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

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.

SUBMITTER: Alie A

PROVIDER: S-EPMC5800845 | biostudies-literature | 2018 Feb

REPOSITORIES: biostudies-literature

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

Alié Alexandre A Devos Lucie L Torres-Paz Jorge J Prunier Lise L Boulet Fanny F Blin Maryline M Elipot Yannick Y Retaux Sylvie S

eLife 20180206

The fish <i>Astyanax mexicanus</i> 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 transcrip ...[more]

PMID: 29405116

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Project description:BackgroundHow and why animals lose eyesight during adaptation to the dark and food-limited cave environment has puzzled biologists since the time of Darwin. More recently, several different adaptive hypotheses have been proposed to explain eye degeneration based on studies in the teleost Astyanax mexicanus, which consists of blind cave-dwelling (cavefish) and sighted surface-dwelling (surface fish) forms. One of these hypotheses is that eye regression is the result of indirect selection for constructive characters that are negatively linked to eye development through the pleiotropic effects of Sonic Hedgehog (SHH) signaling. However, subsequent genetic analyses suggested that other mechanisms also contribute to eye regression in Astyanax cavefish. Here, we introduce a new approach to this problem by investigating the phenotypic and genetic relationships between a suite of non-visual constructive traits and eye regression.ResultsUsing quantitative genetic analysis of crosses between surface fish, the Pachón cavefish population and their hybrid progeny, we show that the adaptive vibration attraction behavior (VAB) and its sensory receptors, superficial neuromasts (SN) specifically found within the cavefish eye orbit (EO), are genetically correlated with reduced eye size. The quantitative trait loci (QTL) for these three traits form two clusters of congruent or overlapping QTL on Astyanax linkage groups (LG) 2 and 17, but not at the shh locus on LG 13. Ablation of EO SN in cavefish demonstrated a major role for these sensory receptors in VAB expression. Furthermore, experimental induction of eye regression in surface fish via shh overexpression showed that the absence of eyes was insufficient to promote the appearance of VAB or EO SN.ConclusionsWe conclude that natural selection for the enhancement of VAB and EO SN indirectly promotes eye regression in the Pachón cavefish population through an antagonistic relationship involving genetic linkage or pleiotropy among the genetic factors underlying these traits. This study demonstrates a trade-off between the evolution of a non-visual sensory system and eye regression during the adaptive evolution of Astyanax to the cave environment.

Dataset Information

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

Publications

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

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