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Embryonic diapause (from late 19th century English: dia- ‘through’ + pause- 'delay') (aka delayed implantation in mammals) is an
evolutionary Evolution is change in the heritable characteristics of biological populations over successive generations. These characteristics are the expressions of genes, which are passed on from parent to offspring during reproduction. Variation t ...
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 ...
strategy used by several animal species across a number of kingdoms, including approximately 130 different
mammals Mammals () are a group of vertebrate animals constituting the class Mammalia (), characterized by the presence of mammary glands which in females produce milk for feeding (nursing) their young, a neocortex (a region of the brain), fur or ...
, which takes place in order to ensure the survival of offspring. The process occurs at the
blastocyst The blastocyst is a structure formed in the early embryonic development of mammals. It possesses an inner cell mass (ICM) also known as the ''embryoblast'' which subsequently forms the embryo, and an outer layer of trophoblast cells called the t ...
stage of embryo development in most species, and is characterized by a dramatic reduction or complete cessation of mitotic activity, arresting most often in the G0 or G1 phase of division. In placental embryonic diapause, the
embryonic Embryonic may refer to: *Of or relating to an embryo An embryo is an initial stage of development of a multicellular organism. In organisms that reproduce sexually, embryonic development is the part of the life cycle that begins just after f ...
blastocyst The blastocyst is a structure formed in the early embryonic development of mammals. It possesses an inner cell mass (ICM) also known as the ''embryoblast'' which subsequently forms the embryo, and an outer layer of trophoblast cells called the t ...
does not immediately implant in the
uterus The uterus (from Latin ''uterus'', plural ''uteri'') or womb () is the organ in the reproductive system of most female mammals, including humans that accommodates the embryonic and fetal development of one or more embryos until birth. The uter ...
after
sexual reproduction Sexual reproduction is a type of reproduction that involves a complex life cycle in which a gamete ( haploid reproductive cells, such as a sperm or egg cell) with a single set of chromosomes combines with another gamete to produce a zygote tha ...
has created the
zygote A zygote (, ) is a eukaryotic cell formed by a fertilization event between two gametes. The zygote's genome is a combination of the DNA in each gamete, and contains all of the genetic information of a new individual organism. In multicellula ...
, but rather remains in this non-dividing state of
dormancy Dormancy is a period in an organism's life cycle when growth, development, and (in animals) physical activity are temporarily stopped. This minimizes metabolic activity and therefore helps an organism to conserve energy. Dormancy tends to be clos ...
until conditions allow for attachment to the uterine wall to proceed as normal. As a result, the normal
gestation Gestation is the period of development during the carrying of an embryo, and later fetus, inside viviparous animals (the embryo develops within the parent). It is typical for mammals, but also occurs for some non-mammals. Mammals during pregna ...
period is extended for a species-specific time. Organisms which undergo embryonic diapause are able to synchronize the birth of all offspring to the most favorable conditions for reproductive success, irrespective of when mating took place. As timing and environment are important, many different factors can induce embryonic diapause, such as the time of year, temperature, lactation and supply of food. Embryonic diapause is considered a relatively widespread phenomenon outside of mammals, with known presence in the reproductive cycles in many insects, nematodes, fish, and other non-mammalian vertebrates. It has been observed additionally in less than 2% of mammalian species, including certain
rodents Rodents (from Latin , 'to gnaw') are mammals of the Order (biology), order Rodentia (), which are characterized by a single pair of continuously growing incisors in each of the upper and lower jaws. About 40% of all mammal species are roden ...
,
bears Bears are carnivoran mammals of the family Ursidae. They are classified as caniforms, or doglike carnivorans. Although only eight species of bears are extant, they are widespread, appearing in a wide variety of habitats throughout the Nort ...
,
armadillos Armadillos (meaning "little armored ones" in Spanish) are New World placental mammals in the order Cingulata. The Chlamyphoridae and Dasypodidae are the only surviving families in the order, which is part of the superorder Xenarthra, along ...
,
mustelids The Mustelidae (; from Latin ''mustela'', weasel) are a family of carnivorous mammals, including weasels, badgers, otters, ferrets, martens, minks and wolverines, among others. Mustelids () are a diverse group and form the largest family in ...
(e.g.
weasels Weasels are mammals of the genus ''Mustela'' of the family Mustelidae. The genus ''Mustela'' includes the least weasels, polecats, stoats, ferrets and European mink. Members of this genus are small, active predators, with long and slender bodi ...
and
badgers Badgers are short-legged omnivores in the family Mustelidae (which also includes the otters, wolverines, martens, minks, polecats, weasels, and ferrets). Badgers are a polyphyletic rather than a natural taxonomic grouping, being united by t ...
), and
marsupials Marsupials are any members of the mammalian infraclass Marsupialia. All extant marsupials are endemic to Australasia, Wallacea and the Americas. A distinctive characteristic common to most of these species is that the young are carried in a po ...
(e.g.
kangaroos Kangaroos are four marsupials from the family Macropodidae (macropods, meaning "large foot"). In common use the term is used to describe the largest species from this family, the red kangaroo, as well as the antilopine kangaroo, eastern gre ...
). Some groups only have one species that undergoes embryonic diapause, such as the
roe deer The roe deer (''Capreolus capreolus''), also known as the roe, western roe deer, or European roe, is a species of deer. The male of the species is sometimes referred to as a roebuck. The roe is a small deer, reddish and grey-brown, and well-adapt ...
in the order
Artiodactyla The even-toed ungulates (Artiodactyla , ) are ungulates—hoofed animals—which bear weight equally on two (an even number) of their five toes: the third and fourth. The other three toes are either present, absent, vestigial, or pointing poster ...
. Furthermore, recent studies have demonstrated even the ability for species which do not traditionally undergo embryonic discontinuous development to exhibit reversible developmental arrest, indicating some potential evolutionary significance of this phenomenon, or at least some evidence that embryonic diapause is more widespread than we currently understand.


