The evolution of menstruation: A new model for genetic assimilation

Abstract

Why do humans menstruate while most mammals do not? Here, we present our answer to this long-debated question, arguing that (i) menstruation occurs as a mechanistic consequence of hormone-induced differentiation of the endometrium (referred to as spontaneous decidualization, or SD); (ii) SD evolved because of maternal-fetal conflict; and (iii) SD evolved by genetic assimilation of the decidualization reaction, which is induced by the fetus in non-menstruating species. The idea that menstruation occurs as a consequence of SD has been proposed in the past, but here we present a novel hypothesis on how SD evolved. We argue that decidualization became genetically stabilized in menstruating lineages, allowing females to prepare for pregnancy without any signal from the fetus. We present three models for the evolution of SD by genetic assimilation, based on recent advances in our understanding of the mechanisms of endometrial differentiation and implantation. Testing these models will ultimately shed light on the evolutionary significance of menstruation, as well as on the etiology of human reproductive disorders like endometriosis and recurrent pregnancy loss.

How Evolution of the Human Brain Shaped Women’s Sexual and Reproductive Health

“…The decidua will be useful if there is a pregnancy, but otherwise it had to be shed by the monthly menstruation. 22 …”

Aberrant expression and localization of deoxyribonucleic acid methyltransferase 3B in endometriotic stromal cells

“…However, in humans and menstruating primates decidualization is initiated in response to ovarian hormones independently of an implanting blastocyst (2). Full differentiation and maintenance of the decidua is contingent upon pregnancy, since the absence of a conceptus provokes shedding of the pre-decidualized endometrial layer and menstruation, and it has been suggested that the evolution of spontaneous decidualization necessitated menstruation (3). This intriguing observation led us to propose that the gene regulatory pathways that coordinate spontaneous decidualization in menstruating primates are the key pathways dysregulated in endometriosis (4).…”

Meaningful menstruation

“…More accurately, they focused on ''spontaneous'' decidualization, a process that precedes the shedding of the endometrium in all known menstruating species (i.e. higher primates, some bats, and the elephant shrew) [1].…”