In animal
dormancy
Dormancy is a period in an organism's Biological life cycle, life cycle when growth, development, and (in animals) physical activity are temporarily stopped. This minimizes metabolism, metabolic activity and therefore helps an organism to conserv ...
, diapause is the delay in development in response to regular and recurring periods of adverse environmental conditions.
[Tauber, M.J., Tauber, C.A., Masaki, S. (1986) ''Seasonal Adaptations of Insects''. Oxford University Press] It is a
physiological
Physiology (; ) is the science, scientific study of function (biology), functions and mechanism (biology), mechanisms in a life, living system. As a branches of science, subdiscipline of biology, physiology focuses on how organisms, organ syst ...
state with very specific initiating and inhibiting conditions. The mechanism is a means of surviving predictable, unfavorable environmental conditions, such as temperature extremes, drought, or reduced food availability. Diapause is observed in all the life stages of
arthropod
Arthropods ( ) are invertebrates in the phylum Arthropoda. They possess an arthropod exoskeleton, exoskeleton with a cuticle made of chitin, often Mineralization (biology), mineralised with calcium carbonate, a body with differentiated (Metam ...
s, especially
insect
Insects (from Latin ') are Hexapoda, hexapod invertebrates of the class (biology), class Insecta. They are the largest group within the arthropod phylum. Insects have a chitinous exoskeleton, a three-part body (Insect morphology#Head, head, ...
s.
Activity levels of diapausing stages can vary considerably among species. Diapause may occur in a completely immobile stage, such as the
pupae and eggs, or it may occur in very active stages that undergo extensive migrations, such as the adult
monarch butterfly
The monarch butterfly or simply monarch (''Danaus plexippus'') is a milkweed butterfly (subfamily Danainae) in the family Nymphalidae. Other common names, depending on region, include milkweed, common tiger, wanderer, and black-veined brown. I ...
, ''Danaus plexippus''. In cases where the insect remains active, feeding is reduced and reproductive development is slowed or halted.
Embryonic diapause
Embryonic diapause (delayed implantation in mammals) is a reproductive strategy used by a number of animal species across different biological classes. In more than 130 types of mammals where this takes place, the process occurs at the blastocys ...
, a somewhat similar phenomenon, occurs in over 130 species of mammals, possibly even in humans, and in the
embryo
An embryo ( ) is the initial stage of development for a multicellular organism. In organisms that reproduce sexually, embryonic development is the part of the life cycle that begins just after fertilization of the female egg cell by the male sp ...
s of many of the
oviparous
Oviparous animals are animals that reproduce by depositing fertilized zygotes outside the body (i.e., by laying or spawning) in metabolically independent incubation organs known as eggs, which nurture the embryo into moving offsprings kno ...
species
A species () is often defined as the largest group of organisms in which any two individuals of the appropriate sexes or mating types can produce fertile offspring, typically by sexual reproduction. It is the basic unit of Taxonomy (biology), ...
of fish in the order
Cyprinodontiformes.
Phases of insect diapause
Diapause in insects is a dynamic process consisting of several distinct phases. While diapause varies considerably from one
taxon
In biology, a taxon (back-formation from ''taxonomy''; : taxa) is a group of one or more populations of an organism or organisms seen by taxonomists to form a unit. Although neither is required, a taxon is usually known by a particular name and ...
of insects to another, these phases can be characterized by particular sets of metabolic processes and responsiveness of the insect to certain environmental stimuli.
For example, ''
Sepsis cynipsea'' flies primarily use temperature to determine when to enter diapause. Similarly, ''
Chrysoperla plorabunda'' lacewings regulate their reproductive cycle using daylight length, with adults entering reproductive diapause when there are less than 12-13 hours of daylight. Diapause can occur during any stage of development in arthropods, but each species exhibits diapause in specific phases of development. Reduced oxygen consumption is typical as is reduced movement and feeding. In ''
Polistes exclamans'', a social wasp, only the queen is said to be able to undergo diapause.
