Parturition and placentophagy in baboons

Yellow Baboon (Papio cynocephalus) female with young
Wikimedia Commons

Two important papers just appeared on reproduction in baboons (Papio spp.). Natalia Schlabritz-Loutsevitch and co-authors (OA here) describe normal birth and pregnancy complications as observed in the laboratory. Their study was based on imaging (MRI, X-ray, ultrasound) and video recording of deliveries. 

I found it particularly fascinating to see the delivery process. When the baby's head emerges it is face upwards so looking directly at the mother (unlike in humans and chimpanzees where the head emerges face down). After cleaning the baby, the mother ignores it for several minutes and devotes all her attention to eating the placenta. Some of this can be seen in the delivery video (supplementary material here). 

Gesquiere and co-authors (here) summarize no less than 36 years of observations in free-ranging baboons, mainly yellow baboons (P. cynocephalus) from Amboseli in southern Kenya. Their focus is on what determines the interval between births. The main determinant was lactational amenorrhoea due to suppression of the ovarian cycle while the infant was breastfeeding. Once the baby was weaned, most females became pregnant again within 6-8 cycles.

There is an interesting parallel with human hunter-gatherers (previous post). Based on data from the !Kung people of South Africa, Roger Short (here) calculated that a woman in a hunter-gatherer society was pregnant for nearly four years of her life and spent 15 years in lactational amenorrhoea. As a consequence she endured menstrual cycles for rather less than four years. Short contrasted this with present day society where a woman might expect to have menstrual cycles for 35 years of her reproductive life.

Evolution of the decidua

In preparation for pregnancy, the endometrium undergoes a process called decidualization (previous post). This involves a change in the size, shape and properties of the connective tissue cells (stromal fibroblasts). Decidualization is a necessary prerequisite for implantation of the blastocyst and often occurs in response to an embryonic signal. In women, decidualization happens in response to a maternal signal in the second half of the menstrual cycle.

 

Decidua was present in the most recent common ancestor of placental
mammals but was lost in some lineages. Data from A. M. Mess and A. M. Carter

Based on a phylogenetic analysis (here), Andrea Mess and I concluded that decidualization was present in the most recent common ancestor of placental mammals (extant Eutheria). It was lost in some lineages, especially in those that evolved a non-invasive epitheliochorial placenta.

Gray Four-eyed Opossum (Philander opossum)
Wikimedia Commons CC-BY-3.0 (André de Souza Pereira)

How about marsupials, all of which have a yolk sac placenta? In most placentation is non-invasive and none has been shown to have a decidua. In the Gray Four-eyed Opossum (Philander opposum), however, there is penetration of the endometrium by trophoblast and traces of a primitive decidual reaction (here). This ties in quite nicely with a recent study (here) of gene expression in the endometrium of the Gray Short-tailed Opossum. This identified a population of endometrial stromal fibroblasts that expressed progesterone receptor and some transcription factors associated with human decidual cells. On the other hand, the fibroblasts did not express the decidual marker desmin or other transcription factors required for decidualization.

The authors of the latter paper are part of a consortium that just published an extensive analysis of gene expression by the endometrium across mammals (here). The study included a frog, chicken, lizard, monotreme (Duck-billed Platypus), marsupial (Gray Short-tailed Opossum), and seven different placental mammals. It identified a huge number of genes that were recruited during the evolution of pregnancy in mammals, including many that are associated with the decidualization process.

The main thrust of the new paper is the central role played in evolution by transposable elements. These were co-opted into regulatory elements that coordinate the endometrial progesterone response.

Menstruation in elephant shrews

Etendeka Round-eared Elephant Shrew or Sengi Macroscelides
micus. Image credit John P. Dumbacher
 

This post is prompted by the discovery in Namibia of a new species of elephant shrew or sengi, the smallest yet of the 19 species in the Order Macroscelidea. Elephant shrews are so named because of their mobile proboscis.





Midgestation conceptus of the Four-toed Elephant Shrew Petrodomus
tetradactylus. The embryo and fetal membranes are enclosed in the embryo
chamber by the decidua pseudocapsularis. Reproduced from
Oduor-Okelo et al. (here) (c) 2004 with permission from Elsevier

The report (here) mentions two pregnant females carrying one fetus in each horn. This suggests they may resemble other elephant shrews in that implantation of the blastocyst occurs in a preformed embryo chamber as shown above for Petrodumus tetradactylus. There is one such chamber in each horn. 

 

Should a female fail to become pregnant, the chamber is discarded in a process akin to menstruation. In most mammals transformation of the endometrial stroma to decidua occurs only following implantation. Exceptions are the catarrhine primates, including humans; if pregnancy does not ensue the decidua is shed together with blood and fluids (see previous post). In the 1940's, when human menstruation was poorly understood, Professor C. J. van der Horst of the University of Witwatersrand proposed using elephant shrews as a model. His suggestion was not followed as the establishment of a breeding colony of macaques at the Carnegie Institution of Washington provided a better alternative.

 

Placentation in elephant shrews was studied by van der Horst and others and more recently has been described by Dominic Oduor-Okelo (here and here). The placental disc has a labyrinth with a haemochorial structure and a spongy zone. In addition there is a paraplacenta. The allantoic sac is large and divided into four lobes. This last feature is a synapomorphy for the superordinal clade Afrotheria (discussed here).