Placentation in a marmot: the woodchuck

Woodchuck or groundhog (Marmota monax)
CC Wikimedia Commons

Not much has been written about placentation in squirrels and other sciuromorph rodents - at least in comparison to myomorphs (e.g. mouse, hamster) and hystricomorphs (e.g. guinea pig, capybara). Marmots belong with chipmunks and ground squirrels in the Tribe Marmotini. The most complete description is for the thirteen-lined ground squirrel (Ictidomys tridecemlineatus) (Mossman & Weisfeldt Am J Anat 1939;64:59-109). It was based largely on specimens collected a century ago by Thomas George Lee (background here).

Interhaemal region in the labyrinth of a woodchuck placenta
Marmota monax Courtesy of Dr. Allen C. Enders

The woodchuck has a labyrinthine, haemochorial placenta. In the above section the large channels with maternal red cells are lined by syncytiotrophoblast. A fetal capillary is seen to the right.

Early Development of the placenta in the Colorado chipmunk
Tamias quadrivittatus Courtesy of Dr. Allen C. Enders

There are several ways to make a haemochorial placenta (discussed here). Squirrels go through a transient endotheliochorial phase. The figure is from a chipmunk and shows a maternal capillary in which part of the endothelium has been replaced by syncytiotrophoblast whilst two endothelial cells remain intact (further figures here). In the first instance this creates the equivalent of the spongy zone found in other rodent placentas.

Later the fetal mesoderm grows into the trophoblast bringing with it the fetal capillaries. To start with the outgrowths are fingerlike (villi) as can be seen in a recent publication on the woodchuck (here). Nearer term, however, the labyrinth occupies most of the depth of the placenta. The spongy zone is then very thin and occupied by syncytiotrophoblast with clumps of nuclei as well as mononucleate giant cells (Dr. Allen C. Enders, personal communication).

Syncytins are endogenous retrovirus envelope genes (previous post). Two occur in murid rodents and another in South American hystricomorphs. Now a search of the genome of the thirteen-lined ground squirrel has turned up several candidates and further work in the woodchuck has shown one of them to be a bona fide syncytin. By in situ hybridization the gene was not expressed in the labyrinth but rather in the part of the spongy zone that had yet to be reached by the fetal vessels.

Placental gas exchange in ground squirrels

Golden-mantled ground squirrel (Callospermophilus lateralis)

(Wikipedia Commons)

Fetal blood tends to have a higher oxygen affinity than maternal blood. This aids oxygen transfer across the placenta. Some mammals (human, sheep) have a special fetal hemoglobin. In many others, hemoglobin is the same in fetus and mother, but in fetal blood it has increased affinity for oxygen because the red blood cells have a low content of DPG (here). This is the case in the few rodents studied so far.

Ground squirrels cannot use this trick. A new study (here) found that even adults have hemoglobin of high oxygen affinity and there is no effect of raising or lowering DPG.

Placenta of the golden-mantled ground squirrel from Carter and Enders (here)

© Carter and Enders 2004; Licensee Biomed Central Ltd.

So is oxygen transfer across the placenta of ground squirrels likely to be less efficient than, say, in a rat? Probably not. The same study established that an unusually large Bohr effect (defined here) aids unloading of oxygen to the tissues of ground squirrels. In any placenta there is a double Bohr effect because, as fetal blood takes up oxygen, it unloads carbon dioxide, while the opposite occurs in the maternal blood (discussed in detail here).

The new study concerns ground squirrels living at low and high altitude. The authors speculate that hemoglobin evolved to meet the demands of their fossorial life style. This in turn made it easier to expand into mountainous habitats. They did not consider the possible impact on reproduction - but perhaps they should.