Comparison of diapause periods
The sensitive stage is the period when stimulus must occur to trigger diapause in the organism. Examples of sensitive stage/diapause periods in various insects:
[The Insects; Structure and Function, 4th Edition. R.F. Chapman, Cambridge University Press, 1998. , p 404.]
Induction
The induction phase occurs at a genetically predetermined stage of life, and occurs well in advance of the environmental stress.
This sensitive stage may occur within the lifetime of the diapausing individual, or in preceding generations, particularly in egg diapause.
[Huffaker, C.B. and Gutierrez, A.P., Eds. 1999. Ecological Entomology. John Wiley & Sons, Inc.] During this phase, insects are responsive to external cues called token stimuli, which trigger the switch from direct development pathways to diapause pathways. Token stimuli can consist of changes in
photoperiod,
thermoperiod, or
allelochemicals from food plants. These stimuli are not in themselves favourable or unfavourable to development, but they herald an impending change in environmental conditions.
Preparation
The preparation phase usually follows the induction phase, though insects may go directly from induction to initiation without a preparation phase.
During this phase, insects accumulate and store molecules such as
lipids
Lipids are a broad group of organic compounds which include fats, waxes, sterols, fat-soluble vitamins (such as vitamins Vitamin A, A, Vitamin D, D, Vitamin E, E and Vitamin K, K), monoglycerides, diglycerides, phospholipids, and others. The fu ...
,
proteins
Proteins are large biomolecules and macromolecules that comprise one or more long chains of amino acid residues. Proteins perform a vast array of functions within organisms, including catalysing metabolic reactions, DNA replication, re ...
, and
carbohydrates
A carbohydrate () is a biomolecule composed of carbon (C), hydrogen (H), and oxygen (O) atoms. The typical hydrogen-to-oxygen atomic ratio is 2:1, analogous to that of water, and is represented by the empirical formula (where ''m'' and ''n'' ma ...
. These molecules are used to maintain the insect throughout diapause and to provide fuel for development following diapause termination. Composition of the
cuticle
A cuticle (), or cuticula, is any of a variety of tough but flexible, non-mineral outer coverings of an organism, or parts of an organism, that provide protection. Various types of "cuticle" are non- homologous, differing in their origin, structu ...
may be altered by changing
hydrocarbon
In organic chemistry, a hydrocarbon is an organic compound consisting entirely of hydrogen and carbon. Hydrocarbons are examples of group 14 hydrides. Hydrocarbons are generally colourless and Hydrophobe, hydrophobic; their odor is usually fain ...
composition and by adding
lipids
Lipids are a broad group of organic compounds which include fats, waxes, sterols, fat-soluble vitamins (such as vitamins Vitamin A, A, Vitamin D, D, Vitamin E, E and Vitamin K, K), monoglycerides, diglycerides, phospholipids, and others. The fu ...
to reduce water loss, making the organism resistant to desiccation. Diapausing
pupa
A pupa (; : pupae) is the life stage of some insects undergoing transformation between immature and mature stages. Insects that go through a pupal stage are holometabolous: they go through four distinct stages in their life cycle, the stages th ...
ria of the
flesh fly, ''Sarcophaga crassipalpis'', increase the amount of cuticular
hydrocarbons
In organic chemistry, a hydrocarbon is an organic compound consisting entirely of hydrogen and carbon. Hydrocarbons are examples of group 14 hydrides. Hydrocarbons are generally colourless and hydrophobic; their odor is usually faint, and may b ...
lining the puparium, effectively reducing the ability of water to cross the cuticle.
Initiation
Photoperiod is the most important stimulus initiating diapause.
[ The initiation phase begins when morphological development ceases.] In some cases, this change may be very distinct and can involve moulting
In biology, moulting (British English), or molting (American English), also known as sloughing, shedding, or in many invertebrates, ecdysis, is a process by which an animal casts off parts of its body to serve some beneficial purpose, either at ...
into a specific diapause stage, or be accompanied by color change. Enzymatic changes may take place in preparation for cold hardening. For example, only diapausing adults of the fire bug, ''Pyrrhocoris apterus'', have the enzymatic complement that allows them to accumulate polyhydric alcohols, molecules that help to lower their freezing points and thus avoid freezing. Insects may also undergo behavioural changes and begin to aggregate, migrate, or search for suitable overwintering sites.
