Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish

Abstract

BackgroundSleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli. Animals ranging from insects to mammals adapt to environments with limited food by suppressing sleep and enhancing their response to food cues, yet little is known about the genetic and evolutionary relationship between these processes. The blind Mexican cavefish, Astyanax mexicanus is a powerful model for elucidating the genetic mechanisms underlying behavioral evolution. A. mexicanus comprises an extant ancestral-type surface dwelling morph and at least five independently evolved cave populations. Evolutionary convergence on sleep loss and vibration attraction behavior, which is involved in prey seeking, have been documented in cavefish raising the possibility that enhanced sensory responsiveness underlies changes in sleep.ResultsWe established a system to study sleep and vibration attraction behavior in adult A. mexicanus and used high coverage quantitative trait loci (QTL) mapping to investigate the functional and evolutionary relationship between these traits. Analysis of surface-cave F2 hybrid fish and an outbred cave population indicates that independent genetic factors underlie changes in sleep/locomotor activity and vibration attraction behavior. High-coverage QTL mapping with genotyping-by-sequencing technology identify two novel QTL intervals that associate with locomotor activity and include the narcolepsy-associated tp53 regulating kinase. These QTLs represent the first genomic localization of locomotor activity in cavefish and are distinct from two QTLs previously identified as associating with vibration attraction behavior.ConclusionsTaken together, these results localize genomic regions underlying sleep/locomotor and sensory changes in cavefish populations and provide evidence that sleep loss evolved independently from enhanced sensory responsiveness.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-015-0119-3) contains supplementary material, which is available to authorized users.

The lateral line confers evolutionarily derived sleep loss in the Mexican cavefish

“…2A,B), revealing the convergent evolution of sleep loss in cave populations (Duboué et al, 2011;Yoshizawa et al, 2015). Furthermore, the convergent evolution of enhanced lateral line function or increased neuromast morphology has been reported in Pachón, Los Sabinos, Piederas, Tinaja and Molino populations of cavefish (Kowalko et al, 2013;Yoshizawa et al, 2010).…”

The Evolution of Sensory Adaptation in Astyanax mexicanus

“…Electrophysiological studies have also suggested that the pineal photosensory function still persists in adult blind cavefish (Tabata, 1982). Indeed, cavefish show largely reduced sleep and attenuated circadian rhythm (see Chapters 16 and 17; Beale et al, 2013;Duboué et al, 2011Duboué et al, , 2012Yoshizawa et al, 2015); however, reproduction is critical. Yoshizawa et al assumed that the pineal organ is retained in cavefish because of its thermo-sensing ability, and its light-sensing ability can be just residual.…”

Behaviors of cavefish offer insight into developmental evolution

“…In summary, the cavefish serves as an excellent model to study the evolution of multiple morphological and behavioral traits because it has provided evidence that morphological and behavioral traits evolved through complex manners. The latest A. mexicanus behaviors studied include: enhanced prey capture ability in 25-day-old cavefish in the dark (Espinasa et al, 2014); feeding control via appetite-related hormones (Penney et al, 2014); and loss of circadian rhythm and sleep (Dubou e et al, 2011(Dubou e et al, , 2012Beale et al, 2013;Moran et al, 2014;Yoshizawa et al, 2015). The next frontier in cavefish research will be to identify more of the genes and mutations involved in the adaptation to the cave environment, thereby establishing a field where genetics, ontogeny, neuroscience, phylogeny, and ecology are integrated.…”