Placentation in the wildebeest

Blue Wildebeest (Connochaetes taurinus)

Photo by Muhammad Mahdi Karim (Wikimedia Commons)

In ruminants binucleate trophoblast cells (BNCs) migrate to and fuse with uterine epithelial cells to form a fetomaternal hybrid - either a syncytium or trinucleate cells. This remarkable mechanism was described some 40 years ago by Peter Wooding. The fusion is aided by a syncytin, the product of an endogenous retroviral gene (previous post).

Almost all the ruminants studied hitherto have trinucleate cells. A fetomaternal syncytium is formed in the basal tragulids (chevrotains), which have a diffuse placenta without cotyledons. The other exception hitherto is syncytium formation in sheep and goats.

Binucleate trophoblast cell of bovine placenta from Benirschke

Now Wooding et al. (here) have undertaken to survey a wide range of ruminants including a chevrotain (Tragulidae), 8 bovids (Bovidae), 8 deer(Cervidae), the pronghorn (Antilocapridae) and a giraffe (Giraffidae). Only the musk deer (Moschidae) are missing.

Almost all the pecoran ruminants studied had trinucleate cells. Exceptions were the sheep and the wildebeest (Connochaetes taurinus). This is a new and highly interesting observation.

Three groups of bovids, classified as Tribes by Groves and Grubb (previous post) and Subfamilies by Wilson and Reeder share a common ancester (here and here). These are Alcelaphini, Hippotragini and Caprini. The first includes the wildebeest and the last sheep and goat. So it is likely that the most recent common ancestor (MRCA) of sheep and goats and the wildebeest had a fetomaternal syncytrium.  

To summarize. The basal Tragulidae have fusion of BNCs and maternal epithelium to form a syncytium. The trinucleate cell replaced this in the MRCA of pecoran ruminants (those with cotyledons). Then a fetomaternal syncytium reappeared in the MRCA of wildebeest and sheep and goats. 

To test this hypothesis it would be useful to have studies of the third tribe Hippotragini, i.e. an oryx, the roan and sable antelopes or the bluebuck.

Placentation in the pronghorn (Antilocapra americana)

Pregnant uterus of the pronghorn. Note the fused amnions in the corpus uteri.
From Wislocki and Fawcett Bull Museum Comp Zool Harvard 1949; 101: 545-559.

The pronghorn is the sole survivor of a North American lineage of ruminants. (Antilocapridae). Its placenta was described by Wislocki and Fawcett (full text available at Biodiversity Heritage Library). It is polycotyledonary and epitheliochorial. The chorionic villi show a pattern of branching distinct from that of other ruminants. Interestingly, Wislocki and Fawcett described and illustrated binucleate giant cells. The amnion is larger than the allantoic sac. There is a fetus in each horn of the bicornuate uterus and the two amnions fuse back to back in the region of the uterine corpus.

Female pronghorn in Wyoming.
Photo by Yathin S Krishnappa Wikimedia Commons CC BY-SA 3.0

The pronghorn bears a superficial resemblance to an antelope, but this is the result of convergent evolution. Pronghorns (Antilocapridae) share a common ancestor with the giraffe and okapi (Giraffidae) whereas Bovidae (including antelopes) is a distinct lineage. The evolution of placentation in even-toed ungulates has been traced by Andrea Mess and Karl Klisch (here).

Given the taxonomic position of the pronghorn, a recent study has examined glycosylation at the fetal maternal interface and compared it with the giraffe, okapi and various bovids (here). The expression of pregnancy-associated glycoproteins (PAGs) in binucleate trophoblast cells was also examined.

Embryo competition in the pronghorn: penetration of the membranes
of a distal embryo by the necrotic tip of a proximal embryo.
From O'Gara Amer J Anat 1969; 125: 217-232. 

Several authors have noted that the number of corpora lutea exceeds the number of fetuses (usually twins). O'Gara (reference here) found that some reduction occurred during the phase of blastocyst elongation. Often two blastocysts managed to implant in the same horn. However, the membranes of the proximal embryo (nearest the uterine body) formed a necrotic tip. As the conceptus grew, this tip pierced the chorion and allantois of the distal embryo, resulting in its death. As O'Gara wrote, "The phenomenom of the necrotic tip acting as a lethal weapon is apparently unique to the pronghorn."