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      Endocrine–circadian interactions in birds: implications when nights are no longer dark

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          Abstract

          Biological clocks are evolved time-keeping systems by which organisms rhythmically coordinate physiology within the body, and align it with rhythms in their environment. Clocks are highly sensitive to light and are at the interface of several major endocrine pathways. Worryingly, exposure to artificial-light-at-night (ALAN) is rapidly increasing in ever more extensive parts of the world, with likely impact on wild organisms mediated by endocrine–circadian pathways. In this overview, we first give a broad-brush introduction to biological rhythms. Then, we outline interactions between the avian clock, endocrine pathways, and environmental and internal modifiers. The main focus of this review is on the circadian hormone, melatonin. We summarize information from avian field and laboratory studies on melatonin and its relationships with behaviour and physiology, including often neglected developmental aspects. When exposed to ALAN, birds are highly vulnerable to disruption of behavioural rhythms and of physiological systems under rhythmic control. Several studies suggest that melatonin is likely a key mediator for a broad range of effects. We encourage further observational and experimental studies of ALAN impact on melatonin, across the full functional range of this versatile signalling molecule, as well as on other candidate compounds at the endocrine–circadian interface.

          This article is part of the theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’.

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          Most cited references137

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          Artificially lit surface of Earth at night increasing in radiance and extent

          Earth’s artificially lit area is expanding at 2.2% per year, with existing lit areas brightening by 2.2% per year.
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            Melatonin: an ancient molecule that makes oxygen metabolically tolerable.

            Melatonin is remarkably functionally diverse with actions as a free radical scavenger and antioxidant, circadian rhythm regulator, anti-inflammatory and immunoregulating molecule, and as an oncostatic agent. We hypothesize that the initial and primary function of melatonin in photosynthetic cyanobacteria, which appeared on Earth 3.5-3.2 billion years ago, was as an antioxidant. The evolution of melatonin as an antioxidant by this organism was necessary as photosynthesis is associated with the generation of toxic-free radicals. The other secondary functions of melatonin came about much later in evolution. We also surmise that mitochondria and chloroplasts may be primary sites of melatonin synthesis in all eukaryotic cells that possess these organelles. This prediction is made on the basis that mitochondria and chloroplasts of eukaryotes developed from purple nonsulfur bacteria (which also produce melatonin) and cyanobacteria when they were engulfed by early eukaryotes. Thus, we speculate that the melatonin-synthesizing actions of the engulfed bacteria were retained when these organelles became mitochondria and chloroplasts, respectively. That mitochondria are likely sites of melatonin formation is supported by the observation that this organelle contains high levels of melatonin that are not impacted by blood melatonin concentrations. Melatonin has a remarkable array of means by which it thwarts oxidative damage. It, as well as its metabolites, is differentially effective in scavenging a variety of reactive oxygen and reactive nitrogen species. Moreover, melatonin and its metabolites modulate a large number of antioxidative and pro-oxidative enzymes, leading to a reduction in oxidative damage. The actions of melatonin on radical metabolizing/producing enzymes may be mediated by the Keap1-Nrf2-ARE pathway. Beyond its direct free radical scavenging and indirect antioxidant effects, melatonin has a variety of physiological and metabolic advantages that may enhance its ability to limit oxidative stress.
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              Thyrotrophin in the pars tuberalis triggers photoperiodic response.

              Molecular mechanisms regulating animal seasonal breeding in response to changing photoperiod are not well understood. Rapid induction of gene expression of thyroid-hormone-activating enzyme (type 2 deiodinase, DIO2) in the mediobasal hypothalamus (MBH) of the Japanese quail (Coturnix japonica) is the earliest event yet recorded in the photoperiodic signal transduction pathway. Here we show cascades of gene expression in the quail MBH associated with the initiation of photoinduced secretion of luteinizing hormone. We identified two waves of gene expression. The first was initiated about 14 h after dawn of the first long day and included increased thyrotrophin (TSH) beta-subunit expression in the pars tuberalis; the second occurred approximately 4 h later and included increased expression of DIO2. Intracerebroventricular (ICV) administration of TSH to short-day quail stimulated gonadal growth and expression of DIO2 which was shown to be mediated through a TSH receptor-cyclic AMP (cAMP) signalling pathway. Increased TSH in the pars tuberalis therefore seems to trigger long-day photoinduced seasonal breeding.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Writing – original draftRole: Writing – review & editing
                Role: Writing – review & editing
                Role: Writing – review & editing
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                March 25, 2024
                February 05, 2024
                February 05, 2024
                : 379
                : 1898 , Theme issue ‘Endocrine responses to environmental variation: conceptual approaches and recent developments’ compiled and edited by Frank Seebacher and Alexander G. Little
                : 20220514
                Affiliations
                [ 1 ] Swiss Ornithological Institute, , Bird Migration Unit, Seerose 1, 6204 Sempach, Switzerland
                [ 2 ] Department of Biological Sciences, North Dakota State University, , Fargo, ND 58102, USA
                [ 3 ] Department of Animal Physiology and Ethology, Faculty of Natural Sciences, Comenius University, , Bratislava SK 84215, Slovakia
                Author notes

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.7007959.

                Author information
                http://orcid.org/0000-0002-6648-1463
                https://orcid.org/0000-0002-2712-6805
                Article
                rstb20220514
                10.1098/rstb.2022.0514
                10838642
                38310930
                2eeb2180-ce95-4924-babb-2b6007187dd7
                © 2024 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : July 24, 2023
                : September 18, 2023
                Categories
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                Custom metadata
                March 25, 2024

                Philosophy of science
                melatonin,clock,light pollution,alan,annual timing,development
                Philosophy of science
                melatonin, clock, light pollution, alan, annual timing, development

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