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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
mammal A mammal () is a vertebrate animal of the Class (biology), class Mammalia (). Mammals are characterised by the presence of milk-producing mammary glands for feeding their young, a broad neocortex region of the brain, fur or hair, and three ...
s where this takes place, 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 ...
stage of
embryonic development In developmental biology, animal embryonic development, also known as animal embryogenesis, is the developmental stage of an animal embryo. Embryonic development starts with the fertilization of an egg cell (ovum) by a sperm, sperm cell (spermat ...
, 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 blastocyst does not immediately implant in the
uterus The uterus (from Latin ''uterus'', : uteri or uteruses) or womb () is the hollow organ, organ in the reproductive system of most female mammals, including humans, that accommodates the embryonic development, embryonic and prenatal development, f ...
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 resulted in the
zygote A zygote (; , ) is a eukaryote, eukaryotic cell (biology), 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 individ ...
, but rather remains in this non-dividing state of
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 ...
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 pregn ...
period is extended for a species-specific time. Diapause provides a survival advantage to offspring, because birth or emergence of young can be timed to coincide with the most hospitable conditions, regardless of when mating occurs or length of gestation; any such gain in survival rates of progeny confers an
evolution Evolution is the change in the heritable Phenotypic trait, characteristics of biological populations over successive generations. It occurs when evolutionary processes such as natural selection and genetic drift act on genetic variation, re ...
ary advantage.


Evolutionary significance

Organisms which undergo embryonic diapause are able to synchronize the birth of offspring to the most favorable conditions for reproductive success, irrespective of when mating took place. Many different factors can induce embryonic diapause, such as the time of year, temperature, lactation and supply of food. Embryonic diapause is a relatively widespread phenomenon outside of mammals, with known occurrence in the reproductive cycles of many insects, nematodes, fish, and other non-mammalian vertebrates. It has been observed in approximately 130 mammalian species, which is less than two percent of all species of mammals. These include certain
pinnipeds Pinnipeds (pronounced ), commonly known as seals, are a widely distributed and diverse clade of carnivorous, fin-footed, semiaquatic, mostly marine mammals. They comprise the extant families Odobenidae (whose only living member is the walr ...
,
rodent 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 Mandible, lower jaws. About 40% of all mammal specie ...
s,
bear Bears are carnivoran mammals of the family (biology), 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 ...
s,
armadillo Armadillos () are New World placental mammals in the order (biology), order Cingulata. They form part of the superorder Xenarthra, along with the anteaters and sloths. 21 extant species of armadillo have been described, some of which are dis ...
s,
mustelid The Mustelidae (; from Latin , weasel) are a diverse family of carnivoran mammals, including weasels, badgers, otters, polecats, martens, grisons, and wolverines. Otherwise known as mustelids (), they form the largest family in the suborde ...
s (e.g.
weasel 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 slend ...
s and
badger Badgers are medium-sized short-legged omnivores in the superfamily Musteloidea. Badgers are a polyphyletic rather than a natural taxonomic grouping, being united by their squat bodies and adaptions for fossorial activity rather than by the ...
s), and
marsupial Marsupials are a diverse group of mammals belonging to the infraclass Marsupialia. They are natively found in Australasia, Wallacea, and the Americas. One of marsupials' unique features is their reproductive strategy: the young are born in a r ...
s (e.g.
kangaroo Kangaroos are 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 ...
s). Some groups only have one species that undergoes embryonic diapause, such as the roe deer in the
order Order, ORDER or Orders may refer to: * A socio-political or established or existing order, e.g. World order, Ancien Regime, Pax Britannica * Categorization, the process in which ideas and objects are recognized, differentiated, and understood ...
Artiodactyla Artiodactyls are placental mammals belonging to the order (biology), order Artiodactyla ( , ). Typically, they are ungulates which bear weight equally on two (an even number) of their five toes (the third and fourth, often in the form of a hoof ...
. Experimental induction of embryonic discontinuous development within species which do not spontaneously undergo embryonic diapause in nature has been achieved; reversible developmental arrest was successfully demonstrated. This may be evidence for the evolutionary significance of this phenomenon, with latent capacity for diapause potentially present in a much wider segment of species than known to occur naturally.


