Chapter 1 - Social Influences on Circadian Rhythms and Sleep in Insects
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.
References (133)
- et al.
Unearthing the phylogenetic roots of sleep
Curr. Biol.
(2008) - et al.
Learning and sleep: The sequential hypothesis
Sleep Med. Rev.
(2001) - et al.
Dopaminergic modulation of arousal in Drosophila
Curr. Biol.
(2005) - et al.
Regulation of copulation duration by period and timeless in Drosophila melanogaster
Curr. Biol.
(2004) - et al.
period expression in the honey bee brain is developmentally regulated and not affected by light, flight experience, or colony type
Insect Biochem. Mol. Biol.
(2004) - et al.
Behaviorally induced synaptogenesis and dendritic growth in the hippocampal region following transient global cerebral ischemia are accompanied by improvement in spatial learning
Exp. Neurol.
(2006) - et al.
Regulation of gustatory physiology and appetitive behavior by the Drosophila circadian clock
Curr. Biol.
(2010) - et al.
Birds of a feather clock together—Sometimes: Social synchronization of circadian rhythms
Curr. Opin. Neurobiol.
(2003) - et al.
Sleeping together: Using social interactions to understand the role of sleep in plasticity
Adv. Genet.
(2009) - et al.
Nocturnal male sex drive in Drosophila
Curr. Biol.
(2007)
Sex differences and effects of social cues on daily rhythms following phase advances in Octodon degus
Physiol. Behav.
Sleep and the fruit fly
Trends Neurosci.
Rest in Drosophila is a sleep-like state
Neuron
Clock genes period and timeless are rhythmically expressed in brains of newly hatched, photosensitive larvae of the fly, Sarcophaga crassipalpis
J. Insect Physiol.
Social experience modifies pheromone expression and mating behavior in male Drosophila melanogaster
Curr. Biol.
Honey bee circadian clocks: Behavioral control from individual workers to whole-colony rhythms
J. Insect Physiol.
Organization of the Drosophila circadian control circuit
Curr. Biol.
Electrophysiological correlates of rest and activity in Drosophila melanogaster
Curr. Biol.
Setting the clock—By nature: Circadian rhythm in the fruitfly Drosophila melanogaster
FEBS Lett.
Social contact synchronizes free-running activity rhythms of diurnal palm squirrels
Physiol. Behav.
Circadian rhythms from multiple oscillators: Lessons from diverse organisms
Nat. Rev. Genet.
Plasticity in the circadian clock and the temporal organization of insect societies
The social clock of the honeybee
J. Biol. Rhythms
Influences of octopamine and juvenile hormone on locomotor behavior and period gene expression in the honeybee, Apis mellifera
J. Comp. Physiol. A
Chronobiology—Reversal of honeybee behavioural rhythms
Nature
Behavioral rhythmicity, age, division of labor and period expression in the honey bee brain
J. Biol. Rhythms
Patterns of PERIOD and pigment-dispersing hormone immunoreactivity in the brain of the European honeybee (Apis mellifera): Age- and time-related plasticity
J. Comp. Neurol.
Sleep and synaptic homeostasis: Structural evidence in Drosophila
Science
Ontogeny of orientation flight in the honeybee revealed by harmonic radar
Nature
The genetic and molecular regulation of sleep: From fruit flies to humans
Nat. Rev. Neurosci.
Is sleep essential?
PLoS Biol.
Molecular correlates of long-term sleep deprivation in rats: A genome-wide analysis
Sleep
Diurnal behavioural differences in forager and nurse honey bees (Apis mellifera carnica Pollm)
Apidologie
Genetic analysis of sleep
Genes Dev.
How sleep affects the developmental learning of bird song
Nature
Use-dependent plasticity in clock neurons regulates sleep need in Drosophila
Science
Inducing sleep by remote control facilitates memory consolidation in Drosophila
Science
Chronobiology: Biological Timekeeping
Differences in the sleep architecture of forager and young honeybees (Apis mellifera)
J. Exp. Biol.
Circadain rhythms and sleep in honey bees
Maternity-related plasticity in circadian rhythms of bumble-bee queens
Proc. R. Soc. Lond. Biol. Sci.
Light and social effects on the free-running circadian activity rhythm in common marmosets (Callithrix jacchus; primates): social masking, pseudo-splitting, and relative coordination)
Behav. Ecol. Sociobiol.
Circadian rhythms in honeybees: Entrainment by feeding cycles
Physiol. Entomol.
Social synchronization of the activity rhythms of honeybees within a colony
Behav. Ecol. Sociobiol.
Ventral lateral and DN1 clock neurons mediate distinct properties of male sex drive rhythm in Drosophila
Proc. Natl. Acad. Sci. U.S.A.
Waking experience affects sleep need in Drosophila
Science
Lack of social entrainment of circadian activity rhythms in the solitary golden hamster and in the highly social Mongolian gerbil
Biol. Rhythm Res.
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Current address: Department of Psychiatry and Behavioral Sciences, Stanford University, Stanford, California, USA