The fact that diapause is programmed well in advance of its onset enables the insect to take preparative steps supporting its upcoming period of developmental arrest. Such steps frequently include modifications in the rate of pre-diapause development (most commonly a prolongation but sometimes an acceleration in development), acquisition of additional energy reserves (usually in the form of lipids), local or distant migration to overwintering sites, selection of a suitable microenvironment for spending the months of diapause, enhancement of the refuge (additional waterproofing, etc.), formation of aggregations, adjusting color to blend with the diapause environment, and making structural modifications (e.g., short- vs. long-winged forms), and, as seen in aphids, switching reproductive modes from parthenogenesis to sexual reproduction. These sorts of pervasive changes that occur even before diapause begin to underscore the idea that diapause is most appropriately viewed as an alternative life cycle, impacting more than just the diapause state.

The diapause response displays rich variability, both within populations as well as between populations, variation that provides the grist for rapid shifts in the diapause response as insects invade new territories or respond to climate change. Variation is evident for not only the decision to enter diapause but also for the timing of its onset and termination. Even progeny from a single egg clutch shows variation in their diapause response. Other variations in the response are noted in few insects that enter and exit diapause repeatedly and among species that exhibit a prolonged diapause that persists for more than 1 year. Prolonged diapause is energetically costly but serves as an important bet-hedging strategy for insects inhabiting an unpredictable environment.

Three questions are addressed here. How did diapause arise? How did evolution shape the diapause response in time and space? And, how did diapause impact evolution of insect sociality? Insect development is a progression of starts and stops. This sets the stage for exploiting the stop points for insertion of a period of developmental arrest. Integration of a photoperiodic clock mechanism with developmental regulation likely leads to the precise developmental timing that is essential for diapause. Though the diapause phenotype is shared among diverse species, the same endpoint (diapause) can be attained using different molecular tools, suggesting that insect diapause has arisen numerous times in evolutionary history. Responses along latitudinal clines and to climate change underscore the rapidity of evolutionary change that is possible. Mounting evidence supports the idea that adult diapause may have been crucial for the evolution of sociality in wasps and related Hymenoptera.

The huge geographic variation in diapause suggests it has an underlying genetic basis, a feature further revealed by selection experiments that are successful in both increasing and decreasing the diapause incidence as well as modifying other attributes of diapause. Genetic crosses between lines with different diapause characteristics reveal diverse inheritance patterns. While some such crosses reflect a simple Mendelian-type pattern, polygenic inheritance patterns are more commonly revealed. Examples of dominance and incomplete dominance abound and a few examples can be found showing diapause traits linked to recessive alleles. Likewise, both sex-linkage and autosomal inheritance are noted in some examples. Mapping quantitative trait loci is a powerful technique for identifying single nucleotide polymorphisms associated with diapause. Results of such analyses elegantly demonstrate the complexity of the diapause response as well as the large number of chromosomal sites that have both major and minor impacts on diapause.

This chapter identifies seasons that are avoided by entry into diapause. The best documented studies on diapause examine overwintering in temperate latitudes. Most overwintering insects enter diapause in early autumn in response to the shortening daylengths that reliably foretell the advent of winter. But summer diapauses are also quite common, especially as a mechanism for synchronizing activity with seasonally restricted food sources. Daylength may regulate summer diapause, but instead of short days, the long days of early summer frequently are used to program such a diapause. Diapause is also widespread among tropical species, especially for bridging dry seasons. Near the equator, the role of daylength may be replaced by cues provided by host plants, moisture levels, or temperature changes. Insects living at high latitudes also rely on diapause, but the fact that multiple years may be required to complete development means that diapause may intercede several times during the life cycle.

Hormones and downstream components of molecular signaling pathways that dictate entry and exit from diapause vary depending on the stage of diapause. Diapause hormone, a neuropeptide, directs entry into embryonic diapause in the silk moth, but embryonic diapauses in other species appear to be regulated by ecdysteroids or juvenile hormones. Larval and pupal diapauses are commonly initiated by a shutdown in the brain-prothoracic gland axis, reflected in failure of the prothoracic gland to produce ecdysone. Adult diapauses commonly are prompted by a failure of the corpora allata to produce the juvenile hormone needed for reproduction. Insulin signaling is central to diapause, and transcription factors such as FoxO provide a pathway to explain how a single hormone response can lead to the multiple downstream effects elicited by the diapause program. Organ cross talk, epigenetics, and small noncoding RNAs have emerged more recently as important new dimensions in the regulatory scheme of diapause.

