Placenta Atlas Tool (PAT)

NICHD have just launched this tool to aid pregnancy research. It promises to be of great value (found here).

Those interested in comparative placentation should go to Explore Images and use the Species filter. This brings up a list that may include your favourite mammal. Click on that and you will get a menu of large icons, although only after a further click can you be sure what they represent (room for improvement here).

The images are fully annotated with original figure legends plus additional context from the source paper.

Open Access appears to be a prerequisite for images to be selected as they link to the Open-i resource of the U. S. National Library of Medicine. 

Aye-aye captain of its own raft

An aye-aye (Daubentonia madagascariensis) foraging
Joseph Wolf c. 1863 Wikipedia Commons (public domain)

We are used to molecular data shaping our view of evolution, so it is all the more delightful when a morphological study shakes the mammalian tree.  The pleasure is no less for it involving that strange Malagasy primate the aye-aye (Daubentonia madagascariensis).

It is widely accepted that Madagascar was colonized by mammals rafting across the Mozambique Strait (see previous post). The lemurs (Lemuriformes) and the aye-aye (within its own Infraorder Chiromyiformes) have hitherto been thought to be descended from a single founder.

New tree for strepsirrhine primates from Gunnel et al. 
Nature Communications 2018 (here) CC

Now a study in Nature Communications paves the way to a new scenario. The historical background is interesting. George Gaylord Simpson (a proponent of the rafting hypothesis) once proposed a new fossil species of strepsirrhine primate Propotto leakeyi from the early Miocene of Kenya. Subsequently this was reinterpreted as a fruit bat. Now Gunnell and co-authors have unearthed the specimens from the National Museums of Kenya and compared the morphology (especially the dentition) both to the aye-aye and to Plesiopithecus teras from a late Eocene site in Egypt.

Firstly, they show Simpson was right about Propotto. Secondly, they construct a tree (combining morphological and molecular data) showing the split between Lemuriformes and Chiromyiformes occurred in the Eocene. Thirdly, it is most parsimonious to assume two separate rafting events with the ancestor of the aye-aye drifting to Madagascar on its own raft. Finally, both rafting events are likely to have occurred in the Miocene, which explains the lack of fossils of earlier date.

Placentation in the aye-aye

Allantochorion of the aye-aye. From Hill & Burne 1922 (here)

Milne-Edwards briefly described the placenta of the aye-aye (C R Acad Sci 1884), but the first complete account is by Hill and Burne (here). They described the villous nature of the allantochorion and the presence of chorionic vesicles. This contributed to Hill's later characterisation of the "lemuroid stage" of placentation where the placenta is diffuse, non-deciduate and epitheliochorial (reviewed here).

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 lizards and a new syncytin

The South American skink Mabuya mabouya 

Mark Stevens from Warrington, UK CC BY 2.0

Viviparity is common in lizards and some have evolved quite complex placentas. One of the first to be studied was Chalcides chalcides. Daniel Blackburn, Luana Paulesu and others have just written an interesting historical account of the 1891 paper by Giacomini (here).  

Placentome and paraplacentomal region in Mabuya sp.

From Cornelis et al. PNAS 2017 (here)

An even more complex placenta is found in South American species of the genus Mabuya. Martha Ramirez-Pinilla, a reproductive biologist from Colombia, has authored several papers on Mabuya placenta (e.g. here). Now she has joined forces with the group at Gustave Roussy in Paris to look for syncytins (here).

As explained in previous posts (e.g. here), syncytins are the products of endogenous retroviral genes. The envelope (env) genes of retroviruses function to promote fusion of the viral membrane with the plasma membrane of a host cell. Syncytins are derived from env genes and are expressed in the placenta, where they promote fusion of cytotrophoblasts with the syncytiotrophoblast. Hitherto they have been identified in six orders of eutherian mammals and in one marsupial (previous post).

Cornelis et al. first determined the transcriptome of Mabuya placenta and identified four env genes. One of these (named Mab-Env1) was highly expressed in placenta and with the highest expression of RNA and protein occurring at the fetal-maternal interface including in a maternal syncytial layer. Importantly, Mab-Env1 was fusogenic in an ex vivo assay, which is an essential criterion for designating the protein as a syncytin. The receptor for Mab-Env1 was also identified in this study. 

Tree shrews move from branch to branch

Species tree by three coalescent-based approaches
from Esselstyn et al 2017 © The Author 2017

In an heroic effort to resolve some of the difficult nodes in the mammalian tree, Esselstyn et al. used data from published genomes and added new data for a total of 100 mammals. Focussing on ultraconserved elements, they analysed all this by a battery of techniques, These included the classical maximum likelihood (ML) on concatenated data and three coalescent-based approaches. How did they do?

The first problem was to resolve the root of the eutherian tree. Here they did rather well. Both the ML tree and two of the coalescent-based methods gave strong support to the Atlantogenata hypothesis, i.e. a sister relationship between Afrotheria (elephants, dugongs, tenrecs and hyraxes) and Xenarthra (sloths and armadillos) with a common ancestor basal to Boreoeutheria (all other eutherian mammals).

