A placenta pioneer from Philadelphia

Newborn and afterbirth of six-banded armadillo
(Euphractus sexcinctus) from Chapman 1901

Some of the earliest studies of placenta in the United States were those of Henry C. Chapman published in Proceedings of the Academy of Natural Sciences of Philadelphia (available on JStor). His observations on the placenta of a six-banded armadillo (Euphractus sexcinctus) were published in 1901 and went unsurpassed for over a century. Importantly, Chapman noted that polyembryony, known from the more widely studied nine-banded armadillo (Dasypus novemcinctus), did not occur in Euphractus.

Fetal membranes of a kangaroo (Macropus giganteus).
Note the small allantois. From Chapman 1881

Chapman is notable for an early study of the fetal membranes of the Eastern grey kangaroo (Macropus giganteus). He noted that there was a large yolk sac but a relatively small allantois that did not form a placenta.

Zonary placenta of an African elephant (Loxodonta africana)
From Chapman c. 1880

Chapman got his armadillo and kangaroo specimens from the Philadelphia Zoo, but his African bush elephant (Loxodonta africana) placenta was from Cooper and Bailey’s London Circus. His was one of several early descriptions of elephant placentation, including a paper by Assheton (here), but there was then a hiatus until the classical work by Amoroso and Perry in 1964 (here). Based on the records of the elephant keeper, Chapman was able to estimate gestation to 650-655 days.

Henry Cadwalader Chapman (1845-1910)

Chapman came from a prominent Philadelphia family. His grandmother was a Biddle and her sister had married a Cadwalader, which may explain his middle name. He studied medicine then spent three years in Europe under Richard Owen in London and Alphonse Milne-Edwards in Paris.

Chapman’s work has been cited by Mossman, Amoroso, Wislocki and Enders (here), but is in danger of being forgotten. When the next paper on Euphractus appeared in 2012 (here), Chapman’s earlier contribution was not acknowledged.

Placentation in the Tasmanian bettong

Tasmanian bettong (Bettongia gaimardi cuniculus)
By JJ Harrison (CC BY-SA 3.0) via Wikimedia Commons
 

Now regarded as a subspecies of Eastern bettong (the mainland subspecies is extinct), the fetal membranes of this small kangaroo were described in 1930 by Theodore Thomson Flynn.

Trilaminar omphalopleure (vascular yolk sac) of Tasmanian bettong
From Flynn Proc Linn Soc NSW 1930; 55: 506-531

The yolk sac comprises a vascular portion (trilaminar omphalopleure) and a non-vascular portion (bilaminar omphalopleure). The sketch above shows trophoblast of the vascular yolk sac (troph) absorbing secretions from a uterine gland (gl ep). It is unclear whether there is exchange between the capillaries on the maternal (m cap) and fetal (foet cap) sides.

Bilaminar omphalopleure (non-vascular yolk sac) of Tasmanian bettongFrom Flynn Proc Linn Soc NSW 1930; 55: 506-531

Trophoblast of the non-vascular yolk sac (bilaminar omphalopleure) was implicated in the uptake of cellular material (cm) and red blood cells (haem). In current terminology (here) it is heterophagous.

Theodore Thomson Flynn (right) with his son the actor Errol Flynn

Theodore Thomson Flynn was a marine biologist and professor at the University of Tasmania. He named a fish Gibbonsia erroli after his son Errol Flynn the film actor.

Hobbits in the headlines again

Liang Bua, the cave where Homo floresiensis was found.
This image was originally posted to Flickr by Rosino (CC-BY-SA-2.0).

When a new hominin was described from Flores in Indonesia (here), it was quickly dubbed "hobbit" with reference to its small stature (1.1 m) and relatively large feet. Even more sensational, however, was the date of 15 thousand years ago (kya) based on charcoal from the same deposit. The implication was that the "hobbit" (Homo floresiensis) overlapped in time with our own species.

Yesterday my Twitter feed lit up with news of a paper (here) that drastically revised the age of these fossils to between 60-100 kya. Briefly there had been slippage of more recent material, including charcoal, into an eroded area where the bones were found. The new study used several methods to obtain the earlier date. Unlike in the original report, these included dating of the bones themselves.

Skull of Homo floresiensisThis image was originally posted to Flickr (CC-BY-SA-2.0).

The new dates match those of stone tools ranging from 50-190 kya. The most recent of those dates corresponds with the arrival of H. sapiens in the region, leading to conjecture that this caused the demise of the "hobbits."

There is a new flurry of speculation about the origin of this species. One idea (discussed here) is that it is derived from Homo erectus (previous post) and its small stature is an example of Island Dwarfism (as seen in pygmy elephants from Flores and pygmy hippopotami from Madagascar).

