Do not marsupials have trophoblast?

Embryonic and trophoblastic areas of the marsupial

blastocyst as envisaged by Hartman 

In the final chapter of her book (previous post), Zofia Kielan-Jaworowska writes on placental mammals, "Their enormous success depends in the first place on the acquisition of the trophoblast, on the basis of which the placenta is formed." In contrast, "Without the trophoblast, marsupials are unable to prolong their gestation period and are born at an extremely early level of anatomical development." This view or a version of it seems to be shared by other zoologists. 

The souce of the misunderstanding can be traced to influential papers by Jason A. Lillegraven (e.g. here). The marsupial blastocyst lacks the inner cell mass of a placental mammal blastocyst. Early on, however, there are two distinct areas that often have been referred to as the embryonic and trophoblastic areas. Lillegraven argues, convincingly in my view, that the "embryonic area" is not equivalent to the inner cell mass and that a considerable portion of the "trophoblastic area" forms part of the developing embryo. In an anatomical sense the trophoblastic area is not the trophoblast as defined by Hubrecht (see previous post).

Nonetheless, Lillegraven also says, "But from a functional point of view (as applied to extra-embryonic parts of the conceptus having direct nutritive significance), the term "trophoblast" may be used to good advantage throughout the Amniota, whether development occurs within a shelled or a shell-free setting."

Thus marsupials do have trophoblast and of course they all have at least a yolk sac placenta and sometimes a chorioallantoic placenta to boot. As shown by Ulrich Zeller and Claudia Freyer (here) there are marsupials where the trophoblast forms  a syncytium and exhibits invasive properties.

As noted in a previous post, there are sound reasons for distinguishing between Eutheria and Placentalia but it is little wonder that marsupial specialists bridle at the term "placental mammals."  

Karl Bogislaus Reichert

Karl Bogislaus Reichert (1811-1883)

Crucial to our understanding of the evolution of mammals is the origin of the bones of the inner ear from what were elements of the jaw articulation in reptiles. This was worked out in 1837 by the German embryologist Karl Bogislaus Reichert. Zofia Kielan-Jaworowska (previous post) notes this is all the more remarkable in view of the primitive tools available at the time. Later Ernst Gaupp built on this work and the supposed origin of the inner ear bones is known as the Reichert-Gaupp theory.



Reichert's membrane (Rm) in the placenta of the capybara

From Kanashiro et al. Reprod Biol Endocrinol 2009; 7: 57 (here)

Students of the placenta will be more familiar with the name of Reichert through the eponymous membrane that lies between the trophoblast and the endoderm of the parietal yolk sac in rodents and insectivores. It was first described by Reichert in the guinea pig (Abh Akad Wissensch Berlin 1862; pp. 97-216).

In pursuit of early mammals

A multituberculate (Catopsbaatar) about to fall prey

to a dinosaur (Saurornithoides)

This fascinating book is the autobiography of the eminent paleontologist Zofia Kielan-Jaworowska and an introduction to the early history of mammals.

Her descriptions of the Polish-Mongolian expeditions in 1963-71 recount the daunting logistics of working in the Gobi Desert 1000 km from Ulaanbaatar and transporting back fossils weighing several tons. The excitement of the fossil hunt is apparent: "I turned the block over and was left speechless! I had in my hands an almost complete, beautifully preserved skull of a small dinosaur." With this as a starting point we follow Zofia Kielan-Jaworowska's subsequent career, which included eight years on the faculty of Oslo University. In 2002 she returned to Gobi with her grandaughter Zosia; ten years on Zosia checked the references for the current volume. 

The second half of the book focuses on the evolution of mammals. It is restricted to the crown group that includes the living monotremes, marsupials and placentals and extinct groups with which they share a common ancestor. Arguably this includes the fossils of greatest interest to the general reader. For a more comprehensive treatment of the subject there is Mammals from the Age of Dinosaurs (2004) by Kielan-Jaworowska, Cifelli and Luo.

The new book contains potted biographies of many eminent vertebrate paleontologists, including some of the author's predecessors as well as recent stars such as Zhe-Xi Luo. It is richly illustrated with historical photos and line drawings of fossil mammals from the age of dinosaurs.

