Sea squirts, lancelets and acorn worms

A sea squirt (Ciona intestinalis) - a member of Tunicata 
Wikimedia Commons uploaded by perezoso (GFDL)

Genomics has clarified our position in the tree of life. To explain this I need to define some taxonomic terms.

Phylum Chordata comprises three subphyla: Vertebrata (Craniata), Tunicata (Urochordata)and Cephalochordata. Tunicates include sea squirts  such as Ciona (pictured) above. A familiar cephalochordate is the lancelet Branchiostoma lanceolatum better known as Amphioxus (shown below).

Amphioxus or Branchiostoma lanceolatum
(c) Virginia Gewin here (CC-BY-SA 3.0)

Amphioxus has long been used to exemplify the general plan of chordate organization and lancelets used to be regarded as the closest relatives to vertebrates. The genomic evidence, however, has tunicates like the sea squirts as sister group to vertebrates with cephalochordates as a deeper branch. Additional support is given by conserved molecular signatures (here).

Chordates belong in the Superphylum Deuterostomia (brilliantly reviewed by Lowe et al. here) along with Phylum Hemichordata and Phylum Echinodermata. Echinoderms are richly represented in the fossil record and the five extant classes include sea urchins, sea cucumbers and starfish. Hemichordates include the acorn worms for which two genomes just became available (here and here).

Acorn Worms (Hemichordata: Enteropneusta)
from Spengel 1883 (public domain)

One of many findings was a cluster of six genes that are conserved across chordates and implicated in patterning of gill slits. This is significant because gill slits were an innovation in the deuterostome lineage (although secondarily lost in echinoderms).

Relationships between deuterostome phyla were largely worked out through their embryology, an example being the erection of Chordata by Haeckel. Understanding the genes involved in developmental processes remains a focus in working out our evolutionary history (see the review by Lowe et al. mentioned above).

Mouse and human blastocysts compared

Mouse blastocyst with trophectoderm (TE),
epiblast (EPI) and primitive endoderm (PE)  from Selenka 1883

Even before implantation, three cell lineages are apparent in the blastocyst of mouse and human. Outermost is the trophectoderm that will contribute trophoblast to the placenta. The inner cell mass has already differentiated into the epiblast and the primitive endoderm or hypoblast. For mouse, this much has been clear since the pioneering studies of Emil Selenka (here).

Gene expression in these three lineages of mouse placenta has been known for some time. What does this tell us about human preimplantation development? A recent paper in Development (here) suggests less than some might like to think.

• For trophectoderm, key lineages expressed in the mouse (e.g. Id2, Elf5, Eomes) either are not expressed in human trophectoderm or are expressed in alternative lineages.
• There are several genes that are exclusively expressed in human epiblast (e.g.the transcription factor KLF17).
• Expression of some genes in primitive endoderm is conserved between mouse and human (e.g. Foxa2/FOXA2).

These findings support other work indicating that the genes and signalling pathways involved in lineage specification differ between mouse and human blastocysts.

The mouse yolk sac

Placenta Volume 36 Issue 10 October 2015

Great to see yolk sacs on the front cover of Placenta. Too often the mouse yolk sac is discarded or ignored in the laboratory - either through ignorance or because it has no obvious equivalent in human pregnancy. This particular study showed how mouse deficient in the OGA gene have defective blood vessel formation (vasculogenesis). This affected branching of the blood vessels in the yolk sac.

Ignorance of the yolk sac is evidenced by a high impact journal publishing a schematic where mouse yolk sac is shown to be only residual as occurs in humans (here).

I believe the mouse model of placentation is incomplete unless the yolk sac is studied along with the chorioallantoic placenta (argued here).

Placentation in the ferret

Transverse section through the uterus of a ferret (Mustela putorius furo)
at 28 days of gestation. From Strahl and Ballmann 1915.
A, allantois; H, hemophagous organ; N. yolk sac

A recent paper discussed the domestic ferret as a model for perinatal brain injury. As  the ferret is an altricial species, events that occur during human pregnancy are deferred to the postnatal period. However, neurogenesis and neuronal migration start in pregnancy and the effects of hypoxia on these processes could be explored.

Electron micrograph of the interhemal region in a ferret placenta.
Courtest of Dr. Allen C. Enders

Like all carnivores (except hyenas), ferrets have an endotheliochorial placenta. The endothelium of the maternal capillaries is swollen as readily seen by comparing with the endothelium of fetal capillaries above.

The interhemal region of the ferret placenta.
Courtesy of Dr. Allen C. Enders

At low power it can be seen that the fetal capillaries indent the surrounding trophoblast so the diffusion distance from maternal to fetal blood is minimized. Thus oxygen should diffuse across this barrier almost as readily as in the human hemochorial placenta.

Hematoidin crystals in the hemophagous region of the ferret placenta.
From Strahl and Ballmann 1915

Like other carnivores, the ferret has a prominent hemophagous region (shown in the top figure). Here trophoblast takes up maternal red blood cells by phagocytosis and processes the contained hemoglobin to extract the iron. The hemoglobin breakdown product is hematoidin, which crystallizes out. We have described the same thing in tenrec placenta (here).

The most thorough study of ferret placenta was published a century ago (full reference here). The ultrastructure was later described by Lawn and Chiquoine (here). There are recent reviews of endotheliochorial placentation (here) and placentation in carnivores (here).

Placentation in gibbons

Agile Gibbon (Hylobates agilis) Bristol Zoo Gallery

A recent paper on a fossil ape (here) highlights the divergence of the lesser apes (gibbons and siamangs) from the great apes (orangutans, gorilla, chimpanzee, bonobo, human). The fossil (Pliobates cataloniae) has a combination of primitive and derived features that make it difficult to place on the evolutionary tree (discussed here).