General mechanism

All multicellular organisms, from their conception, begin as a small number of cells and only grow and develop as those cells divide. In organisms which are capable of embryonic development, in non-ideal reproductive conditions, there is a cessation of cellular division which prevents the embryo from growing and maturing, delaying the maturation of the embryo until conditions are ideal enough to promote the survival of the offspring, and in some cases, the mother. Regulation of the cell cycle as it relates to embryonic diapause has been linked to the ''dacapo'' gene in the fruit fly, responsible for inhibiting the formation of cyclin E-cdk2 complexes necessary for DNA synthesis. There is also evidence pointing to the upregulation of B cell translocation gene 1 (Btg1) in the mouse embryo during diapause, another known regulator of the cell cycle, responsible for inhibiting transition from G0/G1. Other studies have demonstrated, inversely, the lack of involvement of more common regulators of the cell cycle such as p53 within the placental model of embryonic diapause. While much of the molecular regulation involved in activating dormant blastocysts has been characterized, little widely applicable characterization is available regarding entry into diapause, and the conditions which enable a
blastocyst The blastocyst is a structure formed in the early embryonic development of mammals. It possesses an inner cell mass (ICM) also known as the ''embryoblast'' which subsequently forms the embryo, and an outer layer of trophoblast cells called the t ...
to remain dormant. Once the embryo exits diapause arrest and resumes regular development, no adverse effects are observed. Specifically within placental embryonic diapause, this cessation is led by the intentional failure of the blastocyst to implant in the uterine wall, which is an essential component in developmental progression in these species. Hormones relating to the failed implantation also contribute to the embryonic arrest.


Types

There are two distinct forms of embryonic diapause, characterized by different conditions of onset. Facultative diapause occurs in response to certain environmental or metabolic stressors, such as drastic changes in temperature, feeding, or lactation. Obligate diapause occurs regularly in the reproductive cycle of the affected species, and is often associated with seasonal changes and photo-period.


