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Unexpected features of Drosophila circadian behavioural rhythms under natural conditions

Abstract

Circadian clocks have evolved to synchronize physiology, metabolism and behaviour to the 24-h geophysical cycles of the Earth1. Drosophila melanogaster’s rhythmic locomotor behaviour provides the main phenotype for the identification of higher eukaryotic clock genes2,3. Under laboratory light–dark cycles, flies show enhanced activity before lights on and off signals4,5, and these anticipatory responses have defined the neuronal sites of the corresponding morning (M) and evening (E) oscillators6,7. However, the natural environment provides much richer cycling environmental stimuli than the laboratory, so we sought to examine fly locomotor rhythms in the wild. Here we show that several key laboratory-based assumptions about circadian behaviour are not supported by natural observations. These include the anticipation of light transitions, the midday ‘siesta’, the fly’s crepuscular activity, its nocturnal behaviour under moonlight, and the dominance of light stimuli over temperature. We also observe a third major locomotor component in addition to M and E, which we term ‘A’ (afternoon). Furthermore, we show that these natural rhythm phenotypes can be observed in the laboratory by using realistic temperature and light cycle simulations. Our results suggest that a comprehensive re-examination of circadian behaviour and its molecular readouts under simulated natural conditions will provide a more authentic interpretation of the adaptive significance of this important rhythmic phenotype. Such studies should also help to clarify the underlying molecular and neuroanatomical substrates of the clock under natural protocols.

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Figure 1: The afternoon (A) component of locomotor activity.
Figure 2: The morning onset (M onset ) of locomotor activity is dependent on temperature and twilight.
Figure 3: Evening onset is temperature and clock modulated.
Figure 4: Diurnal phenotypes of D. melanogaster.

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Acknowledgements

We thank S. Bastianello for building the natural light simulator, and C. Helfrich-Forster for comments on the manuscript. This work was funded by grants from the European Community (the 6th Framework Project EUCLOCK no. 018741; to R.C. and C.P.K.), the Biotechnology and Biological Sciences Research Council and National Environmental Research Council (to C.P.K.), the Royal Society Wolfson Research Merit Award (to C.P.K.) and a Medical Research Council studentship (to E.W.G.) R.C. also thanks the Italian Space Agency (DCMC grant) and the Ministero dell’Università e delle Ricerca (MIUR).

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Contributions

C.P.K. and R.C. conceived the study. C.P.K. supervised the UK work, and R.C. the Italian component. S.B. conducted all the field experiments in the UK, and S.V., F.S. and M.P. the fieldwork in Italy. S.V. performed the laboratory simulations. S.M. performed the per splicing work, and P.M. the immunocytochemistry experiments. E.W.G. developed the software to analyse the behavioural data. Statistical analyses were performed by S.B., S.V. and C.P.K. C.P.K., S.V., S.B. and R.C. wrote the manuscript.

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Correspondence to Rodolfo Costa.

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The authors declare no competing financial interests.

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Vanin, S., Bhutani, S., Montelli, S. et al. Unexpected features of Drosophila circadian behavioural rhythms under natural conditions. Nature 484, 371–375 (2012). https://doi.org/10.1038/nature10991

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