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 diapause, 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
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 ...
s has been characterized, little widely applicable characterization is available regarding entry into diapause, and the conditions which enable a blastocyst 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 process ...
promotes
prolactin Prolactin (PRL), also known as lactotropin and mammotropin, 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 secr ...
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 ma ...
secretion from the
corpus luteum The corpus luteum (Latin for "yellow body"; : 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 the ...
in a pregnant female. The corpus luteum is a temporary endocrine organ 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. In humans, women have approximately 200,000 to 300,000 follicles at the time of puberty, ea ...
in the
ovary 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 end ...
, once it has released a mature
ovum The egg cell or ovum (: ova) is the female reproductive cell, or gamete, in most anisogamous organisms (organisms that reproduce sexually with a larger, female gamete and a smaller, male one). The term is used when the female gamete is not capa ...
. 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 ma ...
during pregnancy in order to maintain the
uterine The uterus (from Latin ''uterus'', : uteri or uteruses) 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 fertilized eggs until bir ...
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 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), ...
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 ...
(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 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), ...
in different groups, there are significant variations in diapause length. Western spotted skunks (''Spilogale gracilis'') have a diapause of around 200 days while
American mink The American mink (''Neogale vison'') is a semiaquatic species of Mustelidae, mustelid native to North America, though human introduction has expanded its range to many parts of Europe, Asia, and South America. Because of range expansion, the Am ...
s (''Neogale vison'') only have a diapause of around fourteen 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 ...
development, prior to implantation, preventing continued growth of the embryo. 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 A solar equinox is a moment in time when the Sun appears directly above the equator, rather than to its north or south. On the day of the equinox, the Sun appears to rise directly east and set directly west. This occurs twice each year, arou ...
, the photoperiod is less than 12 hours. This increases the production of
melatonin Melatonin, an indoleamine, is a natural compound produced by various organisms, including bacteria and eukaryotes. Its discovery in 1958 by Aaron B. Lerner and colleagues stemmed from the isolation of a substance from the pineal gland of cow ...
in the
pineal gland The pineal gland (also known as the pineal body or epiphysis cerebri) is a small endocrine gland in the brain of most vertebrates. It produces melatonin, a serotonin-derived hormone, which modulates sleep, sleep patterns following the diurnal c ...
. Due to the inhibitory relationship between melatonin and
prolactin Prolactin (PRL), also known as lactotropin and mammotropin, 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 secr ...
, this increase in melatonin decreases prolactin secretion from the
pituitary gland The pituitary gland or hypophysis is an endocrine gland in vertebrates. In humans, the pituitary gland is located at the base of the human brain, brain, protruding off the bottom of the hypothalamus. The pituitary gland and the hypothalamus contr ...
. 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 ma ...
production in the
corpus luteum The corpus luteum (Latin for "yellow body"; : 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 the ...
, 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 ...
). The Odc gene produces the ODC protein, a rate-limiting enzyme in the production of the
polyamine A polyamine is an organic compound having two or more 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 Putrefaction, putref ...
, within the
uterine The uterus (from Latin ''uterus'', : uteri or uteruses) 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 fertilized eggs until bir ...
environment. The presence of putrescine may indicate a role in inducing the escape of the embryo from obligate diapause.


Embryonic stem cells

Embryonic stem cell Embryonic stem cells (ESCs) are Cell potency#Pluripotency, pluripotent stem cells derived from the inner cell mass of a blastocyst, an early-stage pre-Implantation (human embryo), implantation embryo. Human embryos reach the blastocyst stage 4� ...
s (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 ''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 ...
,
biosynthesis Biosynthesis, i.e., chemical synthesis occurring in biological contexts, is a term most often referring to multi-step, enzyme-Catalysis, catalyzed processes where chemical substances absorbed as nutrients (or previously converted through biosynthe ...
and
gene expression Gene expression is the process (including its Regulation of gene expression, regulation) by which information from a gene is used in the synthesis of a functional gene product that enables it to produce end products, proteins or non-coding RNA, ...
pathways. These similarities allow for the potential to use ESCs as a cellular model to identify the molecular factors which regulate embryonic diapause.


See also

* Weddell seal#Breeding


Notes


References


Further reading

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