South American Tapir (Tapirus terrestris)

Photo by Bernard Dupont CC BY-SA 2.0

They did almost as well with the second problem: the sister group to horses, rhinos and tapirs (Perissodactyla). In most analyses the found Cetartiodactyla (cetaceans and even-toed ungulates) as sister to Perissodactyla. However, they could not rule out one of the alternative hypotheses, which had bats (Chiroptera) as the sister group.

Whereas horses and cetartiodactyls (including ruminants, pigs, dolphins) all have epitheliochorial placentation, no bat does, so I am happy with their majority finding!

Pen-tailed tree shrew (Ptilocercus lowii)

From Wolf 1848 via Wikipedia Commons

On the third thorny problem the exercise failed. Tree shrews used to be thought the closest relatives to primates but have been toppled from this position in favour of colugos (previous post). Because some previous studies did not even include colugos, the present authors sought a remedy in including two colugos and three tree shrews, including the pen-tailed tree shrew above. The hope was that high taxon coverage would give a sounder result. But they were forced to conclude that placement remains uncertain. Tree shrews may be sister to rodents and lagomorphs (Glires) or to colugos plus primates (Primatomorpha).

Fortunately they could confirm colugos as sister to primates, which was the basis for my recent paper with Andrea Mess on the evolution from labyrinthine to villous placentation (here).

Marsupial and eutherian placentation

Placenta of the tammar wallaby showing the bilaminar (BOM)
and trilaminar (TOM) omphalopleure. From Guernsey et al.
eLife 2017 CC The Authors

A brand new paper compares the transcriptomes of marsupial (tammar) and eutherian (mouse and human) placentas and mammary glands (here). It confirms that marsupials have fully functional placentas expressing many of the same genes as eutherian ones.

There is evidence for a division of function between the two parts of the yolk sac placenta, with the nonvascular part (BOM) being responsible for uptake and metabolism of nutrients and the vascular part (TOM) for respiration. I am not sure how much oxygen the tiny marsupial embryo needs. Perhaps the TOM is more important for removing CO₂ and regulating the acid-base balance of the embryo. The tammar has an embryonic-type hemoglobin more capable of sequestering oxygen (protecting the embryo from reactive oxygen species) than transporting it to tissues.

A fascinating detail is that the yolk sac endoderm of the tammar has assumed functions, especially to do with trafficking of nutrients, that in eutherians are served by trophoblast.

Genes expressed in mammary gland and placenta
of marsupials and eutherians. From Guernsey et al.
eLife 2017 CC The Authors

Because much of development in the wallaby is supported by lactation, it is interesting to find considerable overlap in the transcriptomes of marsupial mammary gland and eutherian placenta.

My only criticism of this paper would be: the mouse has a yolk sac that supports early embryonic development and continues to function alongside the placenta right up to term. Perhaps the authors could not identify a data set on mouse yolk sac transcriptome, but they should have referenced the eutherian yolk sac in their discussion. An interesting theory by Claudia Freyer et al. (here) is that the stem species of therians (marsupials and eutherians) had both types of placentation.

For additional remarks on this paper see Nature News and Comments (here).

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 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."

Carnegie Collection of human embryos

Carnegie embryo 8171. Early lacunar stage (Stage 5b)
Courtesy of Dr. Allen C. Enders

An important source for human embryology, including implantation and formation of the placenta, is the Carnegie Collection now housed at the Human Developmental Anatomy Center in Washington D.C. The core of this collection is the carefully dated series of embryos first described by Hertig, Rock and Adams (here).

The Virtual Human Embryo is an online ressource based on the serially sectioned embryos in this collection and includes 3D reconstructions. It covers all 23 Carnegie stages in the first 8 weeks of embryonic development and cannot be too highly recommended.

Carnegie Embryo 7801. Showing extraembryonic coelom (eec)
and secondary yolk sac (sys) (Stage 6)
Courtesy of Dr.Allen C. Enders

Now a group in Amsterdam has used the Carnegie Collection to develop an additional annotated digital atlas of human development (described here). They also utilized material from the Boyd Collection at the Centre for Trophoblast Research in Cambridge.

They make two claims. First that representations in textbooks have become increasingly schematic. This is demonstrably true. Second that the descriptions in standard texts are often based on extrapolation to humans from animal models. It is hard to assess if the latter truly is the case. For example Human Embryology by Hamilton, Boyd and Mossman (previous post) was based on the human embryos in the possession of the three authors. In Germany there was a strong tradition to cover the embryology of all vertebrates, concluding with the human, exemplified by Dietrich Starck's Embryologie.

In physiology, on the other hand, animal data often are presented as if they were human. One example concerns oxygen tensions in various parts of the fetal circulation. Pretty much every textbook of physiology has a large illustration of the fetal circulation with data obtained in sheep by Dawes, Mott and Widdicombe. The figure legends often fail to acknowledge the source or the species or both.