Maintenance
During the maintenance phase, insects experience lowered metabolism
Metabolism (, from ''metabolē'', "change") is the set of life-sustaining chemical reactions in organisms. The three main functions of metabolism are: the conversion of the energy in food to energy available to run cellular processes; the co ...
and developmental arrest is maintained. Sensitivity to certain stimuli which act to prevent termination of diapause, such as photoperiod and temperature
Temperature is a physical quantity that quantitatively expresses the attribute of hotness or coldness. Temperature is measurement, measured with a thermometer. It reflects the average kinetic energy of the vibrating and colliding atoms making ...
, is increased. At this stage, insects are unresponsive to changes in the environment that will eventually trigger the end of diapause, but they grow more sensitive to these stimuli as time progresses.
Termination
In insects that undergo obligate diapause, termination may occur spontaneously, without any external stimuli. In facultative diapausers, token stimuli must occur to terminate diapause. These stimuli may include chilling, freezing, or contact with water
Water is an inorganic compound with the chemical formula . It is a transparent, tasteless, odorless, and Color of water, nearly colorless chemical substance. It is the main constituent of Earth's hydrosphere and the fluids of all known liv ...
, depending on the environmental conditions being avoided. These stimuli are important in preventing the insect from terminating diapause too soon, for instance in response to warm weather in late fall. In the Edith's checkerspot butterfly, individuals must receive enough sunlight in order to terminate the diapause stage and become a fully grown butterfly. Termination may occur at the height of unfavourable conditions, such as in the middle of winter. Over time, depth of diapause slowly decreases until direct development can resume, if conditions are favourable. Termination can also occur in specific time frames linked to reproductive periods, such as in the beetle '' Colaphellus bowringi:'' diapause ends for spring-reproducing beetles between late February and early April and for autumn-reproducing beetles between mid August and early October''.''
Post-diapause quiescence
Diapause frequently ends prior to the end of unfavourable conditions and is followed by a state of quiescence from which the insect can arouse and begin direct development, should conditions change to become more favourable. This allows the insect to continue to withstand harsh conditions while being ready to take advantage of good conditions as soon as possible.
Regulation
Diapause in insects is regulated at several levels. Environmental stimuli interact with genetic pre-programming to affect neuron
A neuron (American English), neurone (British English), or nerve cell, is an membrane potential#Cell excitability, excitable cell (biology), cell that fires electric signals called action potentials across a neural network (biology), neural net ...
al signalling, endocrine
The endocrine system is a messenger system in an organism comprising feedback loops of hormones that are released by internal glands directly into the circulatory system and that target and regulate distant organs. In vertebrates, the hypotha ...
pathways, and, eventually, metabolic and enzymatic changes.
Environmental
Environmental regulators of diapause generally display a characteristic seasonal pattern. In temperate
In geography, the temperate climates of Earth occur in the middle latitudes (approximately 23.5° to 66.5° N/S of the Equator), which span between the tropics and the polar regions of Earth. These zones generally have wider temperature ran ...
regions, photoperiod is the most reliable cues of seasonal change. This informs entry into reproductive diapause for many northern insects, including the fruit fly '' Drosophila montana.'' Depending on the season in which diapause occurs, either short or long days can act as token stimuli. Insects may also respond to changing day length as well as relative day length. Temperature may also act as a regulating factor, either by inducing diapause or, more commonly, by modifying the response of the insect to photoperiod. Insects may respond to thermoperiod, the daily fluctuations of warm and cold that correspond with night and day, as well as to absolute or cumulative temperature. This has been observed in many moth species including the Indian mealmoth, where individuals diapause in different developmental stages due to environmental temperature. Food availability and quality may also help regulate diapause. In the desert locust
The desert locust (''Schistocerca gregaria'') is a species of locust, a periodically swarming, short-horned grasshopper in the family Acrididae. They are found primarily in the deserts and dry areas of northern and eastern Africa, Arabia, and ...
