Chapter 1 - Social Influences on Circadian Rhythms and Sleep in Insects

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Abstract

The diverse social lifestyle and the small and accessible nervous system of insects make them valuable for research on the adaptive value and the organization principles of circadian rhythms and sleep. We focus on two complementary model insects, the fruit fly Drosophila melanogaster, which is amenable to extensive transgenic manipulations, and the honey bee Apis mellifera, which has rich and well-studied social behaviors. Social entrainment of activity rhythms (social synchronization) has been studied in many animals. Social time givers appear to be specifically important in dark cavity-dwelling social animals, but here there are no other clear relationships between the degree of sociality and the effectiveness of social entrainment. The olfactory system is important for social entrainment in insects. Little is known, however, about the molecular and neuronal pathways linking olfactory neurons to the central clock. In the honey bee, the expression, phase, and development of circadian rhythms are socially regulated, apparently by different signals. Peripheral clocks regulating pheromone synthesis and the olfactory system have been implicated in social influences on circadian rhythms in the fruit fly. An enriched social environment increases the total amount of sleep in both fruit flies and honey bees. In fruit flies, these changes have been linked to molecular and neuronal processes involved in learning, memory, and synaptic plasticity. The studies on insects suggest that social influences on the clock are richer than previously appreciated and have led to important breakthroughs in our understanding of the mechanisms underlying social influences on sleep and circadian rhythms.

Introduction

The social environment, which we define as the sum of social interactions, cues, and signals encountered by an animal, has a profound influence on its development, physiology, and behavior. In the current review, we focus on the influences of the social environment on two fundamental biological systems, circadian rhythms and sleep, in insects. Circadian rhythms are biological rhythms that cycle with a daily period of roughly 24 h (see Section II). Sleep is a complex behavioral state that is characterized by reduced activity and responsiveness (see Section IV). These two systems interact in various ways. For example, the circadian clock influences the timing of sleep and wakefulness, and clock genes are implicated in the regulation of different aspects of sleep, such as sleep quality and homeostasis (Andretic et al., 2005, Sehgal and Mignot, 2011). Circadian rhythms and sleep are sensitive to environmental variables such as light and temperature (for a recent review see Peschel and Helfrich-Forster, 2011). There is also evidence that circadian rhythms and sleep are influenced by the social environment, but little is known about the functional significance or the mechanisms underlying these interactions (Davidson and Menaker, 2003, Mistlberger and Skene, 2004). Insects provide an excellent system for addressing these questions because their nervous system is relatively small and accessible. Insects are very diverse in terms of their activity phase and include species that are diurnal, nocturnal, or crepuscular, as well as those that can switch between these states or be active with no circadian rhythms. Importantly, insects show a broad range of social lifestyles, ranging from solitary to highly structured societies.

Highly eusocial insects such as ants, honey bees, and termites are characterized by the restriction of reproduction to a single or a few individuals (e.g., queens), by the fact that individuals from older generations cooperatively care for the young, and by an elaborate communication system (Wilson, 1971). The social environment influences almost every facet of the life of highly social insects, including their patterns of activity and sleep (see below). The social environment is also important for many animals living in simple societies, and for solitary animals as well. The social environment of these animals may include interactions with potential mates, offspring, or conspecifics with which they compete for resources such as territory, shelter, or mates. We focus mainly on the highly social honey bee and the fruit fly, which is commonly considered solitary or facultatively gregarious. The honey bee provides an excellent model for identifying and studying the social signals influencing circadian rhythms and sleep in an ecological context. The arsenal of genetic and transgenic toolkits available for Drosophila make it an excellent model for studying the molecular mechanisms underlying the interaction between social factors and the circadian and sleep systems.

Section snippets

The Circadian System of Insects

Circadian rhythms are defined as biological rhythms that meet the following three criteria: (1) they persist, or “free-run,” with a period of about 24 h in the absence of external time cues, (2) they are reset, or entrained, by environmental cues, in particular, light and temperature, and (3) they exhibit “temperature compensation”; in other words, their period length is stable over a wide range of physiological temperatures. The circadian clock influences many physiological and behavioral

Social Influences on Circadian Rhythms in Insects

The social environment of insects consists of conspecific individuals at all life stages (i.e., eggs, larvae, pupae, and adults), which they may contact directly or indirectly by sensing cues and signals they release to the environment (such as volatile pheromones or acoustic signals). Such social factors in the environment may influence the phase (entrainment), strength, expression, or development of circadian rhythms.

Sleep

Sleep is a fundamental and evolutionarily conserved biological phenomenon. Sleep research has traditionally focused on humans and other mammals, and it was commonly believed that invertebrates do not sleep in the strict sense. This view has been revised dramatically over the past two decades during which sleep-like states have been described for diverse nonmammalian species, including fish (Prober et al., 2006), insects (Hendricks et al., 2000, Kaiser and Steiner-Kaiser, 1983, Tobler, 1983),

Social Influences on Sleep in Insects

The influences of the social environment on sleep were recently reviewed in depth by Donlea and Shaw (2009) and are therefore only briefly summarized here. Drosophila flies and other animals experiencing enriched social environments typically show an increase in the total amount of sleep (Bushey et al., 2011, Donlea et al., 2009, Donlea and Shaw, 2009, Donlea et al., 2011, Ganguly-Fitzgerald et al., 2006). For example, flies that were placed with ∼ 40 siblings for 5 days slept for approximately

Conclusions

Research on social influence on circadian rhythms has traditionally focused on social entrainment in mammals. Our review shows that social influences on the circadian system are richer than being merely entrainment of the phase of activity. For example, in honey bees, social signals not only convincingly entrain circadian rhythms, but also influence their development and context-dependent expression. These influences on the clock appear to be functionally significant. Plasticity in circadian

Acknowledgments

Research in the authors’ laboratory was supported by grants from the Israeli Science Foundation (ISF), US-Israel Binational Foundation (BSF), German-Israeli Foundation (GIF), the National Institute for Psychobiology in Israel (NIPI), the US-Israel Binational Agricultural Research and Development Fund (BARD), and the Joseph H. and Belle R. Braun Senior Lectureship in Life Sciences. The authors thank two anonymous reviewers for their excellent comments on an earlier version of this chapter.

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    Current address: Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, California, USA

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