Insect Clocks

D.S. Saunders, C.G.H. Steel X. Vafopoulou, R.D. Lewis

• Publisher: Elsevier Science
• Year: 2002
• ISBN:
  9780080534718
• Topic: Biological Sciences
• Subtopic: Entomology
• Index: Biological Sciences

Chronobiology is the study of timing mechanisms in biological systems as diverse as plants, animals and some micro-organisms. It includes rhythmic phenomena ranging from short period (ultradian) through daily (circadian) to long period (monthly, annual) cycles of behaviour, physiology and biochemistry. In recent years spectacular advances have been made, particularly in the field of circadian rhythms, and hardly a week passes without important papers appearing in the major scientific journals.

The third edition of Insect Clocks, like its predecessors, deals with the properties and functions of clock-like processes in one of the planet's most abundant groups of organisms. The first half of the book is concerned with circadian rhythmicity, the second with annual responses such as over-wintering diapause, seasonal morphs and cold hardiness. Insect Clocks puts modern developments in these fields into a secure framework of the 'classical' literature that has defined the subject.

The book is directed at active researchers in the field as well as newcomers and scientists working in many other areas of modern biology. It will also serve as a textbook for advanced and less advanced students and should find its way into university libraries wishing to keep abreast of the times.

CHAPTER 1

INTRODUCTION: RHYTHMS AND CLOCKS

While the earth remaineth, seedtime and harvest, and cold and heat, and summer and winter, and day and night shall not cease. Genesis 8:22

EVER since life first appeared on this planet it has been subjected to daily cycles of light and dark, and to seasonal cycles of climatic change, caused by the rotation of the earth around its axis and around the sun. Marine and inter-tidal organisms have in addition been subjected to tidal and lunar periodicities. Only those animals that invaded the depths of the ocean, or underground caves and rivers, have avoided this fluctuating environment. Other species - especially those on the land, where daily and seasonal changes may include violent fluctuations in temperature and humidity - have developed strategies to counteract or to exploit this periodicity. The majority of insects, for example, show daily and annual cycles of activity and development. They may be nocturnal, diurnal or crepuscular. They may hibernate or aestivate. Plants may produce leaves or flowers only at certain seasons, and flowers may open and close at particular times of the day.

Some of these phenomena are direct responses to environmental changes, but many more are overt manifestations of an endogenous periodicity. These innate rhythms must have astounded early workers such as the French astronomer De Mairan who discovered (in 1729) that the daily leaf movements of Mimosa would persist in constant darkness. The oscillations underlying such phenomena are now known to provide a temporal organisation for physiological and behavioural activities in practically every group of organisms, including prokaryotes such as some blue-green ‘algae’ (see Johnson et al. 1998). Of particular interest are those endogenous oscillations that evolved with a periodicity close to 24 hours (circadian rhythms). These are used by animals and plants to ‘time’ daily events and thus allow the organism to perform functions at the ‘right time of the day’, or to attain synchrony with other individuals of the population. It is clear that these circadian oscillations in the cell and the organism have evolved to match almost exactly the oscillations in the physical environment. In the fruit fly Drosophila melanogaster the circadian period is inherited and important advances have been made in understanding the genetics and molecular biology of these rhythms (Chapter 4). These rhythms, therefore, are not ‘imposed’ on the organism by the environment, neither are they ‘learned’; they are part of the genome and a product of evolution. The natural cycles of light and temperature, however, do serve to entrain and phase-control these endogenous oscillators so that under natural conditions their periods become exactly 24 hours and the overt events they control achieve a particular phase relationship to the environmental periodicity. In the absence of temporal cues from the environment (i.e. in darkness and constant temperature) the rhythms ‘free-run’ and reveal their own natural period (τ) which is close to, but significantly different from that of the solar day. The observation that this period is temperature-compensated, and that the rhythms are used by the organisms to measure the passage of time (Pittendrigh, 1954, 1960), justifies the use of the term ‘biological clock’.

Apart from circadian rhythms which have evolved as a match to the 24-hour periodicity of the earth’s rotation around its axis, endogenous oscillations with tidal (-12.4 hours), semilunar (-14.7 days), lunar (-29.4 days) or annual (∼a year) periods are also to be found in organisms, including the insects. In many cases the endogenous nature of these rhythms has been demonstrated by allowing them to ‘free-run’ in the absence of the environmental cues (Zeitgeber) which normally entrain them.

The brief account of these biological oscillations given above - and the more extensive description of their properties given later in this book - amply demonstrate their endogenous nature. They are, in fact, every bit a part of the organism as its morphological organisation. Some investigators, however - principally Brown (1960, 1965) - at one time held an alternative view, namely that all of the observed periodicities were in some way exogenously controlled by “subtle geophysical forces” associated with the solar day. These ‘forces’ were thought to include air pressure, periodic fluctuations in gravity associated with the earth’s rotation in relation to the sun and the moon, or cosmic ray intensity - which remained unaccounted for in laboratory experiments in which the obvious periodicities (light, temperature, etc.) had been eliminated. This view will receive no further attention in this book. As a partial answer to the endogenous-exogenous controversy, Hamner et al. (1962) maintained a number of organisms at the South Pole on a turntable arranged to rotate once every 24 hours counter to the earth’s own rotation, thereby eliminating most diurnal variables. Under these conditions several rhythmic systems, including the pupal eclosion rhythm in Drosophila pseudoobscura (Chapter 3), continued to show a circadian periodicity apparently unaffected by either their location at the South Pole or by their rotation on the turntable. Therefore, as far as these experiments or their results allow, the data support the endogenous hypothesis.

