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

Cody Loomis,Nicolas Rohner,Yongfu Wang,Daniel Whu,Erik R Duboue,Sean A Mckinney,Suzanne E Mcgaugh,Alex C Keene,Robert Peuß,Stephan C Raftopoulos,Matthew Green,Austin Raftopoulos,James B Jaggard

doi:10.3389/fnana.2019.00088

Abstract

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.

Highlights

Shifts in environmental conditions drive evolutionary changes in development, morphology, and behavior (Peichel et al, 2001; Shapiro et al, 2004; Jeffery, 2009)
We found the total volume of the hypothalamus was significantly enlarged in the cavefish populations compared to surface fish (Figures 5A–D and Supplementary Movies S5–S8; Pachón = 185.2% increase in volume compared to surface fish, Tinaja = 85% increase in volume compared to surface fish, Molino = 263% increase in volume compared to surface fish)
We found that the gross neuroanatomy of A. mexicanus and zebrafish were largely similar, allowing for identification major brain structures

Summary

Introduction

Shifts in environmental conditions drive evolutionary changes in development, morphology, and behavior (Peichel et al, 2001; Shapiro et al, 2004; Jeffery, 2009). The Mexican cavefish, Astyanax mexicanus, provides the unique opportunity to investigate the relationship between brain anatomy and behavioral evolution in a single species (Yoshizawa et al, 2010; Elipot et al, 2013; Alié et al, 2018; Jaggard et al, 2018; Lloyd et al, 2018) These fish exist as an eyed, pigmented population that inhabits the rivers and streams of northeast Mexico and southern Texas, and at least 29 independent populations of largely blind and depigmented fish that inhabit the caves of northeast Mexico’s Sierra de El Abra and Sierra de Guatemala regions (Mitchell et al, 1977). Comparisons between surface fish and cavefish populations reveal evolved differences in diverse behavioral traits ranging from social behavior to sleep, and the emergence of these behaviors in multiple cavefish populations has established A. mexicanus as a model for convergent evolution (Duboué et al, 2011; Elipot et al, 2013; Kowalko et al, 2013a,b; Chin et al, 2018)

Methods

Results

Conclusion