The evolution of endometrial cycles and menstruation

Q Rev Biol. 1996 Jun;71(2):181-220. doi: 10.1086/419369.

Abstract

According to a recent hypothesis, menstruation evolved to protect the uterus and oviducts from sperm-borne pathogens by dislodging infected endometrial tissue and delivering immune cells to the uterine cavity. This hypothesis predicts the following: (1) uterine pathogens should be more prevalent before menses than after menses, (2) in the life histories of females, the timing of menstruation should track pathogen burden, and (3) in primates, the copiousness of menstruation should increase with the promiscuity of the breeding system. I tested these predictions and they were not upheld by the evidence. I propose the alternative hypothesis that the uterine endometrium is shed/resorbed whenever implantation fails because cyclical regression and renewal is energetically less costly than maintaining the endometrium in the metabolically active state required for implantation. In the regressed state, oxygen consumption (per mg protein/h) in human endometria declines nearly sevenfold. The cyclicity in endometrial oxygen consumption is one component of the whole body cyclicity in metabolic rate caused by the action of the ovarian steroids on both endometrial and nonendometrial tissue. Metabolic rate is at least 7% lower, on average, during the follicular phase than during the luteal phase in women, which signifies an estimated energy savings of 53 MJ over four cycles, or nearly six days worth of food. Thus the menstrual cycle revs up and revs down, economizing on the energy costs of reproduction. This economy is greatest during the nonbreeding season and other periods of amenorrhea when the endometrium remains in a regressed state and ovarian cycling is absent for a prolonged period of time. Twelve months of amenorrhea save an estimated 130 MJ, or the energy required by one woman for nearly half a month. By helping females to maintain body mass, energy economy will promote female fitness in any environment in which fecundity and survivorship is constrained by the food supply. Endometrial economy may be of ancient evolutionary origin because similar reproductive structures, such as the oviducts of lizards, also regress when a fertilized egg is unlikely to be present. Regression of the endometrium is usually accompanied by reabsorption, but in some species as much as one third of the endometrial and vascular tissue is shed as the menses. Rather than having an adaptive basis in ecology or behavior, variation in the degree of menstrual bleeding in primates shows a striking correlation with phylogeny. The endometrial microvasculature is designed to provide the blood supply to the endometrium and the placenta, and external bleeding appears to be a side effect of endometerial regression that arises when there is too much blood and other tissue for complete reabsorption. The copious bleeding of humans and chimps can be attributed to the large size of the uterus relative to adult female body size and to the design of the microvasculature in catarrhines.

Publication types

  • Review

MeSH terms

  • Adult
  • Animals
  • Biological Evolution*
  • Embryo Implantation
  • Endometrium / physiology*
  • Energy Metabolism
  • Estrogens / physiology
  • Female
  • Fertility
  • Humans
  • Menstrual Cycle / physiology*
  • Menstruation / physiology
  • Models, Biological
  • Ovary / physiology
  • Pan troglodytes
  • Placenta / physiology
  • Pregnancy
  • Primates
  • Reproduction

Substances

  • Estrogens