Diapause offers the obvious benefit of enabling an insect to survive seasons that would otherwise be unsuitable for continuous development, but it usually comes at a cost. Costs may be reflected during the insect’s life or as reduced fitness in the progeny. Costs can include high mortality, depletion of energy reserves, low fecundity, delay in oviposition, shortened post-diapause longevity, and missed opportunities as a consequence of lost generations. Costs may differ between males and females, resulting in sex-specific trade-offs that may influence the timing of diapause entry. A few species, however, appear to have escaped obvious costs associated with diapause. Alternatives enable some insects to survive without diapause. These include entering quiescence (a dormant state readily entered and exited in direct response to prevailing conditions), cold hardening without diapause, extending the life cycle without diapause, seeking a favorable environment, and remaining winter-active.

Our highly seasonal world imposes environmental challenges for insects. To survive these inimical periods they rely on a diapause (dormancy) mechanism to bridge unfavorable seasons. The origin of the term “diapause” is discussed, as well as its relationship to related forms of dormancy in other animals. Diapause is distinct from quiescence in that it is not an immediate response to an adverse environment but is programmed at an earlier developmental stage, an attribute that enables the insect to take steps in preparation for entering the arrested state. Diapause can occur at any point in the life cycle (embryo, larva, pupa, adult), but when it occurs it is species-specific. The chapter summarizes who does it and in what stage, as well as addressing the occurrence of diapause in social insects. The pervasive impact of diapause on the insect life cycle begins prior to diapause and continues well beyond its termination.

To use information inherent in the seasonal change in daylength, an insect must be able to measure daylength, distinguish long from short days, count the days, store that information in the brain, and then act on that information at the correct developmental stage to engage the diapause program. This chapter explains the nature of the photoperiodic signal, when it is received, where this information is stored, and how that information triggers the hormonal response. Formal models and molecular approaches examining the role of circadian clock genes consistently point to a circadian basis for the photoperiodic clock. Thermoperiod sometimes substitutes for photoperiod, suggesting alternative pathways for evoking the diapause program. Some tropical insects rely exclusively on temperature or rainfall as environmental signal regulating diapause. Input from hosts can also be important for plant-feeders and parasitoids. The diapause decision is sometimes relegated to the mother, thus requiring an intriguing mechanism for the transfer of environmental information across generations.

Correctly timing the break of diapause and reactivation of development is critical for synchronizing the insect with its food source as well as optimizing mating opportunities. In many cases, diapause is actually broken (i.e., the insect is capable of developing) in early winter, but the progression of development is suppressed by the prevailing low temperatures. This post-diapause quiescence is followed by resumption of development when temperatures rise above a developmental threshold in the spring. This mechanism allows insects that have entered diapause at different times to be stockpiled in post-diapause quiescence and then develop synchronously in the spring. Alterations in the timing of spring development have led to host plant specialization and speciation. Several environmental factors, including chilling, daylength, rainfall patterns, and food availability, exert an influence on diapause duration, and an internal energy-sensing mechanism plays a key role in monitoring levels of energy reserves available to the insect.

Understanding diapause is vital for the development of sound insect pest management practices, including population modeling as well as the implementation of effective cultural measures. Tools for breaking or promoting diapause on demand have utility for managing domesticated species, for mass rearing of insects for sterile insect release, and for stockpiling valuable genetic lines or parasitoids used in the biological control industry. A wide range of chemical and physical manipulators of diapause are known, many of which are species-specific. Insect conservation can be promoted by first knowing where insects overwinter and then protecting such sites. Diapause has implications for transmission of human disease, as noted in mosquitoes that harbor viruses while in diapause, thus enabling the disease to become re-established the following summer. Diapause also offers rich potential as a model for exploring issues of human health, such as aging, obesity, and ischemia, as well as providing a rich resource for pharmacological prospecting.

Diverse physiological features characterize the diapause state. Development is halted or dramatically retarded, the cell cycle is arrested, metabolic rates are suppressed, and a global metabolic shift from aerobic to anaerobic metabolism is evident. Energy reserves and body water are usually not replenished during diapause, thus conservation of these resources is essential. Patterns of heartbeat and discontinuous gas exchange are distinct during diapause. Structural modifications such as flight muscle degeneration in adults and cytoskeletal distinctions are evident at both tissue and transcriptomic levels. Defense responses are usually bolstered. Heat shock proteins are commonly upregulated, as are immune and antioxidant responses, as well as cold-hardening mechanisms and hypoxia responses essential for surviving in winter habitats that are oxygen-limited. Diapause is not static, as evidenced by systematic shifts in metabolism and energy sources tapped at different phases of diapause, as well as changes in responsiveness to exogenous hormones or environmental stress.