Menstruation (mammal)

Menstruation is the shedding of the uterine lining (endometrium). It occurs on a regular basis in uninseminated[1] sexually reproductive-age females of certain mammal species.

For menstruation in humans, see Menstruation.

Although there is some disagreement in definitions between sources, menstruation is generally considered to be limited to primates. Overt menstruation (where there is bleeding from the uterus through the vagina) is found primarily in humans and close relatives such as chimpanzees.[2] It is common in simians (Old World monkeys, and apes), but completely lacking in strepsirrhine primates and possibly weakly present in tarsiers. Beyond primates, it is known only in bats, the elephant shrew, and the spiny mouse.[3][4][5][6][7]

Females of other species of placental mammal undergo estrous cycles, in which the endometrium is completely reabsorbed by the animal (covert menstruation) at the end of its reproductive cycle. Many zoologists regard this as different from a "true" menstrual cycle. Female domestic animals used for breeding —for example dogs, pigs, cattle, or horses— are monitored for physical signs of an estrous cycle period, which indicates that the animal is ready for insemination.

Estrus and menstruation
See also: Estrous cycle

Females of most mammal species advertise fertility to males with visual behavioral cues, pheromones, or both.[8] This period of advertised fertility is known as oestrus, "estrus" or heat.[8] In species that experience estrus, females are generally only receptive to copulation while they are in heat[8] (dolphins are an exception).[9] In the estrous cycles of most placental mammals, if no fertilization takes place, the uterus reabsorbs the endometrium. This breakdown of the endometrium without vaginal discharge is sometimes called covert menstruation.[10] Overt menstruation (where there is blood flow from the vagina) occurs primarily in humans and close evolutionary relatives such as chimpanzees.[2] Some species, such as domestic dogs, experience small amounts of vaginal bleeding while approaching heat;[11] this discharge has a different physiologic cause than menstruation.[12]

Concealed ovulation
See also: concealed ovulation

A few mammals do not experience obvious, visible signs of fertility (concealed ovulation). In humans, while women can learn to recognize their own level of fertility (fertility awareness), whether men can detect fertility in women is debated; recent studies have given conflicting results.[13][14]

Orangutans also lack visible signs of impending ovulation.[15] Also, it has been said that the extended estrus period of the bonobo (reproductive-age females are in heat for 75% of their menstrual cycle) [16] has a similar effect to the lack of a "heat" in human females.[17]

Evolution

Most female mammals have an estrous cycle, yet only ten primate species, four bats species, the elephant shrew, and one known species of spiny mouse have a menstrual cycle.[18][19] As these groups are not closely related, it is likely that four distinct evolutionary events have caused menstruation to arise.[20]

Many have questioned the evolution of overt menstruation in humans and related species, speculating on what advantage there could be to losing blood associated with dismantling the uterine lining rather than absorbing it, as most mammals do. The reason is likely related to differences in the ovulation process.

Most female placental mammals have a uterine lining that builds up when the animal begins ovulation, and later further increases in thickness and blood flow after a fertilized egg has successfully implanted. This final process of thickening is known as decidualization, and is usually triggered by hormones released by the embryo. In humans, decidualization happens spontaneously at the beginning of each menstrual cycle, triggered by hormonal signals from the mother's ovary. For this reason, the human uterine lining becomes fully thickened during each cycle as a defense to trophoblast penetrate of the endometrial wall [21], regardless of whether an egg becomes fertilized or successfully implants in the uterus. This produces more unneeded material per cycle than in non-menstruating mammals, which may explain why the extra material is not simply reabsorbed as done by those species. In essence, menstruating animals treat every estrous cycle as a possible pregnancy by thickening the protective layer around the endometrial wall, while non-menstruating placental mammals do not begin the pregnancy process until a fertilized egg has implanted in the uterine wall.

