An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish

A shift in environmental conditions impacts the evolution of complex developmental and behavioral traits. The Mexican cavefish, Astyanax mexicanus, is a powerful model for examining the evolution of development, physiology, and behavior because multiple cavefish populations can be compared to an ext...

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Main Authors: Cody Loomis, Robert Peuß, James B. Jaggard, Yongfu Wang, Sean A. McKinney, Stephan C. Raftopoulos, Austin Raftopoulos, Daniel Whu, Matthew Green, Suzanne E. McGaugh, Nicolas Rohner, Alex C. Keene, Erik R. Duboue
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-10-01
Series:Frontiers in Neuroanatomy
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnana.2019.00088/full
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author Cody Loomis
Cody Loomis
Robert Peuß
James B. Jaggard
James B. Jaggard
Yongfu Wang
Sean A. McKinney
Stephan C. Raftopoulos
Austin Raftopoulos
Daniel Whu
Matthew Green
Suzanne E. McGaugh
Nicolas Rohner
Nicolas Rohner
Alex C. Keene
Alex C. Keene
Erik R. Duboue
Erik R. Duboue
author_facet Cody Loomis
Cody Loomis
Robert Peuß
James B. Jaggard
James B. Jaggard
Yongfu Wang
Sean A. McKinney
Stephan C. Raftopoulos
Austin Raftopoulos
Daniel Whu
Matthew Green
Suzanne E. McGaugh
Nicolas Rohner
Nicolas Rohner
Alex C. Keene
Alex C. Keene
Erik R. Duboue
Erik R. Duboue
author_sort Cody Loomis
collection DOAJ
description A shift in environmental conditions impacts the evolution of complex developmental and behavioral traits. The Mexican cavefish, Astyanax mexicanus, is a powerful model for examining the evolution of development, physiology, and behavior because multiple cavefish populations can be compared to an extant, ancestral-like surface population of the same species. Many behaviors have diverged in cave populations of A. mexicanus, and previous studies have shown that cavefish have a loss of sleep, reduced stress, an absence of social behaviors, and hyperphagia. Despite these findings, surprisingly little is known about the changes in neuroanatomy that underlie these behavioral phenotypes. Here, we use serial sectioning to generate brain atlases of surface fish and three independent cavefish populations. Volumetric reconstruction of serial-sectioned brains confirms convergent evolution on reduced optic tectum volume in all cavefish populations tested. In addition, we quantified volumes of specific neuroanatomical loci within several brain regions that have previously been implicated in behavioral regulation, including the hypothalamus, thalamus, and habenula. These analyses reveal an enlargement of the hypothalamus in all cavefish populations relative to surface fish, as well as subnuclei-specific differences within the thalamus and prethalamus. Taken together, these analyses support the notion that changes in environmental conditions are accompanied by neuroanatomical changes in brain structures associated with behavior. This atlas provides a resource for comparative neuroanatomy of additional brain regions and the opportunity to associate brain anatomy with evolved changes in behavior.