The spiny mouse

Spiny mouse (Acomys sp.) Wikimedia Commons

Despite its appearance the spiny mouse belongs to a different subfamily than the laboratory mouse. More importantly, it has a different reproductive strategy. Litter size is smaller and much of organ development occurs in utero resulting in the birth of precocial young. Thus it is a better model for late gestation in humans than the mouse, which has large litters and altricial young (see previous post).

At the same time, the laboratory species (Acomys cahirinus) is sufficiently close to mouse and rat that it is possible to develop primers based on the nucleotide sequences of mouse and rat genes (exemplified here). 

A group at Monash University has been using the spiny mouse in studies of fetal programming and sex-dependent effects of glucocorticoids on placental development (here). The spiny mouse holds great promise as a new model for placental and fetal development. Moreover, its potential for studies in a quite different area, tissue regeneration (here), means it is likely to be come more widely available as a laboratory animal.

Maureen Young 1915-2013



Maureen Young in Denmark 1989

Professor I. Maureen Young made an important contribution to our knowledge of amino acid transfer across the placenta and its role in fetal nutrition.

Maureen Young graduated from Bedford College for Women in 1938 and continued there as a demonstrator and assistant lecturer. During the Second World War the College evacuated to Cambridge where Maureen met Sir Joseph Barcroft. This was the start of a life long interest in fetal physiology (see her review of Barcroft's book here). In 1946 she moved to St. Thomas's Hospital Medical School. She was Professor of Perinatal Physiology there from 1976 until her retirement in 1982. She then settled at Toft in Cambridge.

Maureen was one of a generation of women who rose to the top in research often at great personal sacrifice. She wrote about some of the others in Women Physiologists (Portland Press 1993). At placenta meetings she was often to be found in the company of her American counterpart Elizabeth M. Ramsey (previous post).

Although international travel was eventually curtailed, Maureen continued to attend scientific meetings at Cambridge until well into her 95th year. She will be greatly missed. 

An ancient endogenous retrovirus

Classes of ERVs Wikimedia Commons

Endogenous retroviruses (ERVs) are genes of retroviral origin that have been incorporated into the genome. They include the syncytins expressed in the placentas of various mammals. Six are known so far and each represents a separate capture of a retroviral gene (see previous post). 

Now an ERV has been described that occurs in representatives of all four superordinal clades of placental mammal (here). In this case the gene is orthologous and thus represents a single integration event that must have predated the divergence of placental mammals in the Cretaceous (for possible dates see my recent post).

This work was published in a special issue of Phil Trans R Soc B on the theme "Paleovirology: insights from the genomic fossil record." Although sequence substitutions occur over time, an ERV is essentially a "fossil" record of a virus as it existed at the time of incorporation into the host genome. Thus the study of ERVs in various organisms (not just mammals) can provide insight into the long term history of viruses and virus-host interactions (see overview here).

In a historical overview of the field (here) Robin A. Weiss notes, "The advantage to the host of ERV protein expression is most dramatic in the evolution of the mammalian placenta." Incidentally, if you find the whole concept hard to swallow you are in good company as the early history of the field so clearly shows.

The Mammalian Ovary

Mossman and Duke 1973

It is now 40 years since publication of Harland Mossman's "other" book (previous post). It differs in many respects from the better known volume on fetal membranes. In particular it is richly illustrated with photomicrographs. Most of the specimens were in the collections of its authors. The Harland W. Mossman Collection is conserved at the University of Wisconsin Zoological Museum and there is a searchable data base (here).

Kenneth L. Duke was an alumnus of Brigham Young University at Provo, Utah. On retiring from Duke University he sent his collection there. Mercifully it has remained intact although it has not been catalogued. Much of the material will be from Duke's yearly field trips to The Great Basin but there is also material from South East Asia. There are placentas from some species including the Philippine colugo.

Comparative Morphology of the Mammalian Ovary takes as a starting point the red squirrel (Tamiasciurus hudsonicus) before dealing with a number of topics across the full range of mammals. For individual taxa the synoptic tables at the back of the book are unsurpassed as a source. The footnotes to these tables indicate where they rely on Duke's Collection now at BYU.

Disclosure: I am adjunct curator of The Harland W. Mossman Collection.