Flores lies East of the Wallace Line, a water barrier that separates the Southeast Asian and Australasian flora and fauna (previous post). It seems not to have presented a barrier to hominins. The enigmatic Denisovans also crossed the Wallace Line (previous post).

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.

 

  

  

Treasure houses under threat

The Field Museum Chicago
by Juanfibarra Wikimedia Commons CC BY 2.5

Museums house vast collections of specimens. For major museums of Natural History, these can be numbered in tens of millions. The specimens of greatest interest to embryologists will be in the wet collection and preserved as a rule in alcohol. Curating these specimens is an expensive business. When Chicago's Field Museum built a new Collections Resource Center the bill ran to $65 million and so stretched the budget that it resulted in cuts to museum staff (here).

Cross section through placental disc of a web-footed tenrec
(Limnogale mergulus) from Enders et al. (here). FMNH 165440

Now museum collections in the US are under further threat as the National Science Foundation has suspended its funding for the maintenance of biological research Collections (here). This is a matter of great concern.

Thanks to the Field Museum were able to describe the placenta from a rare specimen of an aquatic tenrec (above). We also used Field Museum specimens when reviewing the reproductive organs of bats (here).

Gravid uterus of a chimpanzee (Pan troglodytes) from the Hill Collection
currently housed at Museum für Naturkunde Berlin

Some museums house dedicated collections of embryological material. The J. P. Hill Collection is a good example and we have used it for several projects, including the first description of deep trophoblast invasion in a non-human primate (here).

The history of this collection is instructive. After Hill's death in 1954 it was stored in the attic of Dixon Boyd's house in Cambridge. It subsequently found what seemed to be a permanent home at the Hubrecht Laboratory in Utrecht. Together with the Hubrecht Collection it was eventually kept in a purpose built facility of a new building. With a change of director this space was seen as more suitable for -70 freezers and the future of the collection remained uncertain until it was removed to Berlin. The director subsequently became President of the Royal Netherlands Academy of Arts and Sciences! 

Genome of the spotted gar

Spotted gar (Lepisosteus oculatus)
Brian Gratwicke  CC BY 2.5 (Wikimedia Commons)

Not all bony fish are teleosts. Teleostei is an infraclass of ray-finned fish (Actinopterygii) with bichirs, sturgeons and gars (some 50 species) all basal to to the more numerous teleosts (some 30,000 species). The phylogeny of bony fishes has been largely resolved by Near et al. (open access).

Alligator gar (Atractosteus spatula) Moon Lake, Mississippi. March 1910, Photographer D. Franklin,
American Museum of Natural History (public domain)

 

Romer's Man and the Vertebrates did not make much of garpikes, but did include a great photo (shown above) of the largest species. My yellowing copy predates the genetic code yet alone genomics.

What we now know is that teleosts are characterized by the Teleost Gene Duplication (TGD). This event was followed by rapid sequence evolution that may explain their success as a group. It can, however, make it difficult to identify orthologs to tetrapod genes and frustrate interpretation of data obtained in zebra fish (Danio rerio). To provide a bridge, Braasch et al. have sequenced and have just published the genome of the spotted gar (open access).

To my knowledge no living species of the gar family is viviparous.

Placenta of the gray four-eyed opossum

The gray four-eyed opossum (Philander opossum) by André de Souza Pereira
Wikipedia Commons CC BY-SA 3.0

The gray four-eyed opossum (Philander opossum) is widely distributed in South and Central America. Its placentation has been described from animals caught on Barro Colorado Island in Panama (here).

Yolk sac of Philander opossum. The sinus terminalis marks the transition
between the avascular and vascular portions.
Courtesy of Dr. Allen C. Enders

As in the Virginia opossum, the yolk sac is comprised of avascular and vascular portions. The avascular part follows the contours of the uterine epithelium (at left in the figure). The vascular portion attaches to it (at right).

Semi-thin section of vascular yolk sac (at top) and fold in the uterine
wall (below) in Philander opossum.
Courtesy of Dr. Allen C. Enders

The study of Philander by Enders and Enders was the first to show invasive trophoblast in a marsupial. In the figure there is a fold of uterine wall with intact epithelium at left and right, but this has disappeared at the centre of the fold, which is occupied by large trophoblast cells. Subsequently invasive trophoblast has been described in another opossum (Monodelphis domestica) and in an Australian marsupial (Sminthopsis crassicaudata).

Photomontage of a section through one uterus of Philander opossum.
The two fetuses share a common yolk sac, but each has its own
allantoic sac one of which can be seen.
Courtesy of Dr. Allen C. Enders

An unusual feature in Philander is that two or more fetuses share a common yolk sac. However, each has its own allantoic sac. The allantois never makes contact with the trophoblast (it remains within the small exocoelom). It may serve as a receptacle for urine secreted by the mesonephros.