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How Mexican cavefish evolved in extreme environments

Credits : Sylvie Rétaux, Hélène Hinaux, Yannick Elipot

New insight into the development and function of Mexican cavefish brains reveals how the animals adapted their behaviour to cope with extreme environments.
In a study published in eLife, researchers from the Paris-Saclay Institute of Neuroscience, demonstrate how the developmental evolution of the brain in cave-dwelling Astyanax mexicanus (A. mexicanus) underlies the evolution of its survival behaviours. A second study from the US, published at the same time in eLife, suggests higher levels of hypocretin (HCRT) in the cavefish brain – a chemical compound associated with human narcolepsy – accounts for the loss of sleep in these animals.

There are two forms of A. mexicanus : surface-dwelling fish that inhabit rivers in south and central America, and fish that live in the total and permanent darkness of Mexican caves. The cavefish display striking differences from their river-dwelling counterparts, including the loss of sleep that makes them a potential model to study human sleep disorders such as insomnia.

“We have previously found that sleep is increased in the cave-dwelling fish during periods of prolonged starvation,” says James Jaggard, graduate researcher at Florida Atlantic University (FAU) and lead author of the US study. “This raised the possibility that they suppress sleep to forage during the wet season when food is plentiful, and increase sleep to save energy during the dry season when it is less abundant.”

“A. mexicanus cave-dwellers have developed this and other beneficial behaviours that allow them to live in adverse environments,” adds senior author Sylvie Retaux, Group Leader at CNRS, Paris-Saclay Institute of Neuroscience. “This makes them a prime model to study the evolution of brain development and its behavioural consequences, providing greater understanding of how vertebrates colonise more unusual locations.”

In their study, Retaux and her team compared the development and natural variations of anatomy in the brains of both surface and cave-dwelling A. mexicanus embryos and larvae, highlighting specific differences in the numbers of neurons between the two forms. “We discovered a higher number of HCRT cells in the brains of cave-dwelling fish compared to surface-dwellers,” explains first author and postdoctoral researcher Alexandre Alié, from CNRS. “By manipulating the numbers of HCRT neurons, we were able to link these to increased activity levels in the animals.”

Co-author Jorge Torres-Paz, also a postdoctoral researcher at CNRS, adds : “Interestingly, we found that the variation in HCRT neuron numbers stems from very early embryonic events, which occur as early as within the first 10 hours after fertilisation. This suggests the mechanisms that lead to the loss of eyes could be shared in part with those that control developmental evolution of brain and behaviour, including sleep.”

In the second study, senior author and FAU Associate Professor Alex Keene and his team set out to discover the mechanics behind sleep loss in A. mexicanus. “Deficiencies in HCRT signalling are associated with altered sleep and narcolepsy in diverse vertebrate organisms,” he explains. “We were interested to find out more about its role in A. mexicanus cave-dwellers.”

Again, Keene and his team conducted a comparative study among A. mexicanus surface and cavefish brain cells. Their results support Alié, Devos, Torres-Paz et al.’s findings that the number of HCRT cells in cavefish is significantly higher than that of their surface-dwelling counterparts.
Next, they showed that inhibiting HCRT signalling, genetically or pharmacologically, increased sleep in cavefish, while it had very little effect on surface fish. This provides the first genetic insight into the evolution of sleep loss in cave-dwellers.

“Altogether, our results reflect the first study’s findings that developmental evolution of the cavefish brain drives evolution in the animals’ behaviour,” Jaggard concludes. “More generally, they also support a role for HCRT in relation to sleep in other animals, providing a new system for investigating sleep differences throughout the entire animal kingdom.”

 

References :

- Developmental evolution of the forebrain in cavefish, from natural variations in neuropeptides to behavior, Alexandre Alié, Lucie Devos, Jorge Torres-Paz, Lise Prunier, Fanny Boulet, Maryline Blin, Yannick Elipot et
Sylvie Rétaux
, eLife, 6 février 2018. doi.org/10.7554/eLife.32808

- Hypocretin underlies the evolution of sleep loss in the Mexican cavefish, James B Jaggard Bethany A Stahl Evan Lloyd David A Prober Erik R Duboue Alex C Keene, eLife, 6 février 2018. doi.org/10.7554/eLife.32637

Contacts :

- Emily Packer, Senior Press Officer, eLife, e.packer[At]elifesciences.org
01223 855373

- Sylvie Rétaux, T 33 (0)1 69 82 34 52, retaux[At]inaf.cnrs-gif.fr


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