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.