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 blastocyst stage of embryonic development, 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 after sexual reproduction has resulted in the zygote, but rather remains in this non-dividing state of dormancy until conditions allow for attachment to the uterine wall to proceed as normal. As a result, the normal gestation 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 evolutionary 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 rodents, bears, armadillos, mustelids (e.g. weasels and badgers), and marsupials (e.g. kangaroos). Some groups only have one species that undergoes embryonic diapause, such as the roe deer in the order Artiodactyla.
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 blastocysts 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.