For this reason, it is speculated that menstruation is not a trait which provides any evolutionary advantage. Instead it is a side effect of spontaneous decidualization, which evolved in some placental mammals due to its advantages over non-spontaneous decidualization. Spontaneous decidualization allows for more maternal control in the maternal-fetal conflict by increasing selectivity over the implanted embryo.[20] This may be necessary in humans and other primates, due to the abnormally large number of genetic disorders in these species. Since most aneuploidy events result in stillbirth or miscarriage, there is an evolutionary advantage to ending the pregnancy early, rather than nurturing a fetus that will later miscarry. There is evidence to show that some abnormalities in the developing embryo can be detected by cells in the uterus. This triggers epigenetic changes that prevent formation of the placenta, leaving the fetus to die and be removed in the next menstruation.[22] This failsafe mode is not possible in species where decidualization is controlled by hormonal triggers from the embryo. This is sometimes referred to as the choosy uterus theory, and it is theorized that this positive outweighs the negative impacts of menstruation in species with high aneuploidy rates and hence a high number of 'doomed' embryos.


Phylogeny tree of menstruating and select non-menstruating mammals. Each color indicates a convergent evolutionary event: green, Primates; blue, Chiroptera; orange, Afrotheria; yellow, Rodentia.[20][23][24]

Animal estrous cycles

The female will ovulate spontaneously and be receptive to the male to be bred (express estrus) at regular biologically defined intervals. The female is receptive to males only while experiencing estrus.

For breeding livestock, there are a number of advantages to be gained by finding methods to induce ovulation on a planned schedule, and thus synchronize the estrus cycle between many female animals. If animals can be bred on the same schedule, it increases convenience for the livestock owner, since the young animals will be at the same stage of development. Also, if artificial insemination (AI) is used for breeding, the AI technician's time can be used more efficiently, by breeding several females at the same time. In order to induce estrus, a variety of techniques have been tried in recent years, involving both more natural, and more hormonal based methods.[25]. Different ways of injecting or feeding hormones to livestock are costly, and have variable success rates.[26]

Average length (days) of estrus and estrous cycles:[26]

SpeciesEstrusCycle
Mouse, rat0.54
Hamster14
Guinea pig0.516
Sheep217
Goat320
Cattle0.521
Pig221
Horse521
Elephant422
Red kangaroo335
Lion955
Dog760
Rabbit24
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See also

