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Photic resetting of the circadian clock is correlated with photic habitat in Anolis lizards

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Abstract

Circadian rhythms are regulated by an internal clock, which is itself synchronized to environmental cues such as light and temperature. It is widely assumed that the circadian system is adapted to local cues, which vary enormously across habitats, yet the comparative data necessary for testing this idea are lacking. We examined photic and thermal resetting of the circadian clock in five species of Anolis lizards whose microhabitats differ in the amounts of sun and shade. The primary circadian oscillator in Anolis is the pineal gland, which produces the hormone melatonin. A flow-through culture system was employed to measure rhythmic melatonin output from individually cultured pineal glands. All species showed temperature-compensated circadian rhythms of pineal melatonin. Light caused significant phase delays of the melatonin rhythm, and this effect varied among species. Controlling for phylogenetic differences, the results indicate that the pineal glands of shade-dwelling species are more sensitive to photic resetting than species living in more brightly illuminated habitats. The differences were not due to variation in free-running period, but may be due to variation in oscillator phase and/or robustness. Surprisingly, thermal resetting was not statistically significant. Overall, the results suggest that the Anolis circadian system is adapted to photic habitat.

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Acknowledgments

We gratefully acknowledge the contributions of Dr. Roelof Hut, who wrote the curve-fitting macro and made useful suggestions for sine wave analysis and interpretation. We also thank Dr. Mark Rollag for the donation of melatonin antiserum and for indispensable technical advice, as well as Dr. Edmund Brodie III for equipment and helpful discussion. Animal care and laboratory assistance was provided by Ralph Ababio, Brian Barry, Maridel Fredericksen, Kelly Underwood, and Emily Wrona. Special thanks go to the Departamento de Recursos Naturales y Ambientales of Puerto Rico for allowing us to collect animals from public land. For assistance with animal capture, we thank Dr. Paul Bartell, Dr. Eric Liebgold, Sarah Steiner, and Helen Vasaly. Funding for this project was provided by National Science Foundation Doctoral Dissertation Improvement Grant 0910075 awarded to AFM, MM, and EDB.

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  1. Department of Biology, University of Virginia, PO Box 400328, Charlottesville, VA, 22904-4328, USA

    Ashli F. Moore & Michael Menaker

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  1. Ashli F. Moore
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  2. Michael Menaker
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Correspondence to Michael Menaker.

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359_2012_715_MOESM1_ESM.tif

Online Resource 1. Representative melatonin profiles with fitted sine curves. Melatonin concentrations (unfilled circles) from individual pineal cultures are plotted over time (h in constant conditions). Shown here is a representative profile (one for each species) from the control groups of the light pulse experiment. Only data from the “constant conditions” portion of the cultures were used for curve fitting. The sine wave function (solid line) was fit to the data using non-linear regression (see text) and used to estimate circadian parameters such as phase and free-running period. The mean parameter estimates for each treatment group within each species, along with the fit statistics, are summarized in Table 1 (TIFF 46181 kb)

359_2012_715_MOESM2_ESM.tif

Online Resource 2. Rayleigh plots illustrating the effect of warm temperature pulse treatment on circadian phase of the pineal melatonin rhythm. Circular plots represent one complete circadian cycle of 24 circadian hours (CT). Phases of individual pineal cultures (in CT h) are represented by small circles on the perimeter of the circular plots (black control pineals; gray warm pulse-treated pineals). The arrows represent mean vectors of the circular distributions for each group; the angle of the arrow indicates the mean phase while the length of the arrow is proportional to the phase clustering (a longer arrow reflects more tightly clustered individual phases). The warm temperature pulse treatment caused a small delay in the mean phase of the pineal melatonin rhythm; however, this effect was not statistically significant. Sample sizes and values for phase, vector length r, and circular statistics are given in Table 2 (TIFF 18460 kb)

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Moore, A.F., Menaker, M. Photic resetting of the circadian clock is correlated with photic habitat in Anolis lizards. J Comp Physiol A 198, 375–387 (2012). https://doi.org/10.1007/s00359-012-0715-4

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  • DOI: https://doi.org/10.1007/s00359-012-0715-4

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