Evolutionary Shift from Fighting to Foraging in Blind Cavefish through Changes in the Serotonin Network

Abstract

We propose that during evolution and adaptation to their cave habitat, cavefish have undergone a behavioral shift, due to modifications of their serotonergic neuronal network. They have lost the typical aggressive behavior of surface fish and evolved a food-seeking behavior that is probably more advantageous to surviving in the dark. We have therefore demonstrated a link between the development of a neuronal network and the likely adaptive behaviors it controls.

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

“…Concerning 5-HT, the pro106leu mutation probably plays a major role. We have also previously reported a difference in the size of the PVa hypothalamic nucleus, which is larger and contains more neurons in CF 17 . We can suppose that both decreased MAO activity and higher cell number contribute to the higher 5-HT levels in CF, and it would actually be difficult to discriminate between the two convergent effects.…”

“…On the other hand, the increased number of cells in the hypothalamus appears like a gain-of-function phenotype. We have recently shown that the change of size of this particular nucleus in cavefish is due to early developmental signalling and neurogenesis timing differences during embryogenesis of the two morphs 17 . Such change corresponds to the 'developmental evolution' component of the variation in monoamine transmission in cavefish.…”

“…This is sometimes referred to as 'the cavefish behavioural syndrome'. Developmental evolution of specific neural circuits is involved in some of these behavioural changes: an increase in the number of serotonin neurons in the cave forms (CF) hypothalamus was shown responsible for their persistent food searching behaviour 17 , and an increase in the number of their head neuromasts is responsible for the emergence of the vibration attraction behaviour 27 . But the origin of most changes in complex motivated behaviours is unknown.…”

“…Indeed, during the approximately 1 MY since they evolved from their river-dwelling and sighted ancestors 8 , cavefish have evolved a number of morphological, physiological and behavioural traits, most likely in adaptation to the darkness of their subterranean habitat. In particular, Astyanax cave morphs have lost their eyes and their pigmentation, and they have also lost sleep 12,13 , schooling 14,15 and hierarchical aggressive behaviour [16][17][18] . On the other hand, they have gained adaptive behaviours such as attraction to vibrations 19 , increased exploratory [20][21][22][23][24] and food searching behaviour 17 , and a special feeding posture 25,26 .…”

“…Indeed, monoaminergic systems are globally well conserved and seem to serve the same types of functions in fish and mammals, with some anatomical and genetic exceptions 31,32 . These include the presence of 5-HT and DA cell bodies in the fish forebrain (5-HT 17,[33][34][35][36][37] ; DA 32,[38][39][40][41][42] ). Also, there are two tyrosine hydroxylases (THs) 43 , two tryptophan hydroxylases (TPH) 44 , and two putative COMT genes 32 in zebrafish (see Fig.…”