Biological Timekeeping Clocks, Rhythms and Behaviour

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Vinod Kumar
Editor

Biological Timekeeping:
Clocks, Rhythms
and Behaviour
Editor
Vinod Kumar
Department of Zoology
University of Delhi
Delhi, India

ISBN 978-81-322-3686-3 ISBN 978-81-322-3688-7 (eBook)

DOI 10.1007/978-81-322-3688-7

Library of Congress Control Number: 2016963684

© Springer (India) Pvt. Ltd. 2017

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Dedicated to my mother and father who
always encouraged me to be honest,
hardworking and truthful.
Foreword

Biology is the study of life in its full richness from the evolution of cyanobacteria
three billion years ago to the human menagerie of 7.5 billion souls on earth today.
This compendium of 31 chapters edited by Vinod Kumar is really a tribute to the
biology of life from the perspective of time. Life and evolution are dynamic and
cannot be severed from the inevitable march of time. Because life on earth is slave
to the energetic cycle of the solar day (both as a resource and as a detriment),
essentially all life forms evolved internal timing systems to anticipate and measure
the time of the (now) 24-h day. This collection of essays is truly a rich and vibrant
set that spans not only the range of organismal diversity (from cyanobacteria to
humans) but also the spectrum of time (from ultradian, to tidal, to circadian, to
circannual). Part I addresses the “History, Concepts, Evolution, and Basic Features
of Biological Clock” and is a refreshing view of the history and development of the
field and the evolution of timekeeping, as well as an excellent primer for under-
standing circadian concepts and analytical methods. Part II on “Animal Clocks:
Complexity and Diversity” reviews the physiological organization of insect and
vertebrate circadian systems, including Drosophila, fish (and zebrafish), amphib-
ians, reptiles, birds and mammals. Part III on “Human Circadian Rhythms: Entrain-
ment and Sleep Regulation” discusses the physiology and behavior of human
circadian rhythms, their implications for health, their regulation by environmental
factors, as well as their impact on the timing of sleep. Part IV on “Clock Interactions
Within and Between Individual and the Natural World” brings into perspective the
novel questions that have arisen from the discovery of cell-autonomous oscillators
throughout the body and how this new system architecture of the physiological
clock is organized and regulated, the implications of circadian photoentrainment
arising from the discovery of intrinsically photosensitive melanopsin-containing
retinal ganglion cells, the paradoxical role of non-photic entrainment cues in both
nocturnal and diurnal animals, and the important role of temperature as an
entraining signal. Part V on “Circadian Clocks, Metabolism, and Immune Func-
tions” highlights the recent explosion of work linking the circadian clock at the
molecular level to metabolism, immunity, and cancer. This is a huge growth area in

vii
viii Foreword

the field that has wide-ranging implications for human health and medicine. Part VI
on “Pineal, Melatonin, and Biological Timekeeping” reprises the long history of
melatonin as one of the first biomarkers of the clock system in animals, its divergent
role in mammals and nonmammalian vertebrates, and its central role in avian
circadian organization. Finally, Part VII on “Circannual Rhythms, Photoperiodism,
and Seasonal Behavior” brings us full circle and addresses biological rhythms that
are synchronized with seasonal cycles driven by the orbit of the earth around the
sun. The rich biology of annual cycles in migration, hibernation, and reproduction
and behaviors associated with these cycles are highlighted, as well as more recent
work on the mechanisms underlying seasonality and circannual rhythms.
In looking back at the modern era of the field of circadian rhythms, first
crystallized at the 1960 Cold Spring Harbor meeting, the field has been revolution-
ized. As described in the opening chapter by Schwartz and Daan, the field, its
phenomena, and its formal properties were conceptualized and codified by Colin
Pittendrigh and Jurgen Aschoff. Initial forays into the genetics of clocks by Ron
Konopka and Seymour Benzer in Drosophila and by Jerry Feldman in Neurospora
heralded the molecular era of clocks that emerged decades later and guides us
today. In a parallel universe (at the time in the 1970s), physiological approaches by
Michael Menaker, Fred Stephan and Irving Zucker, and Robert Moore and Eichler
Victor led to the discovery of the avian pineal gland and the mammalian
suprachiasmatic nucleus as critical anatomical foci for the regulation of organismal
rhythms. Now many decades later, the field is fully integrated with the knowledge
of circadian clock genes, the cell-autonomous mechanisms of clock systems from
cyanobacteria to humans, the multiplicity of clocks throughout the body, and the
intricate and intimate role that clock genes play in all aspects of biology. Today,
clocks equal biology equal life!
In closing, Biological Timekeeping: Clocks, Rhythms, and Behavior is an impor-
tant contribution to the field and will be a valuable resource for students, faculty,
and anyone interested in the biological significance of circadian clocks.

