BACKGROUND: Within the species Astyanax mexicanus, there are several interfertile populations of river-dwelling sighted fish and cave-dwelling blind fish which have evolved morphological and behavioral adaptations, the origins of which are unknown. Here, we have investigated the neural, genetic, and developmental bases for the evolution of aggressive behavior in this teleost. RESULTS: We used an intruder-resident behavioral assay to compare aggressiveness quantitatively (attack counts) and qualitatively (pattern and nature of attacks) between the surface and cave populations of Astyanax. Using this paradigm, we characterize aggressive behavior in surface fish, bring support for the genetic component of this trait, and show that it is controlled by raphe serotonergic neurons and that it corresponds to the establishment of dominance between fish. Cavefish have completely lost such aggressive/dominance behavior. The few attacks performed by cavefish during the behavioral test instead correspond to food-seeking behavior, driven by the developmental evolution of their hypothalamic serotonergic paraventricular neurons, itself due to increased Sonic Hedgehog signaling during early forebrain embryogenesis. CONCLUSIONS: 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.
BACKGROUND: Within the species Astyanax mexicanus, there are several interfertile populations of river-dwelling sighted fish and cave-dwelling blind fish which have evolved morphological and behavioral adaptations, the origins of which are unknown. Here, we have investigated the neural, genetic, and developmental bases for the evolution of aggressive behavior in this teleost. RESULTS: We used an intruder-resident behavioral assay to compare aggressiveness quantitatively (attack counts) and qualitatively (pattern and nature of attacks) between the surface and cave populations of Astyanax. Using this paradigm, we characterize aggressive behavior in surface fish, bring support for the genetic component of this trait, and show that it is controlled by raphe serotonergic neurons and that it corresponds to the establishment of dominance between fish. Cavefish have completely lost such aggressive/dominance behavior. The few attacks performed by cavefish during the behavioral test instead correspond to food-seeking behavior, driven by the developmental evolution of their hypothalamic serotonergic paraventricular neurons, itself due to increased Sonic Hedgehog signaling during early forebrain embryogenesis. CONCLUSIONS: 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.
Authors: Johanna E Kowalko; Nicolas Rohner; Tess A Linden; Santiago B Rompani; Wesley C Warren; Richard Borowsky; Clifford J Tabin; William R Jeffery; Masato Yoshizawa Journal: Proc Natl Acad Sci U S A Date: 2013-10-01 Impact factor: 11.205
Authors: Jacqueline S R Chin; Claude E Gassant; Paloma M Amaral; Evan Lloyd; Bethany A Stahl; James B Jaggard; Alex C Keene; Erik R Duboue Journal: Dev Biol Date: 2018-05-25 Impact factor: 3.582
Authors: Jasmine L Loveland; Natalie Uy; Karen P Maruska; Russ E Carpenter; Russell D Fernald Journal: J Exp Biol Date: 2014-05-22 Impact factor: 3.312
Authors: Suzanne E McGaugh; Johanna E Kowalko; Erik Duboué; Peter Lewis; Tamara A Franz-Odendaal; Nicolas Rohner; Joshua B Gross; Alex C Keene Journal: J Exp Zool B Mol Dev Evol Date: 2020-07-07 Impact factor: 2.656
Authors: Johanna E Kowalko; Nicolas Rohner; Santiago B Rompani; Brant K Peterson; Tess A Linden; Masato Yoshizawa; Emily H Kay; Jesse Weber; Hopi E Hoekstra; William R Jeffery; Richard Borowsky; Clifford J Tabin Journal: Curr Biol Date: 2013-09-12 Impact factor: 10.834