Journal Article

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

Yoshizawa, Masato, Robinson, Beatriz G., Duboue, Erik R., Masek, Pavel, Jaggard, James B., O'Quin, Kelly E., Borowsky, Richard L., Jeffery, William R. and Keene, Alex C.

Record Number:
2912
Year:
2015
Journal:
BMC Biology
Pages:
1-17
Volume:
13:15
Short Title:
Distinct genetic architecture underlies the emergence of sleep loss and prey-seeking behavior in the Mexican cavefish
Notes:
yoshizaw@hawaii.edu
URL:
://ZOOREC:ZOOR15108051925
Accession Number:
Zoorec:Zoor15108051925
Language:
English
Abstract:
Background: Sleep 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. Results: We 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. Conclusions: Taken 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.
Times Cited:
1
Author Address:
Usa
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(1964)Thines, G., Wolff-Van Ermengem, F., Boucquey, C. and Soffie, M. (1965)Boucquey, C., Thines, G. and Van Der Borght, C. (1965)Carmignani, M. P. A. (1966)Cavicchioli, G. and Guarnieri, P. (1966)Peters, N. and Peters, G. (1966)Thines, G., Soffie, M. and Vandenbussche, E. (1966)Reed, M. (1966)Sadoglu, P. (1967)Schemmel, C. (1967)Pfeiffer, W. (1967)Pfeiffer, W. (1967)Popper, A. N. and Tavolga, W. N. (1967)Walters, V. and Liu, R. K. (1967)Carmignani, M. P. A. (1968)Mattheij, J. A. (1968)Mattheij, J. A. (1968)Wilkens, H. (1968)Sadoglu, P. and McKee, A. (1969)Mattheij, J. A. (1969)Weiss, B. A. (1969)Mattheij, J. A. and Sprangers, J. A. P. (1969)Gertychowa, R. (1970)Gertychowa, R. (1970)Popper, A. N. (1970)Mattheij, J. A. (1970)Mattheij, J. A. (1970)Weiss, B. and Martini, J. (1970)Whitt, G. S. and Maeda, F. S. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Wilkens, H. (1970)Gertychowa, R. (1971)Popper, A. N. (1971)Zaccone, G. (1971)Wiley, S. and Mitchell, R. W. (1971)Wiley, S. and Mitchell, R. W. (1971)Wilkens, H. (1971)Wilkens, H. (1972)Wilkens, H. (1972)Wilkens, H. (1972)Avise, J. C. and Selander, R. K. (1972)Thines, G. and Wissocq, N. (1972)Wilkens, H. and Burns, R. J. (1972)Zaccone, G. (1972)Schemmel, C. (1973)Thines, G. and LeGrain, J. M. (1973)Voneida, T. J. (1973)Yasuda, K. (1973)Durand, J. P. (1973)Zeitlin, S. M. (1973)Zeitlin, S. M. and McDevitt, D. S. (1973)Mitchell, R. W. (1973)Chakraborty, R. and Nei, M. (1974)Schemmel, C. (1974)Schemmel, C. (1974)Sligar, C. (1974)Omura, Y. (1975)Sadoglu, P. (1975)Peters, N., Scholl, A. and Wilkens, H. (1975)Wilkens, H. (1976)Herwig, H. J. (1976)Herwig, H. J. (1976)Sligar, C. and Voneida, T. J. (1976)Voneida, T. J. and Sligar, C. (1976)Durand, J. P. (1976)Erckens, W. and Weber, F. (1976)Wilkens, H. (1977)Yew, D. T. and Yoshihara, H. M. (1977)Kirby, R. F., Thompson, K. W. and Hubbs, C. (1977)Zaccone, G. (1977)Mitchell, R. W., Russell, W. H. and Elliott, W. R. (1977)Thines, G. and Weyers, M. (1978)Durand, J. P. (1978)Sadoglu, P. 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