Howard Hughes Medical Institute Joseph S. Takahashi

Department of Neuroscience
University of Texas Southwestern Medical Center
Dallas, TX
USA
Preface

Time is neither an entity nor a process and hence, cannot be measured and defined.
In physical terms, however, the temporal measurement is observed in the form of
the output from a clock – a mechanistic process that progressively counts the
passage of time in seconds, minutes and hours. This in turn provides a calendar,
which is a mathematical abstraction of ‘clock time’ over a longer period, e.g. day,
month or year. In the biological context, time almost serves as the ‘sixth’ sense. All
living beings have the sense of time and use it to sequence and restrict their most, if
not all, biological activities to a specific time during the day and during a season of
the year. Central to this is the evolution of an elaborate timekeeping mechanism(s),
the ‘clock’ that keeps on ‘ticking’ and ‘telling’ an organism with great precision
about the ‘correct’ time of day and time of year. Based on the temporal information
coming out, we designate these clocks as the circadian (circa ¼ about; dian ¼ day),
circannual (circa ¼ about; annum ¼ year), ultradian (shorter than the day) and tidal/
lunar (periods matching the ocean tides and lunar day) clocks. The clock-driven
measurable recurring processes are appropriately called as the circadian,
circannual, ultradian and tidal/lunar rhythms.
Natural selection has operated in such a way that all rhythmic events occur
synchronized (entrained) by external agents in the geophysical environment. In the
natural environment, therefore, the rhythms are exhibited as daily, annual and tidal/
lunar rhythms. The main agents (factors, cues) from the environment that synchro-
nize (entrain) these endogenous rhythms to local time include the daily cycle of
changes in the illumination, temperature, food availability, social factors, etc.
The endogenous timekeeping is achieved through a layered system of the
organization and control, which consists of the molecules, cells, tissues, circuits
and networks. These layers add to the complexity of orchestration of body rhythms
to a concerted action in synchrony with changes in the local environment. Thus,
unless carefully operated in sync with the external world a species or individual
inhabits, there are heightened chances of the disruptions and hence dysfunctions;
anything can go wrong anywhere. The self-sustained and robust timekeeping
mechanisms, therefore, exhibit interesting individual and species between the

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habitats and latitudes, since each individual and species can define its own rela-
tionship with the environment it inhabits.
The time perspective in biology was fully recognized some 50 years ago in a
Cold Spring Harbor symposium. Since then, the study of biological timekeeping –
called chronobiology – has evolved as a truly interdisciplinary science and attained
a global appeal, expanding from the biodiversity, physiology and genetics to health
issues, fitness and survival. Spectacular advances have been made in the field of
chronobiology during the last years, with contributions by some of the best brains
drawn from different disciplines, viz. biology, chemistry, physics and medicine.
Much effort has been directed towards deciphering the clock mechanisms, partic-
ularly the cellular and network interactions within and between individuals as well
as with the environment. In the last decade, there have been significant advances in
our appreciation of the role of clocks in metabolism, sleep, cognition, immune
functions and diseases. Increasingly evident is the application value of the biolog-
ical clock in the human society, especially among the people working at ‘unnatural’
times of day (e.g. shift workers). Intensive research has shown associations of
several chronic disorders and lifestyle-related diseases with disruptions of the
circadian rhythm or the clock networks. No wonder, with outlets open 24  7,
eating at the wrong time or consuming food more than required by frequent eating
can lead to obesity and in turn have consequences on fitness and health. The ever-
growing list of diseases linked with clock disruptions includes obesity, diabetes,
cardiac diseases, depression and cancer. Also, the timing and duration of therapy,
called chronotherapy, have been found critical in determining the efficacy of drugs.
The present book treats the organization and importance of clocks in animals and
humans alike and covers significant aspects of the timekeeping mechanisms in both
the groups. The book attempts at answering questions related to the ecological and
evolutionary implications of the clock. I set out clear goals when I conceived the
idea of bringing out this volume. Besides clearly outlining the history, origin and
basic features of the clock, the book comprehensively includes the organization of
clock system in Drosophila, fish, amphibia, reptile, birds and rodents, to present a
complex and diverse nature of the timekeeping mechanisms among different animal
groups, as this is generally not available in recent volumes on the subject. Secondly,
the book includes topics that characterize rhythms in human and deal with the
potential applications of circadian rhythms to health issues, including the metabo-
lism and immune functions. Thirdly, a few chapters deal with the mechanism(s) of
time generation and synchronization to the environment, both at cellular and
molecular levels. A small section deals with the role of melatonin in regulation of
daily and seasonal functions in animals. Finally, the book details on seasonal
timekeeping mechanisms, with emphasis placed on genetic and epigenetic regula-
tions of physiology and behaviour. Overall, the book tends to cater the needs of
advanced undergraduates, researchers and professionals engaged in the field of
chronobiology. I have avoided duplications or curtailed texts on topics that have
been covered in important books published during the last 10 years, unless a
particular topic was important for the present book and required a fresh look at
this time.
Preface xi

