Embryologists then and now

International Institute of Embryology London 2-5 August 1938

The photos in this post are separated by three quarters of a century. We know the identities of the 1938 embryologists because an annotated copy was sent by Fritz Strauss to Harland W. Mossman and is curated in the latter's collection in Madison, Wisconsin.

Top row (left to right): T. Thomson Flynn (Belfast); H. M. W. Woerdeman (Amsterdam); Hans Bluntschli (Bern); Jan Florian (Brno).

Middle row: G.L. Streeter (Carnegie Institution); Karl Peter (Greifswald); Mrs. Katherine Jones Hill (London); E.S. Goodrich (Oxford); Miss E. G. Fraser (London); Warren H. Lewis (Carnegie Institution); A. Celestino da Costa (Lisbon); Paul Gérard (Brussels); H. Woollard (London). 

Bottom row: Otto Grosser (Prague); J.T. Wilson (Cambridge); J. Boeke (Utrecht); Honor B. Fell (Cambridge); Dan de Lange (Utrecht); J. P. Hill (London).

It was my pleasure to attend a recent meeting in Göttingen and find that embryology is still going strong. As in the 1938 Group there are some eminent biologists here. But the most striking difference between the two photos is the inclusion of many postdocs and graduate students with the promise it brings for the future of the field.

Some curiosa

Together with Elliott Smith, J. T. Wilson and J. P. Hill were part of the Fraternity of the Duckmaloi that pioneered research in monotreme and marsupial embryology. Their heirs are Marilyn Renfree (front row fourth from left) and Karen Lychau Hansen (front row third from right).

Theodore Thomson Flynn also worked on marsupials but later turned to fish. He named one species Gibbonsia erroli after his son, who later achieved fame as the swashbuckling film star Errol Flynn.  

One of the few women in the 1938 Photo is Katherine Jones Hill. The daughter of J. P. Hill, she was an embryologist in her own right. She catalogued the Hill Collection now housed in Berlin. 

Zofia Kielan-Jaworowska

Zofia Kielan-Jaworowska 1925-2015

The current issue of Nature carries an obituary of Professor Zofia Kielan-Jaworowska, the eminent palaeontologist, who died 13 March 2015.

In Pursuit of Mammals

Previously I reviewed the autobiography of this remarkable woman (here) and it remains a fascinating account of her adventurous life and the early history of mammals.

A leadership role for post-menopausal killer whales

Male killer whale (Orcinus orca) near Tysfjord, Norway
Wikimedia Commons (CC)

The male killer whale above may have an impressive dorsal fin, but when it comes to leadership, older females play a greater role. A recent study of a resident population found that females with an age of 35 or older led the pod, especially when food resources were scarce.

Ovarian function in whales has been assessed by counting the number of corpora lutea and corpora albicantia in each ovary. Baleen whales ovulate from both ovaries with about the same frequency. In toothed whales, however, the left ovary tends to be more active. In some dolphins, all ovulations occur on the left side early in life; later the right ovary kicks in, perhaps because the left ovary is becoming exhausted. According to the renowned scientist Seiji Ohsumi, this pattern occurs in the bottlenose dolphin (Tursiops truncatus) and striped dolphin (Stenella coeruleoalba).

In some cetaceans, it would seem the ovaries have a limited capacity. Once it is exhausted the females enter a post-reproductive phase that has been likened to human menopause. This was documented for the short-finned pilot whale (Globicephala macrorhynchus) by Marsh and Kasuya and later for the killer whale (Orcinus orca).

A resident population of killer whales off the coast of British Columbia and Washington State has been under observations for years. Individuals can be identified in the field and their ages are known. Their main source of food is Chinook salmon. When resources were scarce the hunt was led by females of post-reproductive age.

Does this provide an explanation for "the evolution of menopause" as the authors of the new study suggest? To my thinking that is a bit of a stretch.    

Ohsumi S. Scientific Reports of the Whale Research Institute 1964; 18: 123-49.

Marsh H, Kasuya t. Rep. Int. Whaling Commission (Special Issues) 1986; 8: 57-74. 

East African fossils cast new light on the origins of Homo

Reconstructed skull of Homo rudolfensis (KNM ER 1470)
Wikipedia Commons (CC) Durova

This week two important papers address the antiquity and diversity of the genus Homo.

A study published in Nature (here) takes a fresh look at Homo habilis, "The Handy Man," first described half a century ago (see previous post). The mandible (lower jaw) of the type specimen (OH 7) is badly distorted, but has been reconstructed using state-of-the-art computer tomography and 3D imaging technology. Comparison with other fossil mandibles from the region shows that not all can be ascribed to H. habilis. Indirectly. this supports the validity of Homo rudolfensis (pictured) as a distinct species.

A similar approach yielded a new estimate for the endocranial volume of OH 7 (a proxy for brain size). Interestingly, similar values are obtained for H. habilis, H. rudolfensis and H. erectus. 