Facultative diapause

Facultative diapause is regulated by several factors, including the maternal environment and ovarian competency, the pituitary gland, and metabolic stress and lactation. With regards to the many other regulators of this form of diapause, in placental mammals, facultative diapause is most often the result of fertilization shortly following the birth of a previous litter, The consequential pups suckling during
lactation Lactation describes the secretion of milk from the mammary glands and the period of time that a mother lactates to feed her young. The process naturally occurs with all sexually mature female mammals, although it may predate mammals. The proce ...
promotes
prolactin Prolactin (PRL), also known as lactotropin, is a protein best known for its role in enabling mammals to produce milk. It is influential in over 300 separate processes in various vertebrates, including humans. Prolactin is secreted from the p ...
to be released. This in turn reduces
progesterone Progesterone (P4) is an endogenous steroid and progestogen sex hormone involved in the menstrual cycle, pregnancy, and embryogenesis of humans and other species. It belongs to a group of steroid hormones called the progestogens and is the major ...
secretion from the
corpus luteum The corpus luteum (Latin for "yellow body"; plural corpora lutea) is a temporary endocrine structure in female ovaries involved in the production of relatively high levels of progesterone, and moderate levels of estradiol, and inhibin A. It is th ...
in a pregnant female. The corpus luteum is a temporary
endocrine organ The endocrine system is a messenger system comprising feedback loops of the hormones released by internal glands of an organism directly into the circulatory system, regulating distant target organs. In vertebrates, the hypothalamus is the neur ...
that is formed from the leftover cells from the
ovarian follicle An ovarian follicle is a roughly spheroid cellular aggregation set found in the ovaries. It secretes hormones that influence stages of the menstrual cycle. At the time of puberty, women have approximately 200,000 to 300,000 follicles, each with t ...
in the
ovary The ovary is an organ in the female reproductive system that produces an ovum. When released, this travels down the fallopian tube into the uterus, where it may become fertilized by a sperm. There is an ovary () found on each side of the body. ...
, once it has released a mature ovum. The main function of the corpus luteum is to secrete
progesterone Progesterone (P4) is an endogenous steroid and progestogen sex hormone involved in the menstrual cycle, pregnancy, and embryogenesis of humans and other species. It belongs to a group of steroid hormones called the progestogens and is the major ...
during pregnancy in order to maintain the
uterine The uterus (from Latin ''uterus'', plural ''uteri'') or womb () is the organ in the reproductive system of most female mammals, including humans that accommodates the embryonic and fetal development of one or more embryos until birth. The ut ...
environment needed. Prolactin acting on the corpus luteum causes the progesterone level to be below optimal concentration and therefore induces embryonic facultative diapause. Each
species In biology, a species is the basic unit of Taxonomy (biology), classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of ...
that undergoes facultative diapause tends to have a specific developmental stage, that is genetically determined, in which this process is initiated. This form of diapause is most well studied in rodents and marsupials but has been identified in many other species, including non-mammals. It is not clear how well the mechanisms studied for the onset, maintenance and release from facultative diapause in the rodent model apply to these other species.


