Congratulations Hiroaki Soma

Professor Hiroaki Soma (at left) recipient of the 2018
IFPA Senior Award

It is a pleasure to record that my good friend and colleague Hiroaki Soma received the Senior Award of the International Federation of Placenta Associations at their recent meeting in Tokyo.

In his address, Professor Soma looked back over 60 years of research including important clinical work on gestational trophoblastic disease in Japan and placental lesions associated with pregnancy at high altitude in Nepal.

In addition, he gave valuable insights about comparative placentation. The range of mammals included chinchilla, giant panda. Japanese serow, sloth, chimpanzee, elephant, manatee and hyrax. As if this were not enough, Professor Soma also presented his research on pregnancy in sharks and rays conducted at the Churaumi Aquarium in Okinawa. 

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.

From antelope placenta to the chi square distribution

The Four-horned Antelope (Tetracerus quadricornis)
Philip Sclater The Book of Antelopes 1894

Despite its appearance, this Indian species is not a true antelope, but belongs to the subfamily Bovinae. Its placenta was described in 1884 by Raphael Weldon then a Scholar of St John's College, Cambridge.

Gravid uterus of the Four-horned Antelope
Weldon Proc Zool Soc London 1884

There was a fetus in each horn and Weldon was struck by the relative paucity of placentomes (30 and 22, respectively).

One extremity of the chorion of the Four-horned Antelope
Weldon Proc Zool Soc London 1884 

Weldon thought the interplacentomal regions resembled the diffuse placenta of the pig. This may have been overinterpretation. There seem to be no subsequent descriptions of placentation in this species.

The Nilgai (Boselaphus tragocamelus)
Rufus46 (Wikimedia Commons) CC BY-SA 3.0

Together with the Nilgai, the Four-horned Antelope forms its own tribe. Benirschki examined a couple of Nilgai placentas (here). He did not find an unusual number of cotyledons but remarked they were not as neatly arranged in rows as in other species. So perhaps Weldon was on to something.

Raphael Weldon is not remembered for his placental research. He became a marine biologist and was professor of Zoology first at University College London then at Oxford. At UCL he collaborated with the mathematician Karl Pearson and founded the science of biometrics. Famously, he rolled a set of 12 dice no fewer than 26,306 times. The results showed a bias towards fives and sixes (more here). These data were used by Karl Pearson in the latter's seminal paper on the chi-square statistic.

Placentation in bovids: can we learn more?

Princeton University Press 2016 ISBN-13: 9780691167176

Field guide or doorstopper? Just published as a Princeton Field Guide, this tome runs to 664 pages and weighs 1.3 kg. It aims to be, "The first comprehensive field guide to all 279 bovid species." Where did that total come from when Mammal Species of the World recognizes half the number?


Johns Hopkins University Press 2011 ISBN-13: 978-1421400938

The answer is the above book on ungulates (hoofed mammals) with a revised taxonomy based on the authors' Phylogenetic Species Concept (PSC). A useful comparison between old and new species can be found at the ultimateungulate site. 

Ungulate Taxonomy was criticised by Frank E. Zachos and colleagues both in a letter to Nature (here) and in a detailed critique (here). They argued that splitting of species was a worrying trend with unfortunate implications for conservation efforts.

Bovid placentation

I bought both these books because bovid placentation deserves further study. Two major clades are recognized. Bovinae include domestic cattle (Bos taurus) and the zebu (B. indicus) - the latter was raised to species status by Groves and Grubb, which should please my Brazilian colleagues.

Antilopinae is less well studied although it does include domestic sheep (Ovis aries). A large amount of antelope material is available in The Harland W. Mossman Collection together with detailed field notes by the principal collector Archie S. Mossman.

Placenta of a klipspringer (Oreotragus oreotragus) with a binucleate cell
From Comparative Placentation courtesy of Dr. Kurt Benirschke

There is much to be done. And which of the rival terminologies should we use? I chose this rather fuzzy image of a klipspringer because Groves and Grubb chose to split it into no less than 11 species. Zachos et al. call this, "a prime example of rash taxonomic conclusions derived from inappropriate data." Even if their judgement is too harsh, the fact remains that this San Diego Zoo specimen cannot be assigned with confidence to any one of those  11 species. We might be on better ground with the Mossman material as it was collected in the wild at known localities and many of the "new" species have clearly defined (often restricted) ranges.

Placentome of a sable antelope (Hippotragus niger)
From Comparative Placentation courtesy of Dr. Kurt Benirschke

Hradecky wrote several papers on placentation in antelopes based mainly on the Mossman material and partly on specimens supplied by Benirschke (e.g. here). A set of his slides is in the Mossman Collection and some reproduced on the Benirschke web site.
 

Handbook of the Mammals of the World

PSC may be a valid taxonomic approach inasmuch as the premisses are defined and understood by experts. But there was renewed controversy when the Groves and Grubb taxonomy was incorporated in Volume 2 of Handbook of the Mammals of the World. Heller et al. (here) criticised PSC and concluded, "Conveying the message to the public that global diversity is on the decrease ... is unnecessarily confounded when the number of bovid species has just doubled without sufficient justification."

Perhaps the same criticism could be levelled at the new field guide. It does, however, have the virtue of supplying an illustrated version of Groves and Grubb - a book that was strangely lacking in pictures (as noted here). Trophy Hunters will find it a useful aid to bagging yet more species.