Evolution of the acoustic startle response of Mexican cavefish

Abstract

The ability to detect threatening stimuli and initiate an escape response is essential for survival and under stringent evolutionary pressure. In diverse fish species, acoustic stimuli activate Mauthner neurons, which initiate a C-start escape response. This reflexive behavior is highly conserved across aquatic species and provides a model for investigating the neural mechanism underlying the evolution of escape behavior. Here, we characterize evolved differences in the C-start response between populations of the Mexican cavefish, Astyanax mexicanus. Cave populations of A. mexicanus inhabit an environment devoid of light and macroscopic predators, resulting in evolved differences in various morphological and behavioral traits. We find that the C-start is present in river-dwelling surface fish and multiple populations of cavefish, but that response kinematics and probability differ between populations. The Pachón population of cavefish exhibits an increased response probability, a slower response latency and speed, and reduction of the maximum bend angle, revealing evolved differences between surface and cave populations. Analysis of the responses of two other independently evolved populations of cavefish, revealed the repeated evolution of reduced angular speed. Investigation of surface-cave hybrids reveals a correlation between angular speed and peak angle, suggesting these two kinematic characteristics are related at the genetic or functional levels. Together, these findings provide support for the use of A. mexicanus as a model to investigate the evolution of escape behavior.

Metabolic reprogramming underlies cavefish muscular endurance despite loss of muscle mass and contractility

“…S1A) than surface fish. These findings are consistent with Paz et al (2020), who found cavefish have reduced angular velocity during a C-start (escape) response, differences observed as early as 6 days post fertilization. Providing support that these differences are not a consequence of laboratory conditions, video recordings of wild cavefish (Pachón cave) and wild surface fish (Rio Choy) swimming revealed surface fish incorporate sustained moderate swimming – a form of rheotaxis required to remain stationary against the river current – interspersed by vigorous burst-like swimming (Movie S2A).…”

Characterizing the genetic basis of trait evolution in the Mexican cavefish

“…To assess escape response kinematics, plates containing fish in individual wells were fastened to a small vibration excitor and the response to escape-inducing vibration was measured with a high-speed camera (Figure 2D). The angular speed of cavefish was reduced, approaching significance (P=0.06), while the peak angle was also reduced (Figure 2E,F), consistent with a previous report that the escape response is blunted in cavefish (Paz et al 2020). Finally, we measured locomotor activity in cavefish because it is a critical for aspects of predator avoidance and foraging.…”

“…Cave-dwelling forms have converged on distinct morphological traits, including albinism and eye loss (Jeffery 2020). In addition, cavefish evolved numerous behavioral changes including different prey capture, startle response, and increased locomotor activity (Duboué et al 2011;Lloyd et al 2018;Paz et al 2020). Overall these changes are thought to be critical for foraging in the absence of visual cues (Yoshizawa 2015;Keene and Duboue 2018;McGaugh et al 2020).…”

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

“…Like morphology, neural circuits can adapt to the environment. Of these, many circuits are sensory and regulate essential behaviors such as foraging, navigation, and escapes ( Blin et al, 2018 ; Hoke et al, 2012 ; Hüppop, 1987 ; Paz et al, 2020 ).…”