Insectivores endemic to the Caribbean

Puerto Rican Nesophontes (N. edithae)
Reconstruction by Jennifer Garcia CC BY SA 3.0

The Caribbean is home to two endemic families of insectivores. The Nesophontidae are recently extinct. Their demise is attributed to the introduction of rats by Spanish Explorers though some believe the genus survived into the 20th Century.

To establish their phylogenetic position, scientists recently extracted DNA from a specimen preserved in an ancient owl pellet (here). This was no mean feat as the specimen was 750-years-old and DNA degrades rapidly in the tropics.



Hispaniolan Solenodon (S. paradoxus)
Biodiversity Heritage Library CC BY 2.0

The main finding was that Nesophontes shares a common ancestor with Solenodon. There are two species of this insectivore both listed as threatened by IUCN. A common origin had not been predicted on anatomical grounds not least because Nesophontes and Solenodon have different patterns of tooth occlusion (here). Together these families represent the oldest branch of the insectivores (Order Lipotyphla).

Placenta of Solenodon paradoxus
Wislocki (1940)

Despite its rarity, the placentation of S. paradoxus has been described (here) and we later compared it with that of other insectivores (here). Interesting features are remnants of capsular decidua, elaborately branched yolk sac villi and a sheath that superficially resembles that of crociduran shrews.

Wombs with a view

ISBN 978-3-319-23567-7

"Illustrations of the Gravid Uterus from the Renaissance through the Nineteenth Century," compiled by Lawrence D. Longo and Lawrence P. Reynolds.

This book contains several iconic images and many that are less well known. Each with a text about the author, artist and engraver as well as an analysis of the influence of the book on contemporary science and midwifery.

Great pains have been taken with reproduction of the images. No doubt many were taken from rare books in Larry Longo's own library. It is a pity he did not live to see the result in print (previous post).

Afterbirth of the sheep with four neat rows of cotyledons
From Girolamo Fabrizio De Formato Foetu 1604

There are plenty of images of the placenta including a few from animals. Anatomists who had dissected the gravid uteri of ruminants and dogs sometimes represented human placenta as cotyledonary or zonary in shape.

I am enjoying this book. It is a pity that the publisher (Springer Nature) did not employ a copy editor. There are many more typos than might be expected in a work of such high quality.

Tidying up the tenrecs

Dobson's shrew tenrec (Nesogale dobsoni)
Photo (C) Peter J. Stephenson

A fresh phylogenetic analysis (here) based on sequence data from all living tenrecs and one otter shrew allows a re-evaluation of tenrec systematics.

The study confirmed the web-footed tenrec (Limnogale mergulus) is nested in the genus Microgale and should henceforth be referred to as M. mergulus.

However, the authors also suggest resurrecting the generic name Nesogale for two species hitherto placed in Microgale. These are Dobson's shrew tenrec (N. dobsoni) and Talazaci's shrew tenrec (N. talazaci). Support for this included a 4-codon deletion shared only by these two species and a separate 9-codon deletion lacking in these species but found in the remaining Microgale. They concluded that this lineage had diverged from other shrew tenrecs in the Miocene.

Placentation

Villous area of the placenta of Dobson's shrew
tenrec (Nesogale dobsoni) stained for cytokeratin (brown)

We included N. talazaci and N. dobsoni in our study of placentation in shrew tenrecs (here). As in Microgale and Oryzorictes there was both a central labyrinth and a more peripheral villous area. We did not notice any differences that would set Nesogale apart.

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.

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.

 

  

  

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. 

Placentation in opossums

Embryo of Virginia Opossum (Didelphys virginiana) at 6 days
of gestation. Opened to show the vessels of the trilaminar yolk sac
and free-floating allantoic sac. From Selenka 1886.

Emil Selenka did not confine himself to rodents and primates (previous post and recent review). He also gave the first detailed description of embryonic development in a marsupial, the Virginia opossum. He bred them in the laboratory and thus had dated pregnancies.

All marsupials have a yolk sac placenta with both two-layered and three-layered areas (bilaminar and trilaminar omphalopleure); the latter has blood vessels that radiate from a sinus terminalis as can be seen in Selenka's illustration.



Neonate of Virginia Opossum. From Selenka 1886.

The Virginia opossum has a pretty short gestation even for a marsupial. The neonate above was born after 13 days. Development is supported largely by histotrophic nutrition, i.e. uptake of uterine gland secretions. The vascular part of the yolk sac is thought to be more important for gaseous exchange.

Note that the allantois makes no contact with the trophoblast. Unlike in the koala, wombat and bandicoots, there is nothing approaching chorioallantoic placentation. The allantois serves mainly as a receptacle for urine excreted by the mesonephros (here). 

Virginia Opossum (D. virginiana) by Cody Pope CC BY-SA 2.5
(Wikipedia Commons)
 

There are 87 species of didelphids in Central and South America, but the Virginia opossum is alone in extending its range to the USA and Canada.

Despite the species richness, placentation has been described for only five opossums; three from the same genus (D. virginiana, D. aurita and D. marsupialis) plus the gray short-tailed opossum (Monodelphis domestica) and gray four-eyed opossum (Philander opossum). I will save them for a later post.