Mammal Diversity Database



Zebu cattle (Bos taurus indicus)
Agricultural Research Service (USDA) Public Domain

How many species of mammals are there? That is the appropriate title of an article (OA here) accompanying the launch of the American Society of Mammalogy's new Mammal Diversity Database (here).


The answer is 6495 species and counting. Compared to Wilson & Reeder Mammal Species of the World (MSW3), which has its own database (here), that is an increase of 1250 in 13 years.


The authors of ASM MDD have erred in favour of the splitters. In particular, acceptance of the taxonomy of Groves & Grubb for Artiodactyla and Perissodactyla (previous post) will raise eyebrows. In anticipation they write, "inclusion of the taxonomy of Groves and Grubb (2011) in the MDD ensures that these taxa are vetted by the greater mammalogical community."


I note, however, that unlike Castello (previous post), they list the zebu as a subspecies of Bos taurus. Important because this species is a focus in research on bovine placentation and reproduction in places like Brazil.


I found the new MDD more difficult to navigate than MSW3. For example, if you enter a higher taxon than genus you get all the entries in that taxon rather than any definition of the Family or Order itself.


As far as I can see there is no possibility to search for synonyms as on MSW3. I have found this search function of MSW3 enormously valuable when delving into the older literature on placentation. Similarly there is little information about subspecies names.


Some choices of terminology meet my approval. They drop Cetartiodactyla in favour of Artiodactyla (whales and their kin are nested within even toed ungulates). Inevitably they retain Afrosoricida for the order that includes tenrecs, otter shrews and golden moles (a really unfortunate name as African shrews are numerous and belong to an entirely different clade).


Most regrettaby, however, they retain Infraclass Placentalia for eutherians. This unfortunate term was introduced by McKenna & Bell and I have ranted about it before (previous post). It has caused countless confusion and the vernacular "placentals" or even "placental mammals" can mislead the unwary to believe marsupials are without placentation. Prothero among them (previous post).

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."

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.