Reproductive ecology and the endometrium: Physiology, variation, and new directions

Abstract

Endometrial function is often overlooked in the study of fertility in reproductive ecology, but it is crucial to implantation and the support of a successful pregnancy. Human female reproductive physiology can handle substantial energy demands that include the production of fecund cycles, ovulation, fertilization, placentation, a 9-month gestation, and often several years of lactation. The particular morphology of the human endometrium as well as our relative copiousness of menstruation and large neonatal size suggests that endometrial function has more resources allocated to it than many other primates. The human endometrium has a particularly invasive kind of hemochorial placentation and trophoblast that maximizes surface area and maternalfetal contact, yet these processes are actually less efficient than the placentation of some of our primate relatives. The human endometrium and its associated processes appear to prioritize maximizing the transmission of oxygen and glucose to the fetus over efficiency and protection of maternal resources. Ovarian function controls many aspects of endometrial function and thus variation in the endometrium is often a reflection of ecological factors that impact the ovaries. However, preliminary evidence and literature from populations of different reproductive states, ages and pathologies also suggests that ecological stress plays a role in endometrial variation, different from or even independent of ovarian function. Immune stress and psychosocial stress appear to play some role in the endometrium's ability to carry a fetus through the mechanism of inflammation. Thus, within reproductive ecology we should move towards a model of women's fecundity and fertility that includes many components of ecological stress and their effects not only on the ovaries, but on processes related to endometrial function. Greater attention on the endometrium may aid in unraveling several issues in hominoid and specifically human evolutionary biology: a low implantation rate, high rates of early pregnancy loss, prenatal investment in singletons but postnatal support of several dependent offspring at once, and higher rate of reproductive and pregnancy-related pathology compared to other primates, ranging from endometriosis to preeclampsia. The study of the endometrium may also complicate some of these issues, as it raises the question of why humans have a maximally invasive placentation method and yet slow fetal growth rates. In this review, I will describe endometrial physiology, methods of measurement, variation, and some of the ecological variables that likely produce variation and pregnancy losses to demonstrate the necessity of further study. I propose several basic avenues of study that leave room for testable hypotheses in the field of reproductive ecology. And finally, I describe the potential of this work not just in reproductive ecology, but in the resolution of broader women's health issues. Yrbk Phys Anthropol 52: 137-154, 2009.

Perfluoroalkyl substances and ovarian hormone concentrations in naturally cycling women

“…If women with higher ovarian hormone levels tend to have a more proliferative endometrial lining (98) and by extension, heavier, more regular menstrual bleeding, then their lower levels of PFOS and PFOSA may be attributable to greater clearance in menstrual blood (91, 99, 100). Indeed, in NHANES, levels of multiple PFASs were higher in post-menopausal women than premenopausal, and highest in women with hysterectomies (43, 101), suggesting that menstrual bleeding may be a major route of clearance of PFASs.…”

Progesterone action in breast, uterine, and ovarian cancers

“…Unlike most mammals, the uterine endometrium of human and some non-human primates undergoes cyclical monthly changes that result in the growth, angiogenesis and differentiation of the functional (proliferative) endometrium (Clancy 2009; Ramsey, et al 1976). Shifts in the synthesis and secretion of the ovarian steroids, estrogen and progesterone, during this menstrual cycle serve as the principal hormonal drivers for these changes.…”

The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset

“…With respect to foetal biology, placentation is more invasive (haemochorial) in simian primates (monkeys, apes, humans) than in rodents; that is, the feto-placental tissues are bathed directly in maternal blood without an intervening cellular barrier (Clancy 2009). It has been demonstrated that fatty acid (but not protein or carbohydrate) transfer from the mother to the foetus is greater in species with more invasive placentation (Elliot and Crespi 2008) and potentially, therefore, increases in glucocorticoid and other stress factor levels in the maternal circulation could also lead to more marked increases in these factors in the foetal circulation in species with more invasive placentation.…”