A well-known expert in the area has authored the chapter. When presenting a
state-of-the-art account, the text provides a consistent thematic coverage with
adequate illustrations and feeling of the methods of investigations to arrive at the
statements. The citation of references within the body of the text adequately reflects
the literature as the subject is developed. Full references at the end of each chapter
are useful to a reader interested to go deeper into the subject.
I am grateful to all the authors who have very kindly agreed to be part of this
book. They have been extremely cooperative all the time. However, I am fully
aware that the present volume of Biological Timekeeping: Clocks, Rhythms and
Behaviour by no means can be considered as a full account of the subject. And I am
solely responsible for the sins of omissions and commissions that are inevitable in
an endeavour of this nature.
Undertaking such a mammoth task along with regular teaching, research and
many other responsibilities requires immense goodwill and huge support. I have no
hesitation that a strong team of doctoral and postdoctoral students during more than
three decades of my professional career has made it possible by enabling me to
learn more and find newer ways to overcome the challenges. I have very sincere
words of praise and acknowledgement for all of them. Also, I have excellent friends
both in India and abroad, who have full trust in me and always have encouraged my
academic pursuits. My whole family supports me in whatever I do in the academics,
and I am sure they would derive some satisfaction that their constant support has
allowed me to produce something worthwhile. Finally, Springer (India) Pvt. Ltd., in
particular Dr. Mamta Kapila and her excellent team, deserves special appreciation
for the full support they have extended all along in bringing out the present volume.

Delhi, India Vinod Kumar

Thursday; 28 April 2016
Contents

Part I History, Concepts, Evolution, and Basic Features

of Biological Clock
1 Origins: A Brief Account of the Ancestry of Circadian Biology . . . 3
William J. Schwartz and Serge Daan
2 Interpreting Circadian Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . 23
Dietmar Weinert and James Waterhouse
3 Basic Principles Underlying Biological Oscillations
and Their Entrainment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47
Theresa Floessner and Roelof A. Hut
4 Circadian Waveform and Its Significance for Clock Organization
and Plasticity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 59
Michael R. Gorman, Elizabeth M. Harrison, and Jennifer A. Evans
5 On the Origin and Implications of Circadian Timekeeping:
An Evolutionary Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81
K.L. Nikhil and Vijay Kumar Sharma

Part II Animal Clocks: Complexity and Diversity

6 The Drosophila Clock System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
Charlotte Helfrich-F€orster
7 The Fish Circadian Timing System: The Illuminating
Case of Light-Responsive Peripheral Clocks . . . . . . . . . . . . . . . . . . 177
Cristina Pagano, Rosa Maria Ceinos, Daniela Vallone,
and Nicholas S. Foulkes

xiii
xiv Contents

8 Molecular Genetic and Genomic Analyses of Zebrafish

Circadian Rhythmicity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 193
Zhaomin Zhong, Mingyong Wang, Guodong Huang,
Shuqing Zhang, and Han Wang
9 The Amphibian Clock System . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 211
Massimiliano Andreazzoli and Debora Angeloni
10 The Reptilian Clock System: Circadian Clock, Extraretinal
Photoreception, and Clock-Dependent Celestial Compass
Orientation Mechanisms in Reptiles . . . . . . . . . . . . . . . . . . . . . . . . 223
Cristiano Bertolucci, Elena Frigato, and Augusto Foa
11 Avian Circadian Organization . . . . . . . . . . . . . . . . . . . . . . . . . . . . 241
Vincent M. Cassone, Jiffin K. Paulose, Clifford E. Harpole, Ye Li,
and Melissa Whitfield-Rucker
12 The Mammalian Neural Circadian System: From Molecules
to Behaviour . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
Beatriz Bano-Otalora and Hugh D. Piggins

Part III Human Circadian Rhythms: Entrainment and Sleep

Regulation
13 Circadian Rhythms Versus Daily Patterns
in Human Physiology and Behavior . . . . . . . . . . . . . . . . . . . . . . . . 279
Josiane L. Broussard, Amy C. Reynolds, Christopher M. Depner,
Sally A. Ferguson, Drew Dawson, and Kenneth P. Wright Jr.
14 Light Resetting and Entrainment of Human
Circadian Rhythms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 297
Joshua J. Gooley
15 Delayed Sleep Phase Disorder: Mechanisms and Treatment
Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 315
Jade M. Murray, Tracey L. Sletten, Michelle Magee, and Shantha M.W.
Rajaratnam

