Circadian rhythms in Mexican blind cavefish Astyanax mexicanus in the lab and in the field

Beale, Andrew D.; Guibal, Christophe; Tamai, T. Katherine; Klotz, Linda; Cowen, Sophie; Nisembaum, Laura Gabriela; Reynoso, Víctor Hugo; Yamamoto, Yoshiyuki; Whitmore, David

doi:10.1038/ncomms3769

Cited by 129 publications

(188 citation statements)

References 45 publications

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“…Sleep is also regulated by circadian rhythms, and both processes are regulated by metabolic state. Cavefish from the Pachón and Chica caves are behaviorally arrhythmic and light-inducible genes are constitutively elevated (Beale et al, 2013). Further circadian regulation of metabolic rate is dramatically reduced in cavefish, resulting in a significant decrease in total oxygen consumption, suggesting that loss of molecular, metabolic and behavioral rhythms provide a mechanism of energy conservation in cavefish (Moran et al, 2014).…”

Section: Metabolic Regulation Of Sleep and Circadian Functionmentioning

confidence: 99%

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

Jaggard

Robinson

Stahl

et al. 2017

Journal of Experimental Biology

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Sleep is an essential behavior exhibited by nearly all animals, and disruption of this process is associated with an array of physiological and behavioral deficits. Sleep is defined by changes in sensory gating that reduce sensory input to the brain, but little is known about the neural basis for interactions between sleep and sensory processing. Blind Mexican cavefish comprise an extant surface dwelling form and 29 cave morphs that have independently evolved increased numbers of mechanoreceptive lateral line neuromasts and convergent evolution of sleep loss. Ablation of the lateral line enhanced sleep in the Pachoń cavefish population, suggesting that heightened sensory input underlies evolutionarily derived sleep loss. Targeted lateral line ablation and behavioral analysis localized the wake-promoting neuromasts in Pachoń cavefish to superficial neuromasts of the trunk and cranial regions. Strikingly, lateral line ablation did not affect sleep in four other cavefish populations, suggesting that distinct neural mechanisms regulate the evolution of sleep loss in independently derived cavefish populations. Cavefish are subject to seasonal changes in food availability, raising the possibility that sensory modulation of sleep is influenced by metabolic state. We found that starvation promotes sleep in Pachoń cavefish, and is not enhanced by lateral line ablation, suggesting that functional interactions occur between sensory and metabolic regulation of sleep. Taken together, these findings support a model where sensory processing contributes to evolutionarily derived changes in sleep that are modulated in accordance with food availability.

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Section: Metabolic Regulation Of Sleep and Circadian Functionmentioning

confidence: 99%

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

Jaggard

Robinson

Stahl

et al. 2017

Journal of Experimental Biology

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“…Paradoxically, despite their lower metabolic rate, cavefish are actually more active. On this basis, Beale et al (11) proposed that the cavefish experience "constant light" rather than perpetual darkness. The distinct metabolic rates between cave and surface populations provide a unique opportunity to uncover the genetic architecture underlying metabolic variation in vertebrates and how cave animals can cope with limited and infrequent food supply.…”

mentioning

confidence: 99%

“…Furthermore, there are multiple independently evolved cave populations that share similar traits, allowing for the study of parallelism in evolution (4). Previous work has focused on understanding the genetic architecture of morphological and behavioral traits, such as pigmentation (5-7), eye size (6), schooling (8), and feeding angle (9); however, relatively little work has gone into understanding physiological traits (10,11). Protas et al (6) mapped sensitivity to dissolved amino acids, weight loss on sustained fasts, and condition factor using quantitative trait loci (QTL) analysis, but the genetic underpinning has not been identified for any of these traits.…”

