Evolutionary increases in catecholamine signaling may underlie the emergence of adaptive traits and behaviors in the blind cavefish, Astyanax mexicanus

Abstract

Evolutionary changes in catecholamine neurotransmitters such as dopamine and noradrenaline can lead to habitat specific behaviors. We used tyrosine hydroxylase, a conserved precursor to the biosynthesis of dopamine and noradrenaline, to compare catecholaminergic neurons in the brain of a species undergoing allopatric speciation. The teleost fish Astyanax mexicanus is extant in two readily available forms, an ancestral river dwelling form (surface) and various derived blind cave forms (cavefish). Adaptation to nutrient poor cave life without predation has led to marked differences in the behavior of this species. The cavefish has lost defensive responses, such as stimulus aversion, found in the ancestral surface fish and instead displays enhanced food seeking behaviors. This is reflected by an increase in catecholamine immunoreactivity in the cavefish brain in regions associated with non-visual sensory perception, motor control pathways, attention, and endocrine release. These neuroanatomical regions include the olfactory system, the basal telencephalon, the preoptic nuclei, the posterior tuberculum, caudal hypothalamus, and isthmus. These results indicate that the evolutionary shift from aversive defensive responses to attractive exploratory behaviors was driven by increases in the size and/or quantity of catecholaminergic neurons in the cavefish brain.

Postprandial sleep in short-sleeping Mexican cavefish

“…Postprandial sleep may provide a mechanism for conserving energy immediately following successful foraging. Conversely, many animals suppress sleep under food-deprived conditions, presumably to forage for food (Macfadyen et al 1973;Danguir and Nicolaidis 1979;Keene et al 2010;Goldstein et al 2018). Larval A. mexicanus survive for only a few days without food, raising the possibility that sleep will be acutely impacted by feeding state.…”

“…Numerous neural mechanisms associated with sleep loss in cavefish have been identified including elevated levels of the wake-promoting neuropeptide Hypocretin (HCRT), changes in wake-promoting catecholamine systems (Duboué et al 2012;Bilandzija et al 2013;Gallman et al 2019) providing candidate regulators of postprandial sleep. Similarly, feeding is increased in multiple populations of adult A. mexicanus (Aspiras et al 2015).…”

“…In many species, sleep deprivation results in increased food intake, while prolonged periods of food deprivation lead to a reduction in metabolic rate and suppression of sleep (Keene et al 2010;Arble et al 2015;Stahl et al 2017;Regalado et al 2017;Goldstein et al 2018). Conversely, animals ranging from the nematode, C. elegans, to humans, increase sleep immediately following a meal, revealing an acute effect of dietary nutrients on sleep regulation (Stahl et al 1983;Murphy et al 2016;Makino et al 2021).…”

Dark world rises: The emergence of cavefish as a model for the study of evolution, development, behavior, and disease

“…Her lab is pioneering methods for implementing CRISPR/Cas9 in A. mexicanus , and has generated surface fish with mutations in the oca2 gene (Klaassen et al, 2018; Stahl, Jaggard, et al, 2019). Multiple labs discussed their efforts to develop a brain atlas for larval and adult A. mexicanus and described how these could be applied to map neuronal regions implicated in sleep and feeding (Gallman, Rivera, & Soares, 2019; Loomis et al, 2019). This study, which expands on several publications from these groups and others (Alié et al, 2018; Jaggard et al, 2017, 2018), demonstrates robust differences in sleep between cave and surface fish.…”