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

Yoshizawa M, Robinson BG, Duboué ER, Masek P, Jaggard JB, O'Quin KE, Borowsky RL, Jeffery WR, Keene AC - BMC Biol. (2015)

Bottom Line: Sleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Nevada, Reno, Reno, NV, 89557, USA. yoshizaw@hawaii.edu.

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.

Show MeSH
VAB does not segregate with sleep or locomotor activity in hybrid or outbred cavefish populations. (A) F2 and F3 hybrid fish were generated from a female surface fish and a male Pachón cavefish. Hybrid fish were then tested for vibration attraction behavior (VAB) followed by locomotor activity (B-D). No correlation was observed between VAB and locomotor activity (B), sleep duration (C) and bout number (D) (P >0.05). (E-G) Pachón cavefish were assayed for VAB and locomotor behavior. No correlation was observed between VAB and locomotor activity (E), sleep duration (F) and bout number (G) (P >0.05).
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Fig3: VAB does not segregate with sleep or locomotor activity in hybrid or outbred cavefish populations. (A) F2 and F3 hybrid fish were generated from a female surface fish and a male Pachón cavefish. Hybrid fish were then tested for vibration attraction behavior (VAB) followed by locomotor activity (B-D). No correlation was observed between VAB and locomotor activity (B), sleep duration (C) and bout number (D) (P >0.05). (E-G) Pachón cavefish were assayed for VAB and locomotor behavior. No correlation was observed between VAB and locomotor activity (E), sleep duration (F) and bout number (G) (P >0.05).

Mentions: Enhanced locomotor activity and VAB are proposed to be adaptive traits that improve the probability of finding food in a nutrient-poor environment [9,10,32]. It is possible that conserved genetic architecture underlies VAB and sleep loss in Pachón cavefish. Alternatively, these traits may have distinct genetic mechanisms that underlie the co-evolution of these traits in Pachón cavefish. To differentiate between these two possibilities, we generated F2 and F3 hybrid fish from a cross of surface fish and Pachón cavefish and individual fish were assayed for sleep duration, locomotor activity and VAB (Figure 3A). All three traits were highly variable in hybrid fish allowing for analysis of trait segregation. The presence of VAB did not correlate with locomotor activity, sleep duration or bout number in surface-Pachón hybrids, suggesting that distinct genetic mechanisms underlie the regulation of locomotor activity and VAB (Figure 3B-D).Figure 3


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

Yoshizawa M, Robinson BG, Duboué ER, Masek P, Jaggard JB, O'Quin KE, Borowsky RL, Jeffery WR, Keene AC - BMC Biol. (2015)

VAB does not segregate with sleep or locomotor activity in hybrid or outbred cavefish populations. (A) F2 and F3 hybrid fish were generated from a female surface fish and a male Pachón cavefish. Hybrid fish were then tested for vibration attraction behavior (VAB) followed by locomotor activity (B-D). No correlation was observed between VAB and locomotor activity (B), sleep duration (C) and bout number (D) (P >0.05). (E-G) Pachón cavefish were assayed for VAB and locomotor behavior. No correlation was observed between VAB and locomotor activity (E), sleep duration (F) and bout number (G) (P >0.05).
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4364459&req=5

Fig3: VAB does not segregate with sleep or locomotor activity in hybrid or outbred cavefish populations. (A) F2 and F3 hybrid fish were generated from a female surface fish and a male Pachón cavefish. Hybrid fish were then tested for vibration attraction behavior (VAB) followed by locomotor activity (B-D). No correlation was observed between VAB and locomotor activity (B), sleep duration (C) and bout number (D) (P >0.05). (E-G) Pachón cavefish were assayed for VAB and locomotor behavior. No correlation was observed between VAB and locomotor activity (E), sleep duration (F) and bout number (G) (P >0.05).
Mentions: Enhanced locomotor activity and VAB are proposed to be adaptive traits that improve the probability of finding food in a nutrient-poor environment [9,10,32]. It is possible that conserved genetic architecture underlies VAB and sleep loss in Pachón cavefish. Alternatively, these traits may have distinct genetic mechanisms that underlie the co-evolution of these traits in Pachón cavefish. To differentiate between these two possibilities, we generated F2 and F3 hybrid fish from a cross of surface fish and Pachón cavefish and individual fish were assayed for sleep duration, locomotor activity and VAB (Figure 3A). All three traits were highly variable in hybrid fish allowing for analysis of trait segregation. The presence of VAB did not correlate with locomotor activity, sleep duration or bout number in surface-Pachón hybrids, suggesting that distinct genetic mechanisms underlie the regulation of locomotor activity and VAB (Figure 3B-D).Figure 3

Bottom Line: Sleep is characterized by extended periods of quiescence and reduced responsiveness to sensory stimuli.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.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.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Nevada, Reno, Reno, NV, 89557, USA. yoshizaw@hawaii.edu.

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.

Show MeSH