A new fossil from Ethiopia, described in Science (here and here), is too incomplete to assign to a species. It is exciting because it can be assigned to the genus Homo and is 400,000 years older than all previous fossils. It pushes the origin of our genus back to at least 2.8 million years ago. There could well be overlap with Australopithecus afarensis best known from the skeletal remains of "Lucy"

Did climate change do for the tragulids?

Lesser Mouse-deer (Tragulus kanchil) at Singapore Zoo
Photo by Bjørn Christian Tørrisen (CC)

In a previous post, on giraffe and okapi placenta, I mentioned that tragulids (chevrotains or mouse-deer) were the most abundant ruminants in the Early Miocene. They were displaced by the pecoran ruminants and today are represented by a mere handful of species.

A new paper in PLoS One re-examines the European fossil fauna and shows tragulids already were on the way out in the Oligocene (full text here). The focus of the study is on a narrow time period called MP28 (MP stands for Mammal Palaeogene zone). This was a period of global warming that led to wooded environments being replaced by more open habitats and the appearance of seasonality including a dry season.

Pecorans have an additional forestomach, the omasum, and this may have given them the edge over tragulids in exploiting new resources. 

Placenta of Lesser Mouse-deer showing binucleate cells stained with
anti-bovine lactogen. From the Benirschke web site.

Although tragulids have the binucleate trophoblast cells that are the signature feature of ruminant placentation, they differ from pecorans in lacking cotyledons (reviewed here).

Selenka's gibbons

Bornean White-bearded Gibbon (Hylobates albibarbis)
Primate Info Net (University of Wisconsin) Photo Credit Marilyn Cole

Emil Selenka showed that the gibbon embryo, like that of humans and other apes, develops in the uterine wall beneath a decidua capsularis. But what species did he study?

Most of his figures are of a gibbon identified as Hylobates concolor (Harlan) from Borneo. The species name is still in use for Nomascus concolor, which is not found on Borneo. I now know, thanks to Dr. Thomas Geissman and his remarkable web site, that this reflects an extraordinary comedy of errors. Harlan described his ape as a hermaphrodite orangutan from Borneo; in fact it was a juvenile gibbon from Indochina!


Geographical distribution of gibbons.
(C) 2010 Thinh et al.

How then can we identify Selenka's gibbon? A study of mitochondrial genes (here) concluded that there were two species of gibbon on Borneo, one of them with three subspecies. Fortunately Selenka stated his specimens were collected on the left bank of the Kapuas River, in the territory occupied by the Bornean White-bearded Gibbon (Hylobates albibarbis) shown above.

Early stage of pregnancy in Hylobates albibarbis with amnion (A), yolk sac (D) and
exocoelom (Ex). The specimen had been flattened by contraction of the uterus but
the decidua capsularis (Dc) is clearly seen.

The embryo is depicted above. It had a primitive streak but no somites. Therefore it may correspond to Carnegie Stage 7 or early Stage 8 in the human. Selenka's paper can be found on the web (read only).

Evolution of the decidua

In preparation for pregnancy, the endometrium undergoes a process called decidualization (previous post). This involves a change in the size, shape and properties of the connective tissue cells (stromal fibroblasts). Decidualization is a necessary prerequisite for implantation of the blastocyst and often occurs in response to an embryonic signal. In women, decidualization happens in response to a maternal signal in the second half of the menstrual cycle.

 

Decidua was present in the most recent common ancestor of placental
mammals but was lost in some lineages. Data from A. M. Mess and A. M. Carter

Based on a phylogenetic analysis (here), Andrea Mess and I concluded that decidualization was present in the most recent common ancestor of placental mammals (extant Eutheria). It was lost in some lineages, especially in those that evolved a non-invasive epitheliochorial placenta.

Gray Four-eyed Opossum (Philander opossum)
Wikimedia Commons CC-BY-3.0 (André de Souza Pereira)

How about marsupials, all of which have a yolk sac placenta? In most placentation is non-invasive and none has been shown to have a decidua. In the Gray Four-eyed Opossum (Philander opposum), however, there is penetration of the endometrium by trophoblast and traces of a primitive decidual reaction (here). This ties in quite nicely with a recent study (here) of gene expression in the endometrium of the Gray Short-tailed Opossum. This identified a population of endometrial stromal fibroblasts that expressed progesterone receptor and some transcription factors associated with human decidual cells. On the other hand, the fibroblasts did not express the decidual marker desmin or other transcription factors required for decidualization.

The authors of the latter paper are part of a consortium that just published an extensive analysis of gene expression by the endometrium across mammals (here). The study included a frog, chicken, lizard, monotreme (Duck-billed Platypus), marsupial (Gray Short-tailed Opossum), and seven different placental mammals. It identified a huge number of genes that were recruited during the evolution of pregnancy in mammals, including many that are associated with the decidualization process.

The main thrust of the new paper is the central role played in evolution by transposable elements. These were co-opted into regulatory elements that coordinate the endometrial progesterone response.