Feed or fight: A behavioral shift in blind cavefish

Abstract

Within the species Astyanax mexicanus, there are several inter-fertile populations of river-dwelling sighted fish and cave-dwelling blind fish which have evolved morphological and behavioral adaptations. We have recently reported a developmental and neurophysiological basis for the loss of aggressive behavior in the blind cavefish morph of Astyanax. Using an appropriate behavioral assay, we have shown that surface Astyanax show intense dominance-related aggressiveness. The expression of this behavior is inversely correlated with the serotonin (5HT) levels in their hindbrain raphe nucleus. Moreover this behavior is not solely visually-evoked and has a genetic component. Conversely in cavefish, there is no raphe-driven dominance aggressiveness. Instead, the embryonic Sonic Hedgehog–dependent modification of the size of a serotonergic neuronal group localized in their hypothalamus causes a shift in their behavioral pattern: instead of fighting, they search for food. Here we further discuss the origin and nature of this behavioral shift.

Contrasting feeding habits of post-larval and adult Astyanax cavefish

“…There is a plethora of literature on Astyanax cavefish discussing the adaptations that allow them to be very skilful at locating nourishment in an environment where food is often scarce (Espinasa et al 2014;Rétaux and Elipot 2013;Soares and Niemiller 2013;Yoshizawa 2015). Our results confirm that they are indeed excellent hunters, but suggest that, at least in this cave and for this particular stage in their ontogeny, food is not that limiting.…”

A mutation in the enzyme monoamine oxidase explains part of the Astyanax cavefish behavioural syndrome

“…6). First, the MAO mutation and decreased MAO activity in CF may constitute part of the molecular basis for changes in 'social' behaviours in cavefish, including their loss of aggressiveness 17,57 and schooling 14 behaviours. Accordingly, deprenyl-treated SF show reduced aggressiveness 17 and reduced schooling 14 , whereas deprenyltreated CF show no change in these behaviours.…”

“…Here we show that the leu 106 allele is also present in the Tinaja population. Finally, we have previously proposed that the loss of aggressiveness in cavefish is related to a general loss of social or collective behaviours during their evolution in subterranean environment 57 . Therefore, the loss of aggressiveness and the loss of schooling could be somehow 'linked', both resulting from the MAO mutation and from the 'hyperserotonergic' phenotype.…”

“…Second, the MAO-dependent high 5-HT neurotransmission index is also relevant to CF-increased foraging behaviour 17,57 and behavioural drive for food (hypothesis in ref. 58).…”

“…In red, developmental evolution of a neuronal 5-HT group of the anterior hypothalamus contributes to higher 5-HT content in the forebrain of the Pachón CF. This process is dependent on Sonic Hedgehog signalling during early embryogenesis and leads to a cavefish-specific behavioural phenotype consisting in persistent foraging 17,57 . In blue, the MAO mutation leads to low MAO activity and high 5-HT content throughout the CF brain.…”