Using the clock analogy for these biological rhythms there is an interesting parallel between the development of man-made ‘time-pieces’ and those ‘clocks’ found in nature. Early man was aware of the passage of time by watching the movement of the sun, moon, and stars, or by observing the movement of the sun’s shadow on the ground or on a dial. Such methods, of course, have nothing to do with clocks. Neither have the direct responses of animals and plants to daily periodicities. These exogenous effects are widespread in nature and in some animals the observed rhythm of activity appears to be related, at least in part, to the immediate effects of the daily changes in light intensity. Under field conditions most daily rhythms -although innate - are nearly always strongly modulated by the immediate character of the environment, particularly the rapid changes in light intensity at dawn and dusk. These ‘masking’ effects will be discussed only where they modify an endogenous periodicity.

The first man-made time-measuring devices were probably sand-glasses, clepsydras (water clocks) and candles. These ‘clocks’ did not oscillate and had to be reset or ‘turned over’ once all the water or sand had run out, or the candle burnt to the bottom. This type of device finds its equivalent in some of the ‘hourglass’-like timers thought to perform night-length measurement in some insects which, after measuring the duration of the dark period, require to be ‘turned over’ by light before they can function again (see Chapter 11).

Mechanical clocks introduced in the fourteenth and fifteenth centuries were either weight-driven or spring-driven and incorporated oscillatory devices that ran continuously so long as the weight was raised or the spring wound up. These find their counterpart in the free-running biological oscillations mentioned above. The escapement in these early clocks consisted of a crown wheel and a verge and foliot. The system was not isochronous and the clocks so constructed tended to lose or gain up to 15 minutes every day. In the seventeenth century the incorporation of a pendulum with an escapement to maintain constant amplitude introduced isochrony to the clock, and brought the error down to about 10 seconds per day. This pendulum analogy and sine-wave representation of the oscillation’s time course remain instructive and useful in model building.

For really accurate time measurement temperature-compensation is required. In man-made clocks an uncompensated pendulum lengthens as the temperature rises and therefore swings more slowly. By the eighteenth century George Graham had compensated for temperature changes by using a mercury-vial pendulum. When the quantity of mercury was correctly adjusted its thermal expansion raised the centre of gravity to compensate for the lengthening of the pendulum rod. Graham’s clock varied by as little as one second per day; Harrison’s grid-iron pendulum, which operated on a similar principle, later cut this error down to less than one second. In biological systems most physiological processes more than double their rate with every 10°C rise in temperature, and such temperature effects would render time measurement impossible. However, during evolution this challenge has been met: most biological oscillators with a ‘clock’ function have a temperature co-efficient (Q₁₀) between 0.85 and 1.1. This property is an absolute functional prerequisite for a clock mechanism. It is also essential for effective entrainment by a natural (24 hour) Zeitgeber because if the oscillator had a Q₁₀ of 2.0 or more it would, at some temperatures, fall outside the limits within which the light-cycle could hold it. The manner in which temperature-compensation is achieved in biological clocks, however, remains obscure (see Chapters 4 and 16).

Defining properties of a biological clock are therefore as follows. (1) They show an overt rhythm, driven by oscillators that persist (‘free-run’) in the absence of environmental signals (thereby attesting to their endogeneity). (2) The free-running rhythm (period τ) is close, but rarely equal to, the environmental periodicity it has evolved to match. (3) The endogenous period shows a well-defined homeostasis when exposed to a wide range of physical, chemical and biological variables, most notably temperature (i.e. the period is temperature compensated). And (4) the ability to synchronise (entrain) to environmental variables so that τ becomes equal to the period of the entraining agent (Zeitgeber), and adopts an adaptive phase relationship to it. These properties are all shown by circadian, circatidal, circa-semilunar, circalunar and circannual rhythms. In addition, some ultradian (short period) rhythms, whilst lacking properties (2) and (4), are nevertheless free-running and temperature compensated. For these reasons they may operate as biological clocks providing temporal organisation within the cell or for some behavioural functions.

