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.

Gorilla-human split - implications for the evolution of deep trophoblast invasion

Lowland gorilla (Gorilla gorilla) female and young
at the Bronx Zoo - Wikipedia Commons (CC-BY-SA 3.0)

The fossil Chororapithecus abyssinicus is the earliest known species of gorilla. A recent paper (here) dates this fossil and calculates that the split between the gorilla and human lineages occurred more than 8 million years ago (Mya). This agrees well with an estimate based on genomic data (here) putting the gorilla-human split at 7.6 to 9.7 Mya.

Placenta of Gorilla gorilla showing invasion of decidua (at left) by
trophoblasts (black stain) following the interstitial route;
villi and intervillous space  are at right

We have shown that trophoblast invasion in gorilla and chimpanzee resembles that in humans. For example there is invasion by the so called interstitial route which does not occur in monkeys or in lesser apes such as gibbons (reviewed here and previous post).

Fetus of Gorilla gorilla photographed by Louis Bolk
Courtesy of Dr. Laurens de Rooy, Museum Vrolik, Amsterdam

Gravid uteri of great apes are not easy to come by; one of the gorilla placentas we saw was collected by Louis Bolk in 1923. He described the fetus (here) and sent the placenta to J. P. Hill in London. 

We have not been able to find a gravid uterus of an orangutan. The split between orangutan and other great apes was as deep as 15-19 Mya (here). It would be interesting to know whether human-like trophoblast invasion evolved before or after that.

Marsupial frogs

Female Brazilian tree frog (Flectonotus pygmaeus) with
brood pouch enclosing the developing embryos
(Mauricio Rivera Correa ShareAlike 2.5)

What happens when frogs abandon their amphibious lifestyle for a more terrestial one? Frogs in the Family Hemiphractidae from South and Central America have evolved some ingenious solutions.

In hemiphractids, the embryo develops on the back of the mother either in a mucous-filled depression or in a closed pouch - as shown above for a Brazilian tree frog (the embryos are under the bumps).

Froglet of a marsupial frog (Gastrotheca ovipera) showing
the external gills. From Nathan 1932 (here)

The embryos may develop into tadpoles and be released to water-filled cavities in plants or skip the tadpole stage and develop directly into froglets. In species of the genus Gastrotheca, embryos have 1-2 pairs of external gills that serve for respiratory gas exchange with maternal tissues in the brood pouch. This would satisfy most people's definition of a placenta. The gills are shed around the time of birth.

Marsupial Frogs by William E. Duellman 2014
Johns Hopkins University Press ISBN 978-1-4214-1676-5

The biology of marsupial frogs is described in painstaking detail in this new book - the destillation of a lifetime's work by William E. Duellman (details here). It is superbly illustrated but at USD 120 a bit pricey. More than half the content comprises species accounts and no doubt it will find a place on the bookshelf of specialists. But it is well worth checking out for its insights into the reproductive biology of frogs. Who knew, for example, that the oocytes of Flectonotus pygmaeus have up to 2000 nuclei reduced during oogenesis to a single one?

For other fun facts on frog reproduction see this video.

The trouble with tree shrews

Pen-tailed tree shrew (Ptilocercus lowii)
By Joseph Wolf (1820 – 1899) [Public domain] via Wikimedia Commons

Tree shrews show so many resemblances to primates that the eminent anthropologist Wilfred Le Gros Clark included them in the same order. Molecular phylogenetics refuted this but placed them in the same clade or superorder (Euarchontoglires) as primates, colugos, rodents and lagomorphs. There has been much discussion about whether colugos (previous post) or tree shrews are the closest relatives to primates.

Just how troublesome tree shrews have become is highlighted by a new paper on mammalian evolution by Tarver et al. (here).  

Alternative roots to the mammalian tree from Mess & Carter (here)

In addition to Euarchontoglires, there are three major clades of placental mammals. But there has been considerable disagreement about how to root the tree with three hypotheses as shown above.

Tarver et al. attempted to resolve this using a huge amount of genomic data and more sophisticated modelling techniques. They argue convincingly for the hypothesis at the top of the diagram where Afrotheria and Xenarthra are sister groups in a clade called Atlantogenata.

But once again tree shrews caused trouble. In a consensus tree based on protein-coding genes, tree shrews were basal to Glires (rodents and lagomorphs). This is in agreement with another recent study (here). But in a separate data set based on genes for microRNA tree shrews were basal to all the other orders in Euarchontoglires. So much so that the clade itself collapsed as a valid taxon. Naughty tree shrews!

