Developmental evolution of the forebrain in cavefish, from natural variations in neuropeptides to behavior.

Alexandre Alié,Lucie Devos,Sylvie Retaux,Yannick Elipot,Fanny Boulet,Maryline Blin,Jorge Torres-Paz,Lise Prunier

doi:10.7554/elife.32808

Abstract

The fish Astyanax mexicanus comes in two forms: the normal surface-dwelling and the blind depigmented cave-adapted morphs. Comparing the development of their basal forebrain, we found quantitative differences in numbers of cells in specific clusters for six out of nine studied neuropeptidergic cell types. Investigating the origins of these differences, we showed that early Shh and Fgf signaling impact on the development of NPY and Hypocretin clusters, via effect on Lhx7 and Lhx9 transcription factors, respectively. Finally, we demonstrated that such neurodevelopmental evolution underlies behavioral evolution, linking a higher number of Hypocretin cells with hyperactivity in cavefish. Early embryonic modifications in signaling/patterning at neural plate stage therefore impact neuronal development and later larval behavior, bridging developmental evolution of a neuronal system and the adaptive behavior it governs. This work uncovers novel variations underlying the evolution and adaptation of cavefish to their extreme environment.

Highlights

The secondary prosencephalon of the vertebrate forebrain, comprising the telencephalon, the optic/ preoptic region and the hypothalamus, develops from the anterior neural plate
A morphogenetic interpretation of the development of the optic/pre-optic region suggests the existence of three morphogenetic units based on centrifugal neurogenesis patterns rather than on gene expression boundaries –the telencephalon, the optic recess region (ORR) and the hypothalamus, which helps to resolve some inconsistencies between tetrapod and teleost basal forebrain (Affaticati et al, 2015)(Figure 1—figure supplement 1B)
A homology relationship was proposed between the teleost ‘neurosecretory pre-optic area’ or NPO and the mammalian paraventricular nucleus (PVN), which belongs to the mammalian alar hypothalamus (Herget et al, 2014; Herget and Ryu, 2015)(Figure 1—figure supplement 1C)

Summary

Introduction

The secondary prosencephalon of the vertebrate forebrain, comprising the telencephalon, the optic/ preoptic region and the hypothalamus, develops from the anterior neural plate. By the end of gastrulation, the neural plate is already patterned and the regional fate of its antero-posterior and medio-lateral domains is specified, as a result of the concerted action of diffusible morphogen molecules that emanate from secondary organizers (reviewed in [Cavodeassi and Houart, 2012]). The elaboration of the vertebrate forebrain depends on the tight spatial and temporal regulation of relatively few morphogenetic signals. Changes in these early events have the potential to modulate brain organization, notably the relative size of different brain regions (Hinaux et al, 2016; Sylvester et al, 2010; Sylvester et al, 2013) (reviewed in [Retaux et al, 2013])

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Results

Conclusion