, ''Schistocerca gregaria'', a plant hormone
A hormone (from the Ancient Greek, Greek participle , "setting in motion") is a class of cell signaling, signaling molecules in multicellular organisms that are sent to distant organs or tissues by complex biological processes to regulate physio ...
called gibberellin
Gibberellins (GAs) are plant hormones that regulate various Biological process, developmental processes, including Plant stem, stem elongation, germination, dormancy, flowering, flower development, and leaf and fruit senescence. They are one of th ...
stimulates reproductive
The reproductive system of an organism, also known as the genital system, is the biological system made up of all the anatomical organs involved in sexual reproduction. Many non-living substances such as fluids, hormones, and pheromones are al ...
development. During the dry season, when their food plants are in senescence
Senescence () or biological aging is the gradual deterioration of Function (biology), functional characteristics in living organisms. Whole organism senescence involves an increase in mortality rate, death rates or a decrease in fecundity with ...
and lacking gibberellin, the locusts remain immature and their reproductive tracts do not develop.
Neuroendocrine
The neuroendocrine
Neuroendocrine cells are cells that receive neuronal input (through neurotransmitters released by nerve cells or neurosecretory cells) and, as a consequence of this input, release messenger molecules ( hormones) into the blood. In this way they b ...
system of insects consists primarily of neurosecretory cells in the brain
The brain is an organ (biology), organ that serves as the center of the nervous system in all vertebrate and most invertebrate animals. It consists of nervous tissue and is typically located in the head (cephalization), usually near organs for ...
, the corpora cardiaca, corpora allata and the prothoracic glands. There are several key hormone
A hormone (from the Ancient Greek, Greek participle , "setting in motion") is a class of cell signaling, signaling molecules in multicellular organisms that are sent to distant organs or tissues by complex biological processes to regulate physio ...
s involved in the regulation of diapause: juvenile hormone (JH), diapause hormone (DH), and prothoracicotropic hormone (PTTH).
Prothoracicotropic hormone stimulates the prothoracic glands to produce ecdysteroids that are required to promote development. Larval and pupal diapauses are often regulated by an interruption of this connection, either by preventing release of prothoracicotropic hormone from the brain or by failure of the prothoracic glands to respond to prothoracicotropic hormone.
The corpora allata is responsible for the production of juvenile hormone (JH). In the bean bug, ''Riptortus pedestris'', clusters of neurons
A neuron (American English), neurone (British English), or nerve cell, is an membrane potential#Cell excitability, excitable cell (biology), cell that fires electric signals called action potentials across a neural network (biology), neural net ...
on the protocerebrum
The protocerebrum is the first segment of the supraoesophageal ganglion, panarthropod brain.
Recent studies suggest that it comprises two regions.
Region associated with the expression of ''six3''
''six3'' is a transcription factor that marks ...
called the pars lateralis maintain reproductive diapause by inhibiting JH production by the corpora allata. Adult diapause is often associated with the absence of JH, while larval diapause is often associated with its presence.
In adults, absence of JH causes degeneration of flight muscles
Muscle is a soft tissue, one of the four basic types of animal tissue. There are three types of muscle tissue in vertebrates: skeletal muscle, cardiac muscle, and smooth muscle. Muscle tissue gives skeletal muscles the ability to muscle contra ...
and atrophy
Atrophy is the partial or complete wasting away of a part of the body. Causes of atrophy include mutations (which can destroy the gene to build up the organ), malnutrition, poor nourishment, poor circulatory system, circulation, loss of hormone, ...
or cessation of development of reproductive tissues, and halts mating behaviour. The presence of JH in larvae may prevent moulting to the next larval instar
An instar (, from the Latin '' īnstar'' 'form, likeness') is a developmental stage of arthropods, such as insects, which occurs between each moult (''ecdysis'') until sexual maturity is reached. Arthropods must shed the exoskeleton in order to ...