Obligate diapause

Obligate {{wiktionary, obligate As an adjective, obligate means "by necessity" (antonym '' facultative'') and is used mainly in biology in phrases such as: * Obligate aerobe, an organism that cannot survive without oxygen * Obligate anaerobe, an organism tha ...
(adj: by necessity) diapause (a.k.a. seasonal delayed implantation) is a mechanism ensuring the birth of offspring is timed during optimal environmental conditions, to ensure maximal survival. The proposed mechanism is to separate conception and
parturition Birth is the act or process of bearing or bringing forth offspring, also referred to in technical contexts as parturition. In mammals, the process is initiated by hormones which cause the muscular walls of the uterus to contract, expelling the f ...
(birth) so that each can occur at the most favourable time of year. Obligate diapause is activated and deactivated by changes to the number of daylight hours within a day (photoperiod) and hence, occurs within specific seasons. While obligate diapause occurs in a variety of
species In biology, a species is the basic unit of Taxonomy (biology), classification and a taxonomic rank of an organism, as well as a unit of biodiversity. A species is often defined as the largest group of organisms in which any two individuals of ...
in different groups, there are significant variations in diapause length. Skunks (
Spilogale gracilis The western spotted skunk (''Spilogale gracilis'') is a spotted skunk of western North America. Description With a total length of , the western spotted skunk is smaller than the striped skunk (''Mephitis mephitis''). Males, which weigh , are s ...
) have a diapause of around 200 days while minks ( Neovision vison) only have a diapause of around 14 days. Similarly to facultative diapause, a series of hormonal changes arrest the
blastocyst The blastocyst is a structure formed in the early embryonic development of mammals. It possesses an inner cell mass (ICM) also known as the ''embryoblast'' which subsequently forms the embryo, and an outer layer of trophoblast cells called the t ...
development, prior to implantation, preventing continued growth of the
embryo An embryo is an initial stage of development of 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 sperm c ...
. However, in obligate diapause, the blastocyst shall enter into the dormant state in every reproductive season. This means every blastocyst a mother produces shall enter a period of diapause. Close regulation of obligate diapause is essential for survival of the mother and offspring. Premature diapause can result in forgone growth and breeding opportunities and late diapause can result in death due to adverse conditions. Prior to the vernal equinox, the photoperiod is less than 12 hours. This increases the production of
melatonin Melatonin is a natural product found in plants and animals. It is primarily known in animals as a hormone released by the pineal gland in the brain at night, and has long been associated with control of the sleep–wake cycle. In vertebrates ...
in the
pineal gland The pineal gland, conarium, or epiphysis cerebri, is a small endocrine gland in the brain of most vertebrates. The pineal gland produces melatonin, a serotonin-derived hormone which modulates sleep patterns in both circadian and seasonal cycl ...
. Due to the inhibitory relationship between melatonin and
prolactin Prolactin (PRL), also known as lactotropin, is a protein best known for its role in enabling mammals to produce milk. It is influential in over 300 separate processes in various vertebrates, including humans. Prolactin is secreted from the p ...
, this increase in melatonin decreases prolactin secretion from the
pituitary gland In vertebrate anatomy, the pituitary gland, or hypophysis, is an endocrine gland, about the size of a chickpea and weighing, on average, in humans. It is a protrusion off the bottom of the hypothalamus at the base of the brain. The hypoph ...
. The decrease in prolactin consequently decreases
progesterone Progesterone (P4) is an endogenous steroid and progestogen sex hormone involved in the menstrual cycle, pregnancy, and embryogenesis of humans and other species. It belongs to a group of steroid hormones called the progestogens and is the major ...
production in the
corpus luteum The corpus luteum (Latin for "yellow body"; plural corpora lutea) is a temporary endocrine structure in female ovaries involved in the production of relatively high levels of progesterone, and moderate levels of estradiol, and inhibin A. It is th ...
, preventing development of the blastocyst. This induces embryonic diapause. After the vernal equinox, the photoperiod is greater than 12 hours. This decreases the production of melatonin in the pineal gland and, therefore, increases the prolactin and progesterone production in the pituitary gland and corpus luteum respectively. The increase in prolactin induces expression of the gene Odc (
ornithine decarboxylase The enzyme ornithine decarboxylase (, ODC) catalyzes the decarboxylation of ornithine (a product of the urea cycle) to form putrescine. This reaction is the committed step in polyamine synthesis. In humans, this protein has 461 amino acids and fo ...
). The Odc gene produces the ODC protein, a rate-limiting enzyme in the production of the
polyamine A polyamine is an organic compound having more than two amino groups. Alkyl polyamines occur naturally, but some are synthetic. Alkylpolyamines are colorless, hygroscopic, and water soluble. Near neutral pH, they exist as the ammonium derivatives. ...
,
putrescine Putrescine is an organic compound with the formula (CH2)4(NH2)2. It is a colorless solid that melts near room temperature. It is classified as a diamine. Together with cadaverine, it is largely responsible for the foul odor of putrefying flesh, ...
, within the
uterine The uterus (from Latin ''uterus'', plural ''uteri'') or womb () is the organ in the reproductive system of most female mammals, including humans that accommodates the embryonic and fetal development of one or more embryos until birth. The ut ...
environment. The presence of putrescine may indicate a role in inducing the escape of the embryo from obligate diapause.


Embryonic stem cells

Embryonic stem cells (ESCs) have the potential to allow for further understanding of the mechanisms controlling embryonic diapause. This is because the ESCs and diapausing blastocysts having very similar transcriptome profiles. ESCs are derived from the undifferentiated inner mass cells of blastocysts of an embryo - with the capability of continual proliferation in vitro. ESCs are mostly derived from mouse models, at the point where the ESCs are at optimal efficiency and are able to enter diapause. Both diapausing blastocysts and ESCs have transcriptome profile similarities, including downregulation of
metabolism Metabolism (, from el, μεταβολή ''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 cel ...
,
biosynthesis Biosynthesis is a multi-step, enzyme- catalyzed process where substrates are converted into more complex products in living organisms. In biosynthesis, simple compounds are modified, converted into other compounds, or joined to form macromolecule ...
and
gene expression Gene expression is the process by which information from a gene is used in the synthesis of a functional gene product that enables it to produce end products, protein or non-coding RNA, and ultimately affect a phenotype, as the final effect. The ...
pathways. These similarities allow for the potential to use ESCs as a cellular model to identify the molecular factors which regulate embryonic diapause.


References

* {{Refend Developmental biology he:דיאפאוזה pl:Ciąża przedłużona fi:Diapaussi