In man-made clocks hourglasses clearly antedate oscillators, but the reverse may be the case in biological systems. Pittendrigh (1966) suspected that circadian oscillations - which occur in all eukaryotes (and some prokaryotes) – possessing the common but seemingly ‘improbable’ properties of accuracy and temperature-compensation are monophyletic in origin and therefore very ancient. Although their original functional significance is unclear, they are now widely used for the purposes of chronometry. In many species of animals and plants the circadian system may also be causally involved in the measurement of day- or night-length, or ‘classical’ photoperiodism. In some insects, on the other hand, this function may be performed by means of an ‘hourglass’ rather than by circadian oscillations - which they surely must possess. Evidence for an evolutionary convergence such as this suggests that the adoption of hourglass-like timers for photoperiodic time measurement is a comparatively recent event. It is suggested here (see Chapter 11) that hourglass-like timers may be heavily damped circadian oscillators.

Many aspects of insect physiology and behaviour are clock-controlled. There are, for example, daily rhythms of general locomotion, feeding, mating, oviposition, pupation, and pupal eclosion, in which these activities are restricted to a particular part of the day or night. Photoperiodism also involves a clock measuring day- or night-length, the most frequent response being the seasonal appearance of a dormant stage (diapause) in the life cycle. The adaptive significance of diapause is clear, but it is not always easy to see the adaptive significance of daily rhythms, and in the absence of concrete experimental evidence most conclusions must remain conjectural. However, adults of Drosophila pseudoobscura emerge from their puparia close to dawn when the relative humidity of the air is at its height, and it is known that success in the act of eclosion is greatest under these conditions (Pittendrigh, 1958). Cycles of feeding may be correlated with the supply of food: the classical example of this is probably the ‘time-memory’ (Zeitgedächtnis) of bees. Bees can be ‘trained’ to visit a food source at a particular time of the day (Beling, 1929), this mechanism ensuring that they visit nectar sources every day at the same time. The significance of this behaviour lies in the observation that not only do flowers open and close at particular hours, but that nectar production is also a circadian event (Kleber, 1935). In many cases the selective advantage of an event being clock-controlled lies in the synchrony attained between individuals of the population. Mating rhythms of certain Diptera, for example, ensure that all sexually active individuals in the population are looking for mates at the same time and thereby increase the likelihood of successful encounters between the sexes. Conversely, differences in mating times between closely related species are known to provide effective mechanisms for genetic isolation (Tychsen and Fletcher, 1971).

Biological clocks have been classified in a number of ways. Pittendrigh (1958) differentiated (1) ‘pure’ rhythms, such as colour change in the crab Uca pugnax (Brown et al., 1953), from (2) ‘interval timers’, in which a particular event such as pupal eclosion occurs at a particular time of the day, and (3) ‘continuously consulted’ clocks such as the bees’ Zeitgedächtnis and time-compensated sun orientation in which time may be ‘recognised’ at any time of the day. Lees (1960a) used the term interval timer to describe some of the non-oscillatory hourglass-like timing devices in aphids. In a later paper Truman (1971d) proposed that animal clocks fall into two well-defined groups. In Type I, such as the rhythm of pupal eclosion in Drosophila spp. (Pittendrigh, 1966) and Antheraea pernyi (Truman, 1971a), the compound eyes (or other ‘organised’ photoreceptors) are not essential for entrainment, the relevant photoreceptors lying in the brain itself. These rhythms also damp out in continuous light of moderate intensity, and the magnitude of the phase-shifts generated by quite short light perturbations may be in the order of 10 hours or more (for D. pseudoobscura). These clocks are generally associated with developmental rhythms such as hatching, moulting, eclosion or release of brain hormones. Truman also placed ph...

Table of contents

• Cover image
• Title page
• Table of Contents
• Copyright
• Dedication
• PREFACE
• GLOSSARY AND LIST OF SYMBOLS
• Chapter 1: INTRODUCTION: RHYTHMS AND CLOCKS
• Chapter 2: CIRCADIAN RHYTHMS OF ACTIVITY IN INDIVIDUAL INSECTS
• Chapter 3: CIRCADIAN RHYTHMS OF ACTIVITY IN POPULATIONS OF INSECTS
• Chapter 4: CIRCADIAN RHYTHMS: GENES AND THE FEEDBACK LOOP
• Chapter 5: PHYSIOLOGY OF CIRCADIAN SYSTEMS
• Chapter 6: THE MULTIOSCILLATOR CIRCADIAN SYSTEM
• Chapter 7: QUANTITATIVE MODELS FOR INSECT CLOCKS
• Chapter 8: CIRCADIAN RHYTHMS: PHOTORECEPTOR AND CLOCK LOCATION
• Chapter 9: PHOTOPERIODISM AND SEASONAL CYCLES OF DEVELOPMENT
• Chapter 10: THE PHOTOPERIODIC RESPONSE
• Chapter 11: CIRCADIAN RHYTHMS IN PHOTOPERIODISM
• Chapter 12: THE PHOTOPERIODIC COUNTER
• Chapter 13: PHOTOPERIODIC TIME MEASUREMENT: THE CLOCK-COUNTER MECHANISM
• Chapter 14: PHOTOPERIODIC PHOTORECEPTORS AND CLOCK LOCATION
• Chapter 15: OTHER TYPES OF INSECT CLOCKS
• Chapter 16: CLOCK COMPLEXITY: THE WAY FORWARD?
• References
• INDEX