Part IV Clock Interactions Within and Between Individual

and the Natural World
16 Interaction Between Central and Peripheral Clocks
in Mammals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 337
Ueli Schibler
17 Circadian Photoentrainment Mechanism in Mammals . . . . . . . . . . 365
Yu Hsin Liu and Satchidananda Panda
Contents xv

18 Mechanisms of Non-photic Entrainment . . . . . . . . . . . . . . . . . . . . . 395

Emma J. Wams, Sjaak J. Riede, Ivor Laan, Tim Bulte,
and Roelof A. Hut
19 Temperature Input for Rhythmic Behaviours in Flies:
The Role of Temperature-Sensitive Ion Channels . . . . . . . . . . . . . . 405
Antara Das and Vasu Sheeba

Part V Circadian Clocks, Metabolism, and Immune Functions

20 Circadian Clocks, Metabolism, and Food-Entrained Rhythms . . . . 427
Rohit Chavan, Urs Albrecht, and Takashi Okabe
21 Circadian Regulation of Metabolism in Health and Diseases . . . . . 443
Breanna Sarkisian, Neelu Jain Gupta, and Satchidananda Panda
22 Circadian Clocks and Immune Functions . . . . . . . . . . . . . . . . . . . . 459
Chloé C. Nobis, Silke Kiessling, Nathalie Labrecque, and Nicolas
Cermakian
23 Clock Genes and Cancer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 481
Silke Kiessling and Nicolas Cermakian

Part VI Pineal, Melatonin, and Biological Timekeeping

24 The Timezyme and Melatonin: Essential Elements
of Vertebrate Timekeeping . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 503
Surajit Ganguly and David C. Klein
25 Pineal Gland, Melatonin, and Timekeeping in Nonmammalian
Vertebrates: Avian Perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . 521
Amit Kumar Trivedi, Devraj Singh, Anand Shankar Dixit,
and Vinod Kumar

Part VII Circannual Rhythms, Photoperiodism,

and Seasonal Behavior
26 Circannual Rhythms Anticipate the Earth’s Annual Periodicity . . . 545
Barbara Helm and Gerald A. Lincoln
27 Seasonal Changes in Brain and Behavior . . . . . . . . . . . . . . . . . . . . 571
Gregory F. Ball, Beau A. Alward, and Jacques Balthazart
28 Molecular Mechanism Regulating Seasonality . . . . . . . . . . . . . . . . 589
Keisuke Ikegami and Takashi Yoshimura
29 Epigenetic Mechanisms Regulating Circannual Rhythms . . . . . . . . 607
Tyler J. Stevenson and Gerald A. Lincoln
xvi Contents

30 Insights into the Regulation of Spring Migration in Songbirds . . . . 625

Sangeeta Rani, Sudhi Singh, Shalie Malik, and Vinod Kumar
31 Orientation in Migrating Animals: Role of Biological Clocks . . . . . 643
Neelu Jain Gupta, Vatsala Dwivedi, Bhanu P. Singh,
and Sanjay K. Bhardwaj

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 659
Contributors

Urs Albrecht University of Fribourg, Fribourg, Switzerland

Beau A. Alward Department of Psychology, University of Maryland, College
Park, MD, USA
Massimiliano Andreazzoli Unita’ di Biologia Cellulare e dello Sviluppo,
Dipartimento di Biologia, Universita’ di Pisa, Pisa, Italy
Debora Angeloni Institute of Life Sciences, Scuola Superiore Sant’Anna, Pisa,
Italy
Gregory F. Ball Department of Psychology, University of Maryland, College
Park, MD, USA
Jacques Balthazart GIGA Neurosciences, University of Liege, Liège, Belgium
Beatriz Bano-Otalora Faculty of Biology, Medicine, and Health, University of
Manchester, Manchester, UK
Cristiano Bertolucci Department of Life Sciences and Biotechnology, University
of Ferrara, Ferrara, Italy
Sanjay K. Bhardwaj Department of Zoology, Chaudhary Charan Singh
University, Meerut, India
Josiane L. Broussard Sleep and Chronobiology Laboratory, Department of
Integrative Physiology, University of Colorado Boulder, Boulder, CO, USA
Vincent M. Cassone Department of Biology, University of Kentucky, Lexington,
KY, USA
Rosa Maria Ceinos Institute of Toxicology and Genetics, Karlsruhe Institute of
Technology, Eggenstein-Leopoldshafen, Germany
Nicolas Cermakian Douglas Mental Health University Institute, McGill
University, Montréal, QC, Canada

xvii