Evolutionary convergence of a neural mechanism in the cavefish lateral line system

Abstract

Animals can evolve dramatic sensory functions in response to environmental constraints, but little is known about the neural mechanisms underlying these changes. The Mexican tetra, Astyanax mexicanus, is a leading model to study genetic, behavioral, and physiological evolution by comparing eyed surface populations and blind cave populations. We compared neurophysiological responses of posterior lateral line afferent neurons and motor neurons across A. mexicanus populations to reveal how shifts in sensory function may shape behavioral diversity. These studies indicate differences in intrinsic afferent signaling and gain control across populations. Elevated endogenous afferent activity identified a lower response threshold in the lateral line of blind cavefish relative to surface fish leading to increased evoked potentials during hair cell deflection in cavefish.. We next measured the effect of inhibitory corollary discharges from hindbrain efferent neurons onto afferents during locomotion. We discovered that three independently-derived cavefish populations have evolved persistent afferent activity during locomotion, suggesting for the first time that partial loss of function in the efferent system can be an evolutionary mechanism for neural adaptation of a vertebrate sensory system.

Sensing in the dark: Constructive evolution of the lateral line system in blind populations of Astyanax mexicanus

“…Pachón cavefish remained unaffected, with sustained neurotransmission. Inhibition of the hair cell synapse in surface fish during swimming is similar to other fish species with intact visual systems, which suggests a unique mechanism evolved in blind cavefish for sustained neurotransmission of the lateral line hair cell afferents (Flock & Russell, 1973;Lunsford et al, 2022Lunsford et al, , 2019Pichler & Lagnado, 2020). However, because efferent neurons are still present and innervating posterior lateral line hair cells in Pachón cavefish, it is likely that other mechanisms are underlying enhanced neurotransmission, like higher sensitivity of the ribbon synapse (discussed below).…”

“…These expansions are also found in other cavefish species (Soares & Niemiller, 2020 ). In A. mexicanus cavefish, lateral line expansions mostly correspond to the anterior lateral line and are apparent as early as 6 days post‐fertilization (dpf) (Figure 2 ) (Lunsford et al., 2022 ). Expansion of the lateral line means that there are more neuromasts and, in turn, more hair cells.…”

Evolution of olfactory sensitivity, preferences and behavioral responses in Mexican cavefish: fish personality matters

“…Finally, Pachón CF, SF and F2 hybrids possess markedly different sensory apparatuses and capacities, not only for chemo- but also for mechano-sensation (Lunsford et al, 2022; Yoshizawa et al, 2010). Therefore, to test behavioral responses specific to olfactory stimuli, we wanted to find a way to deliver odors that would be vibration-less.…”

Sensory evolution in a cavefish radiation: patterns of neuromast distribution and associated behaviour inSinocyclocheilus(Cypriniformes: Cyprinidae)

“…Wall-following behaviour has also been characterized in A. mexicanus ; however, eyeless morphs orient their lateral side with fewer neuromasts towards the wall, while perhaps using the opposite side for detecting stimuli important for feeding, communication and spatial learning [14,42]. Eyeless Sinocyclocheilus species show a similar pattern of asymmetry; however, herein the side with more neuromasts appears to be essential for mediating this lateral preference [64].…”