, though successive stationary moults may still occur. In the corn borer, ''Diatraea gradiosella'', JH is required for the accumulation by the fat body of a storage protein
Proteins are large biomolecules and macromolecules that comprise one or more long chains of amino acid residue (biochemistry), residues. Proteins perform a vast array of functions within organisms, including Enzyme catalysis, catalysing metab ...
that is associated with diapause.
Diapause hormone regulates embryo
An embryo ( ) is the initial stage of development for a multicellular organism. In organisms that reproduce sexually, embryonic development is the part of the life cycle that begins just after fertilization of the female egg cell by the male sp ...
nic diapause in the eggs of the silkworm
''Bombyx mori'', commonly known as the domestic silk moth, is a moth species belonging to the family Bombycidae. It is the closest relative of '' Bombyx mandarina'', the wild silk moth. Silkworms are the larvae of silk moths. The silkworm is of ...
moth, ''Bombyx mori''. DH is released from the subesophageal ganglion of the mother and triggers trehalase production by the ovaries
The ovary () is a gonad in the female reproductive system that produces ova; when released, an ovum travels through the fallopian tube/oviduct into the uterus. There is an ovary on the left and the right side of the body. The ovaries are endocr ...
. This generates high levels of glycogen
Glycogen is a multibranched polysaccharide of glucose that serves as a form of energy storage in animals, fungi, and bacteria. It is the main storage form of glucose in the human body.
Glycogen functions as one of three regularly used forms ...
in the eggs, which is converted into the polyhydric alcohols glycerol
Glycerol () is a simple triol compound. It is a colorless, odorless, sweet-tasting, viscous liquid. The glycerol backbone is found in lipids known as glycerides. It is also widely used as a sweetener in the food industry and as a humectant in pha ...
and sorbitol. Sorbitol
Sorbitol (), less commonly known as glucitol (), is a sugar alcohol with a sweet taste which the human body metabolizes slowly. It can be obtained by reduction of glucose, which changes the converted aldehyde group (−CHO) to a primary alco ...
directly inhibits the development of the embryos. Glycerol
Glycerol () is a simple triol compound. It is a colorless, odorless, sweet-tasting, viscous liquid. The glycerol backbone is found in lipids known as glycerides. It is also widely used as a sweetener in the food industry and as a humectant in pha ...
and sorbitol
Sorbitol (), less commonly known as glucitol (), is a sugar alcohol with a sweet taste which the human body metabolizes slowly. It can be obtained by reduction of glucose, which changes the converted aldehyde group (−CHO) to a primary alco ...
are reconverted into glycogen
Glycogen is a multibranched polysaccharide of glucose that serves as a form of energy storage in animals, fungi, and bacteria. It is the main storage form of glucose in the human body.
Glycogen functions as one of three regularly used forms ...
at the termination of diapause.
Tropical diapause
Diapause in the tropics
The tropics are the regions of Earth surrounding the equator, where the sun may shine directly overhead. This contrasts with the temperate or polar regions of Earth, where the Sun can never be directly overhead. This is because of Earth's ax ...
is often initiated in response to biotic rather than abiotic component
In biology and ecology, abiotic components or abiotic factors are non-living chemical and physical parts of the environment that affect living organisms and the functioning of ecosystems. Abiotic factors and the phenomena associated with them und ...
s. For example, food in the form of vertebrate
Vertebrates () are animals with a vertebral column (backbone or spine), and a cranium, or skull. The vertebral column surrounds and protects the spinal cord, while the cranium protects the brain.
The vertebrates make up the subphylum Vertebra ...
carcasses may be more abundant following dry seasons, or oviposition
The ovipositor is a tube-like organ used by some animals, especially insects, for the laying of eggs. In insects, an ovipositor consists of a maximum of three pairs of appendages. The details and morphology of the ovipositor vary, but typica ...
sites in the form of fallen trees
In botany, a tree is a perennial plant with an elongated stem, or trunk, usually supporting branches and leaves. In some usages, the definition of a tree may be narrower, e.g., including only woody plants with secondary growth, only p ...
may be more available following rainy seasons. Also, diapause may serve to synchronize mating seasons or reduce competition, rather than to avoid unfavourable climatic conditions.