References
  1. Gras, Lyn, et al. "The incidence of chromosomal aneuploidy in stimulated and unstimulated (natural) uninseminated human oocytes." Human Reproduction 7.10 (1992): 1396-1401.
  2. Strassmann BI (June 1996). "The evolution of endometrial cycles and menstruation". The Quarterly Review of Biology. 71 (2): 181–220. doi:10.1086/419369. PMID 8693059.
  3. Bellofiore N, Cousins F, Temple-Smith P, Dickinson H, and Evans J (July 2018). "A missing piece: the spiny mouse and the puzzle of menstruating species". Journal of Molecular Endocrinology. 61 (1): R25–R41. doi:10.1530/JME-17-0278.
  4. Profet M (September 1993). "Menstruation as a defense against pathogens transported by sperm". The Quarterly Review of Biology. 68 (3): 335–86. doi:10.1086/418170. PMID 8210311.
  5. Martin RD (2007). "The evolution of human reproduction: a primatological perspective". American Journal of Physical Anthropology. Suppl 45: 59–84. doi:10.1002/ajpa.20734. PMID 18046752.
  6. Coutinho EM, Segal SJ (1999). Is menstruation obsolete?. Oxford University Press.
  7. Bischof P, Cohen M. "Course 4:Implantation" (PDF). European Society of Human Reproduction and Embryology. Archived from the original (PDF) on 2013-06-13. Retrieved 2018-12-04.
  8. "Estrus". Britannica Online. Retrieved 5 October 2008.
  9. Mikkelson DP (29 June 2007). "Buried Pleasure". Snopes.com. Retrieved 5 October 2008., which references:
    Diamond JM (1997). Why is sex fun?: the evolution of human sexuality. London: HarperCollins. ISBN 978-0-465-03127-6.
  10. Profet M (September 1993). "Menstruation as a defense against pathogens transported by sperm". The Quarterly Review of Biology. 68 (3): 335–86. doi:10.1086/418170. PMID 8210311.
  11. Senger PL (2012). Pathways to Pregnancy and Parturition. Redmon, OR: Current Conceptions, Inc. p. 146. ISBN 978-0-9657648-3-4.
  12. "Canine False Pregnancy and Female Reproduction". Mar Vista Animal Medical Center. 2 February 2008. Archived from the original on 15 October 2008. Retrieved 5 October 2008.
  13. Studies that found women are more attractive to men when fertile:
    Roberts SC, Havlicek J, Flegr J, Hruskova M, Little AC, Jones BC, Perrett DI, Petrie M (August 2004). "Female facial attractiveness increases during the fertile phase of the menstrual cycle". Proceedings. Biological Sciences. 271 Suppl 5 (Supp): S270–2. doi:10.1098/rsbl.2004.0174. PMC 1810066. PMID 15503991.
    Miller G, Tybur JM, Jordan BD (June 2007). "Ovulatory cycle effects on tip earnings by lap dancers: economic evidence for human estrus?" (PDF). Evolution and Human Behavior. 28 (6): 375–381. CiteSeerX 10.1.1.154.8176. doi:10.1016/j.evolhumbehav.2007.06.002. Retrieved 21 January 2008.
  14. Study that found male sexual behavior is not affected by female fertility:
    Bullivant SB, Sellergren SA, Stern K, Spencer NA, Jacob S, Mennella JA, McClintock MK (February 2004). "Women's sexual experience during the menstrual cycle: identification of the sexual phase by noninvasive measurement of luteinizing hormone". Journal of Sex Research. 41 (1): 82–93. doi:10.1080/00224490409552216. PMID 15216427.
  15. Knott C (2003). "Orangutans: Reproduction and Life History". Gunung Palung Orangutan Project. Harvard University. Archived from the original on April 21, 2008. Retrieved 5 October 2008.
  16. Lanting F, de Waal FB (1997). Bonobo: the forgotten ape. Berkeley: University of California Press. p. 107. ISBN 978-0-520-20535-2. Retrieved 5 September 2007.
  17. Stanford CB (March–April 2000). "The Brutal Ape vs. the Sexy Ape? The Make-Love-Not-War Ape". American Scientist. 88 (2): 110. doi:10.1511/2000.2.110.
  18. "Why do women menstruate?". ScienceBlogs. 2011. Archived from the original on 27 January 2013. Retrieved 15 January 2013.
  19. Bellofiore N, Ellery SJ, Mamrot J, Walker DW, Temple-Smith P, Dickinson H (January 2017). "First evidence of a menstruating rodent: the spiny mouse (Acomys cahirinus)". American Journal of Obstetrics and Gynecology. 216 (1): 40.e1–40.e11. doi:10.1016/j.ajog.2016.07.041. PMID 27503621.
  20. Emera D, Romero R, Wagner G (January 2012). "The evolution of menstruation: a new model for genetic assimilation: explaining molecular origins of maternal responses to fetal invasiveness". BioEssays. 34 (1): 26–35. doi:10.1002/bies.201100099. PMC 3528014. PMID 22057551.
  21. Haig (December 1993). "Genetic Conflicts in Human Pregnancy". The Quarterly Review of Biology. 68 (4): 495–532.
  22. "The 'choosy uterus': New insight into why embryos do not implant". medicalxpress.com. Retrieved 2020-01-26.
  23. Bellofiore N, Cousins F, Temple-Smith P, Dickinson H, Evans J (July 2018). "A missing piece: the spiny mouse and the puzzle of menstruating species". Journal of Molecular Endocrinology. 61 (1): R25–R41. doi:10.1530/jme-17-0278. PMID 29789322.
  24. Zhang X, Zhu C, Lin H, Yang Q, Ou Q, Li Y, Chen Z, Racey P, Zhang S, Wang H (August 2007). "Wild fulvous fruit bats (Rousettus leschenaulti) exhibit human-like menstrual cycle". Biology of Reproduction. 77 (2): 358–64. CiteSeerX 10.1.1.1013.9590. doi:10.1095/biolreprod.106.058958. PMID 17494915.
  25. Synchronized mating and lambing in spring-bred Merino sheep: the use of progestogen-impregnated intravaginal sponges and teaser rams (Met opsomming in Afrikaans) (Avec resume en francais) G. L. HUNTER, P. C. BELONJE and C. H. VAN NIEKERK, Department of Agricultural Technical Services, Stellenbosch, Agroanimalia 3,133-140 (1971)
  26. "Estrous". University of Wyoming. Retrieved September 15, 2011.
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