mentioning

confidence: 99%

Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions

Aspiras

Rohner

Martineau

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

213

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Despite recent advances in the understanding of morphological evolution, the genetic underpinnings of behavioral and physiological evolution remain largely unknown. Here, we study the metabolic changes that evolved in independently derived populations of the Mexican cavefish, Astyanax mexicanus. A hallmark of cave environments is scarcity of food. Cavefish populations rely almost entirely on sporadic food input from outside of the caves. To survive under these conditions, cavefish have evolved a range of adaptations, including starvation resistance and binge eating when food becomes available. The use of these adaptive strategies differs among independently derived cave populations. Although all cavefish populations tested lose weight more slowly than their surface conspecifics during restricted rations, only a subset of cavefish populations consume more food than their surface counterparts. A candidate gene-based screen led to the identification of coding mutations in conserved residues of the melanocortin 4 receptor (MC4R) gene, contributing to the insatiable appetite found in some populations of cavefish. Intriguingly, one of the mutated residues has been shown to be linked to obesity in humans. We demonstrate that the allele results in both reduced maximal response and reduced basal activity of the receptor in vitro. We further validate in vivo that the mutated allele contributes to elevated appetite, growth, and starvation resistance. The allele appears to be fixed in cave populations in which the overeating phenotype is present. The presence of the same allele in multiple caves appears to be due to selection from standing genetic variation present in surface populations.Astyanax mexicanus | cavefish | MC4R | metabolic evolution | hyperphagia T he dark and relatively nutrient-poor environment of caves imposes strong selective pressures on colonizing species. As a consequence of the pitch-black environment, no photosynthetic primary producers exist in the caves. Cave inhabitants therefore rely entirely on food chains originating outside of the caves. The external food input can be introduced into the cave environments by bats living in the caves or through seasonal flooding. As a consequence, the food supply is limited and infrequent (1). To deal with this challenge, obligate cave species converge on similar metabolic adaptations, such as reduced metabolic rate, increased metabolic efficiency (weight gain/food consumed), starvation resistance (reduced weight loss during fasting), and increased body fat composition (2). To understand the underlying genetic basis of metabolic evolution better, we have focused on Astyanax mexicanus, the Mexican cavefish. There are two distinct forms of this species, a surface form and a cave form that displays a reduction or absence of melanin pigmentation and is eyeless (reviewed in 3). Although these morphs exhibit numerous morphological and behavioral differences, they remain interfertile. Furthermore, there are multiple independently evolved cave populations that share simi...

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“…Circadian locomotor activity has been subject of study in other populations of some caves in the El Abra System (Erkens and Martin 1982a and b;Thines and Weyers;1978). Recent studies confirm that circadian activity at molecular clockwork still can be detected in specimens collected at the Chica and Pachon caves (Beale et al 2013) but some fish collected in these locations also show attenuated and arrhythmic metabolism (Moran et al 2014). When cyclic motor activity persists, it is consistent with the expression of clock genes monitored in the fins of fish from La Chica cave (Beale et al 2013).…”

Section: Introductionmentioning

confidence: 77%

“…Circadian locomotor activity has been detected in laboratory conditions in diverse species of cave-dwelling animals such as: fish (Beale et al 2013, Cavallari et al 2011Trajano et al 2005;Trajano et al 2012, Pati 2001, crustaceans (De la O- Martinez et al 2004), crickets (Hoenen, 2005) millipedes (Koilraj et al 2000), spiders (Soriano-Morales et al 2013;Hoenen and Gnaspini, 1999) beetles (Pasquali and Sbordoni, 2014) salamanders (Hervant and Durand, 2000) frogs (Espino Del Castillo et al 2009) and bats Joshi and Vanlalnghaka, 2005) indicating that the mechanisms underlying circadian rhythms in these species are still functional in a diverse range of expression, from nearly arrhythmic to a well defined cyclic activity. Such diversity in expressions seems to be related with the animal´s niche if they are troglophile, trogloxene (both may be part of their life cycle in surface conditions) or troglobiotic (all their biological cycles occur in caves).…”

Section: Introductionmentioning

confidence: 99%

Circadian rhythms and photic entrainment of swimming activity in cave-dwelling fishAstyanax mexicanus(Actinopterygii: Characidae), from El Sotano La Tinaja, San Luis Potosi, Mexico

Caballero-Hernández

Hernández-Patricio

Sigala

et al. 2015

Biological Rhythm Research

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Running title: Circadian rhythms in cave-dwelling fish Astyanax Abstract:Circadian regulation has a profound adaptive meaning in timing the best performance of biological functions in a cyclic niche. However, in cave-dwelling animals (troglobiotic) a lack of photic cyclic environment may represent a disadvantage for persistence of circadian rhythms. There are different populations of cave-dwelling fish Astyanax mexicanus in caves of the Sierra El Abra, Mexico, with different evolutive history. In the present work we report that fish collected from El Sótano la Tinaja show circadian rhythms of swimming activity in laboratory conditions. Rhythms observed in some of the organisms entrain to either continuous light-dark cycles or discrete skeleton photoperiods tested. Our results indicate that circadian rhythm of swimming activity and their ability to entrain in discrete and continuous photoperiods persist in some organisms that might represent one of the oldest populations of cave-dwelling Astyanax mexicanus in the Sierra

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Circadian rhythms in Mexican blind cavefish Astyanax mexicanus in the lab and in the field

Cited by 129 publications

References 45 publications

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

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

Melanocortin 4 receptor mutations contribute to the adaptation of cavefish to nutrient-poor conditions

Circadian rhythms and photic entrainment of swimming activity in cave-dwelling fishAstyanax mexicanus(Actinopterygii: Characidae), from El Sotano La Tinaja, San Luis Potosi, Mexico

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