Diapause in the tropics poses several challenges to insects that are not faced in temperate
In geography, the temperate climates of Earth occur in the middle latitudes (approximately 23.5° to 66.5° N/S of the Equator), which span between the tropics and the polar regions of Earth. These zones generally have wider temperature ran ...
zones. Insects must reduce their metabolism without the aid of cold temperatures and may be faced with increased water loss due to high temperatures. While cold temperatures inhibit the growth of fungi
A fungus (: fungi , , , or ; or funguses) is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and mold (fungus), molds, as well as the more familiar mushrooms. These organisms are classified as one ...
and bacteria
Bacteria (; : bacterium) are ubiquitous, mostly free-living organisms often consisting of one Cell (biology), biological cell. They constitute a large domain (biology), domain of Prokaryote, prokaryotic microorganisms. Typically a few micr ...
, diapausing tropical insects still have to deal with these pathogens
In biology, a pathogen (, "suffering", "passion" and , "producer of"), in the oldest and broadest sense, is any organism or agent that can produce disease. A pathogen may also be referred to as an infectious agent, or simply a germ.
The term ...
. Also, predator
Predation is a biological interaction in which one organism, the predator, kills and eats another organism, its prey. It is one of a family of common List of feeding behaviours, feeding behaviours that includes parasitism and micropredation ...
s and parasites may still be abundant during the diapause period.
Aggregations are common among diapausing tropical insects, especially in the orders Coleoptera
Beetles are insects that form the Taxonomic rank, order Coleoptera (), in the superorder Holometabola. Their front pair of wings are hardened into wing-cases, elytra, distinguishing them from most other insects. The Coleoptera, with about 40 ...
, Lepidoptera
Lepidoptera ( ) or lepidopterans is an order (biology), order of winged insects which includes butterflies and moths. About 180,000 species of the Lepidoptera have been described, representing 10% of the total described species of living organ ...
, and Hemiptera
Hemiptera (; ) is an order of insects, commonly called true bugs, comprising more than 80,000 species within groups such as the cicadas, aphids, planthoppers, leafhoppers, assassin bugs, bed bugs, and shield bugs. They range in size from ...
. Aggregations may be used as protection against predation
Predation is a biological interaction in which one organism, the predator, kills and eats another organism, its prey. It is one of a family of common List of feeding behaviours, feeding behaviours that includes parasitism and micropredation ...
, since aggregating species are frequently toxic and predators quickly learn to avoid them. They can also serve to reduce water loss, as seen in the fungus beetle
Beetles are insects that form the Taxonomic rank, order Coleoptera (), in the superorder Holometabola. Their front pair of wings are hardened into wing-cases, elytra, distinguishing them from most other insects. The Coleoptera, with about 40 ...
, '' Stenotarsus rotundus'', which forms aggregations of up to 70,000 individuals, which may be eight beetles deep. Relative humidity
Humidity is the concentration of water vapor present in the air. Water vapor, the gaseous state of water, is generally invisible to the human eye. Humidity indicates the likelihood for precipitation (meteorology), precipitation, dew, or fog t ...
is increased within the aggregations and beetles experience less water loss, probably due to decreased surface area to volume ratios reducing evaporative water loss.
See also
Embryonic diapause
Embryonic diapause (delayed implantation in mammals) is a reproductive strategy used by a number of animal species across different biological classes. In more than 130 types of mammals where this takes place, the process occurs at the blastocys ...
*'' Eburia quadrigeminata'', the species with the longest reported diapause among insects (up to 40 years).
*'' Polygonia c-album'', whose larvae exhibit density-dependent polymorphism where one of two morphs is a diapausing phase.
*'' Nebria brevicollis,'' a carabid beetle who exhibits diapause behavior due to low food resource availability.
References
{{reflist
Physiology
Developmental biology
Ethology
Animal migration
Arthropod ecology
Lepidopterology