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spelling doaj.art-7c9da24f9dea4844a58e3078135330382022-12-21T17:34:01ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292019-10-011310.3389/fnana.2019.00088475270An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican CavefishCody Loomis0Cody Loomis1Robert Peuß2James B. Jaggard3James B. Jaggard4Yongfu Wang5Sean A. McKinney6Stephan C. Raftopoulos7Austin Raftopoulos8Daniel Whu9Matthew Green10Suzanne E. McGaugh11Nicolas Rohner12Nicolas Rohner13Alex C. Keene14Alex C. Keene15Erik R. Duboue16Erik R. Duboue17Department of Biology, Charles E. Schmidt College of Science, Florida Atlantic University, Jupiter, FL, United StatesJupiter Life Science Initiative, Florida Atlantic University, Jupiter, FL, United StatesStowers Institute for Medical Research, Kansas City, MO, United StatesDepartment of Biology, Charles E. Schmidt College of Science, Florida Atlantic University, Jupiter, FL, United StatesJupiter Life Science Initiative, Florida Atlantic University, Jupiter, FL, United StatesStowers Institute for Medical Research, Kansas City, MO, United StatesStowers Institute for Medical Research, Kansas City, MO, United StatesHarriet L. Wilkes Honors College, Florida Atlantic University, Jupiter, FL, United StatesHarriet L. Wilkes Honors College, Florida Atlantic University, Jupiter, FL, United StatesHarriet L. Wilkes Honors College, Florida Atlantic University, Jupiter, FL, United StatesJupiter Life Science Initiative, Florida Atlantic University, Jupiter, FL, United StatesDepartment of Ecology, University of Minnesota, St. Paul, MN, United StatesStowers Institute for Medical Research, Kansas City, MO, United StatesDepartment of Molecular and Integrative Physiology, KU Medical Center, Kansas City, KS, United StatesDepartment of Biology, Charles E. Schmidt College of Science, Florida Atlantic University, Jupiter, FL, United StatesJupiter Life Science Initiative, Florida Atlantic University, Jupiter, FL, United StatesJupiter Life Science Initiative, Florida Atlantic University, Jupiter, FL, United StatesHarriet L. Wilkes Honors College, Florida Atlantic University, Jupiter, FL, United StatesA shift in environmental conditions impacts the evolution of complex developmental and behavioral traits. The Mexican cavefish, Astyanax mexicanus, is a powerful model for examining the evolution of development, physiology, and behavior because multiple cavefish populations can be compared to an extant, ancestral-like surface population of the same species. Many behaviors have diverged in cave populations of A. mexicanus, and previous studies have shown that cavefish have a loss of sleep, reduced stress, an absence of social behaviors, and hyperphagia. Despite these findings, surprisingly little is known about the changes in neuroanatomy that underlie these behavioral phenotypes. Here, we use serial sectioning to generate brain atlases of surface fish and three independent cavefish populations. Volumetric reconstruction of serial-sectioned brains confirms convergent evolution on reduced optic tectum volume in all cavefish populations tested. In addition, we quantified volumes of specific neuroanatomical loci within several brain regions that have previously been implicated in behavioral regulation, including the hypothalamus, thalamus, and habenula. These analyses reveal an enlargement of the hypothalamus in all cavefish populations relative to surface fish, as well as subnuclei-specific differences within the thalamus and prethalamus. Taken together, these analyses support the notion that changes in environmental conditions are accompanied by neuroanatomical changes in brain structures associated with behavior. This atlas provides a resource for comparative neuroanatomy of additional brain regions and the opportunity to associate brain anatomy with evolved changes in behavior.https://www.frontiersin.org/article/10.3389/fnana.2019.00088/fullA. mexicanushypothalamusbrain evolutionbrain atlassleepstress
spellingShingle Cody Loomis
Cody Loomis
Robert Peuß
James B. Jaggard
James B. Jaggard
Yongfu Wang
Sean A. McKinney
Stephan C. Raftopoulos
Austin Raftopoulos
Daniel Whu
Matthew Green
Suzanne E. McGaugh
Nicolas Rohner
Nicolas Rohner
Alex C. Keene
Alex C. Keene
Erik R. Duboue
Erik R. Duboue
An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
Frontiers in Neuroanatomy
A. mexicanus
hypothalamus
brain evolution
brain atlas
sleep
stress
title An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
title_full An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
title_fullStr An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
title_full_unstemmed An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
title_short An Adult Brain Atlas Reveals Broad Neuroanatomical Changes in Independently Evolved Populations of Mexican Cavefish
title_sort adult brain atlas reveals broad neuroanatomical changes in independently evolved populations of mexican cavefish
topic A. mexicanus
hypothalamus
brain evolution
brain atlas
sleep
stress
url https://www.frontiersin.org/article/10.3389/fnana.2019.00088/full
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