of brain region volume and neural circuits associated with cavefish behavior identified evolutionary convergence in hindbrain and hypothalamic expansion, and changes in neurotransmitter systems, including increased numbers of catecholamine and hypocretin/orexin neurons. To define evolutionary changes in brain function, we performed whole-brain activity mapping associated with behavior. Hunting behavior evoked activity in sensory processing centers, while sleep-associated activity differed in the rostral zone of the hypothalamus and tegmentum. These atlases represent a comparative brain-wide study of intraspecies variation in vertebrates and provide a resource for studying the neural basis of behavioral evolution.

Original languageEnglish
Article numbereaba3126
JournalScience advances
Volume6
Issue number38
DOIs
StatePublished - Sep 2020

Bibliographical note

Publisher Copyright:
Copyright © 2020 The Authors, some rights reserved.

Funding

We are grateful for support from J. Boerner (FAU) for image analysis and H. Burgess (NIH) for the helpful discussion. In addition, A. Loppato and P. Lewis (FAU) provided critical animal care support. Funding: This work was supported by NIH grants R21NS105071 (to A.C.K. and E.R.D.) and R01GM127872 (to A.C.K.), NSF awards DEB 174231 (to A.C.K. and J.E.K.), IOS 165674 (to A.C.K.), and IOS 1923372 (to A.C.K. and J.E.K.), and BSF award SP#2018-190 (to A.C.K. and L.A.). Author contributions: Conceptualization: J.B.J., J.E.K., L.A., E.R.D., E.L., and A.C.K. Data acquisition and analysis: J.B.J., E.L., A.Y., A.P., and Y.F. All authors contributed to the writing of the manuscript. Competing interests: The authors declare that they have no competing interests. Data and materials availability: All data needed to evaluate the conclusions in the paper are present in the paper and/or the Supplementary Materials. Additional data related to this paper may be requested from the authors.

FundersFunder number
National Science FoundationIOS 165674, DEB 174231, IOS 1923372
National Institutes of HealthR21NS105071, R01GM127872
National Heart, Lung, and Blood InstituteT32HL110952
Bonfils-Stanton Foundation2018-190
Florida Atlantic University

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