Evolutionary Convergence on Sleep Loss in Cavefish Populations

Abstract

Patterns of sleep vary widely among species, but the functional and evolutionary principles responsible for this diversity remain unknown. The characin fish, Astyanax mexicanus, has eyed surface and numerous blind cave populations. The cave populations are largely independent in their origins, and the species is ideal for studying the genetic bases of convergent evolution. Here we show that this system is also uniquely valuable for the investigation of variability in patterns of sleep. We find that a clearly defined change in ecological conditions, from surface to cave, is correlated with a dramatic reduction in sleep in three independently derived cave populations of A. mexicanus. Analyses of surface × cave hybrids show that the alleles for reduced sleep in the Pachón and Tinaja cave populations are dominant in effect to the surface alleles. Genetic analysis of hybrids between surface and Pachón cavefish suggests that only a small number of loci with dominant effects are involved. Our results demonstrate that sleep is an evolutionarily labile phenotype, highly responsive to changes in ecological conditions. To our knowledge, this is the first example of a single species with a convergence on sleep loss exhibited by several independently evolved populations correlated with population-specific ecologies.

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

“…1b). These results are consistent with previous behavioural studies of Astyanax, which showed that cavefish had higher activity in the night and therefore appeared to sleep less than surface fish 1,3,5 . Together, these molecular and behavioural data reveal that cavefish do possess a functional circadian clock, but one that is distinctly less robust than that of the surface river population.…”

“…Clock-controlled locomotor rhythms are absent in cavefish in DD, following entrainment on a LD cycle. This corroborates previous work on locomotor rhythms in Astyanax, which suggests a significant reduction or lack of rhythmic behaviour in cavefish 3,5 . Cavefish activity in LD is weakly rhythmic, with a general increase in the day, which probably represents a masking influence of the light on their behaviour.…”

“…It has therefore been the generally held view that cave or deep sea animals that have evolved in a constant dark environment have no need for a functional clock and, in fact, no longer possess one. Although this makes apparent sense, there are relatively few studies that have examined circadian clocks in cave species, less that have studied the molecular nature of these clocks and none that have done so under native cave conditions in the wild [1][2][3][4][5][6][7][8][9] .…”

A mutation in the enzyme monoamine oxidase explains part of the Astyanax cavefish behavioural syndrome

“…DA may as well play a role in what could be described as a sort of 'addiction' to food in CF. Third, elevated NA brain levels in CF may be related to their reported loss of sleep 13 . Consistently, a blockade of b1-adrenergic receptors rescues sleep in CF 12 , indeed involving the NA system in this striking behavioural peculiarity.…”

“…Indeed, during the approximately 1 MY since they evolved from their river-dwelling and sighted ancestors 8 , cavefish have evolved a number of morphological, physiological and behavioural traits, most likely in adaptation to the darkness of their subterranean habitat. In particular, Astyanax cave morphs have lost their eyes and their pigmentation, and they have also lost sleep 12,13 , schooling 14,15 and hierarchical aggressive behaviour [16][17][18] . On the other hand, they have gained adaptive behaviours such as attraction to vibrations 19 , increased exploratory [20][21][22][23][24] and food searching behaviour 17 , and a special feeding posture 25,26 .…”