Placentation in several species of tree shrew was studied by Luckett (here) and later in Tupaia glis by Kaufmann (here and here). The placenta is labyrinthine and endotheliochorial. So far nobody has looked at a placenta from the pen-tailed tree shrew (pictured above). It occupies its own family and a new paper (here) characterizes it as a living fossil that has undergone little change since the Oligocene.

Incidentally, pen-tailed tree shrews have a large intake of fermented nectar from the bertram palm (described here); see this blog for "boozing tree shrews."

Larry Longo

Lawrence D. Longo M.D. 1926-2016

Larry Longo was among the most important perinatal physiologists of our time. He is perhaps best known for enhancing understanding of placental gas exchange by mathematical modelling. The work was conducted in close collaboration with Gordon G. Power and Esther P. Hill and summarized in a seminal review (here). Much of the input data was derived from experiments in his lab.

Together with Gordon Power and Raymond D. Gilbert, Larry founded the Center for Perinatal Biology at Loma Linda University. The research program was impressive and is still ongoing. It has been responsible for training a great number of good scientists.

Larry was not just interested in the history of science. He actively researched it. Of particular note is his 2013 book The Rise of Fetal and Neonatal Physiology (here). Larry's Collection of rare books is legendary and those priveleged to have entered his library are unlikely to forget the experience. Many images from these tomes will appear in a forthcoming book Wombs with a View co-authored with Lawrence P. Reynolds (here).

Larry will be remembered for his humility, courteousness and encouragement of all who came his way. He passed 5 January 2016.

A fuller account of Larry Longo's career can be found here and here.

Steller's sea cow

Reconstruction of Steller's sea cow (Hydrodamalis gigas)
By Emőke Dénes (Natural History Museum in London) (CC BY-SA 2.5)

When first described by Steller in 1741, the range of this sirenian was already restricted. Intensification of hunting led to extinction of the species within another 27 years.

A recent paper with a "stellar" cast of authors (here) uses molecular data to firmly establish the position of Steller's sea cow within crown Afrotheria; with additional morphological data it also shows shows how the species fits into the fossil record.

Steller's sea cow (Hydrodamalis gigas) belongs with the dugong (Dugong dugon) in Family Dugongidae whereas the three species of manatee belong to Trichechidae. Together they make up the Order Sirenia, which is sister to the elephant Order Proboscidea.

Endotheliochorial placenta of the Amazonian manatee

Fetal (fc) and maternal (mc) capillaries are present

Elephants have an endotheliochorial placenta. Therefore it perplexed us that Wislocki had described the placenta of the West Indian manatee (Trichechus manatus) as haemochorial. Therefore we reopened the matter by studying placentas from the Amazonian manatee (T. inunguis). We were able to demonstrate two sets of capillaries (shown above) and conclude this placenta to be endotheliochorial (here).

The allantoic sac of elephants and manatees has four chambers and we have shown this to be a shared, derived character of the superorder Afrotheria (here).

Placentation in salps

Placenta of a salp (Salpa fusiformis)
Reproduced from Bone, Pulsford and Amoroso (here)
(C) 1985 with permission from Elsevier

Sea squirts? asked a faithful reader of this blog. OK, sea squirts do not have placentas, but salps do! They, too, are tunicates, and thus included in the sister group to vertebrates (previous post). Whilst sea squirts are mainly sessile, salps are pelagic, living near the surface of oceans and at times more numerous than krill. They are tubular animals and swim by jet propulsion.

The life cycle involves alternation between asexual and sexual generations. The asexual phase (oozooid) develops within the jet chamber of the sexual phase (blastozooid). The image above is from Amoroso's last paper, published almost three years after his death (see previous post for Amo). The placenta consists of two layers: an outer cortex (co) and an inner central layer (c). These separate the embryonic (E) and maternal (M). circulations. Both layers are syncytial and both are maternal in origin. However, embryonic leucocytes pass into and add to the cortical layer.

Blastozooids are hermaphrodite, but the egg develops before the testis matures so is fertilized by sperm from a different blastozooid

HMS Rattlesnake on which Thomas Henry Huxley served as
Assistant Surgeon during the voyage to Australia and New Guinea 1846-50
National Maritime Museum (public domain)

The first English language description of placentation in the Family Salpida was given by T. H. Huxley R.N., "late of HMS Rattlesnake," in 1851 (here) although he cites even earlier work by Cuvier, Chamisso and Meyen.

We tend to think of placentation in terms of mammals, reptiles and fish, but a current paper in Biological Reviews (here) shows that maternal provision of nutrients (matrotrophy) and even placentation is not infrequent in invertebrate phyla.