 

Gibbons themselves have placentation with some monkey-like features and others shared with the great apes.

 

Uterus of an agile gibbon (H. agilis) opened to show the decidua
capsularis enclosing the embryo. From Selenka 1899

The most important shared characteristic is that the fetus develops beneath a decidua capsularis (see previous post) implying that implantation is interstitial as in great apes. In Old World monkeys implantation is superficial and no decidua capsularis is found. 

 

Placental bed of a Javan gibbon (Hylobates moloch)
Reproduced from Carter et al. (c) Museum for Naturkunde Berlin

However, when we examined the placenta of a Javan gibbon we found a continuous trophoblastic shell and a sharp boundary between the shell and the underlying endometrium - just as in Òld World monkeys. In great apes, the boundary is less distinct because trophoblast cells invade the endometrium by this route.

Clan of the cave bear: researching ancient DNA

Reconstruction of a cave bear (Ursus spelaeus)
Uploaded by Sergiodlarosa to Wikimedia Commons (CC)

The proceedings of a Royal Society discussion meeting on ancient DNA have just been published (here). Three reviews in particular captured my interest.

Ancient DNA: the first three decades by Hagelberg, Hofreiter and Keyser (here) is a lucid account of the history of the field (a major advance was shotgun sequencing as applied to the cave bear). It highlights not only high profile papers from Nature and Science (some of them reviewed in my blog), but also gives credit to important follow up studies from specialist journals. A very useful ressource indeed!

Ancient genomics by Der Sarkissian et al. (here) is from the renowned Centre for GeoGenetics in Copenhagen. This review is especially strong on the technical advances in the field and even includes a user's manual. With the techniques initially available it would have required 180 kg of material and 130 million amplicons to generate a first draft of the cave bear genome. A lot has happened since then. They conclude that even "Looking back 5 years, no one could have predicted the current state of current genomics."

Almost 20 years of Neanderthal palaeogenetics by Sánchez-Quinto and Lalueza-Fox (here) does a remarkably good job of surveying what has been learned from the DNA of Neanderthals from various geographical locations. It covers more than just their relations to and interbreeding with Denisovans and modern humans (previous post). A great deal can be inferred about their demographics, population size and ultimate extinction.

ISBN 0-517-54202-1

 The title of this post is of course an homage to the fiction of Jean M. Auel. The clan of the cave bear are Neanderthals who interact (and interbreed) with modern humans. First published in 1980 it far anticipated the scientific evidence given in the above reviews.

Pregnancy-associated malaria research suggests a way to target cancer cells

Anopheles stephensi - a vector for the malaria parasite
Centers for Disease Control and Prevention

The malaria parasite Plasmodium falciparum is spread by mosquitos. It multiplies and resides in the liver and erythrocytes (red blood cells). In areas with heavy infection with Plasmodium most individuals acquire immunity. During pregnancy, however, infected erythrocytes are able to accumulate in the placenta. Pregnancy-associated malaria is an important cause of maternal and fetal morbidity and mortality (reviewed here).



Placenta from a stillbirth due to maternal malaria infection. Normal erythrocytes lack
a nucleus. Thus a nucleus indicates the presence of the malaria parasite.
Wikimedia Commons (CC BY-SA 3.0) uploaded by Nephron

Infected erythrocytes express surface proteins, among them VAR2CSA, which can bind to a placental variant of chondroitin sulphate A (CSA) expressed by syncytiotrophoblast.

A paper just out in Cancer Cell (here) shows that placental CSA is expressed by many types of cancer cell. This knowledge was leveraged to target cancer cells using recombinant VAR2CSA fused to diptheria toxin or conjugated to hemiasterlin. Human cancer cells in vitro were effectively killed by this means. Tumour growth and metastasis in mice could be inhibited by a similar approach.

A. C. Haddon

Mask of turtle shell plates made by Torres Strait Islander and described by A. C. Haddon
Creative Commons (CC BY-NC-SA 4.0) The Trustees of the British Museum

Alfred Cort Haddon was a marine zoologist who  morphed into an eminent ethnologist and anthropologist after joining an expedition to the Torres Strait in 1898.

The Torres Strait Islanders are a Melanesian people distinct from the Aborigines of mainland Australia. Haddon collected their artefacts avidly -- convinced that their culture would soon be repressed by zealous missionaries. I had an opportunity to view some of these artefacts on a recent visit to the Queensland Museum in Brisbane. Haddon donated also to the British Museum, but the bulk of his Collection is now in the Museum of Anthropology and Archaeology at Cambridge University.

Alfred Cort Haddon (1855-1940)
The Wellcome Museum, Wellcome Images (CC BY 4.0)

Haddon's Collection was key to a 2011 study that examined the origin of the Australian Aborigines (here). A genomic sequence was obtained from a hair sample that had been collected in the 1920s as Haddon passed through Golden Ridge, near Kalgoorlie, Western Australia. Ethical concerns about using this material were allayed when it could be shown, with the aid of contemporary newspaper reports, that the sample was donated voluntarily. The main finding was that Aborigines are descendents of a human dispersal out of Africa that was separate and much earlier than that giving rise to present day Asians.



Cambridge University Press 1924 (Second and Revised Edition)

Human genomics has greatly improved our understanding of the migrations that gave rise to modern peoples. Haddon would have been fascinated. He did what he could with the tools then available to him and summarized them in the above book. The title was not as controversial at the time as it might be considered today.

Transcriptome of the pregnant male seahorse

Pot-bellied seahorse (Hippocampus abdominalis) from Sketchbook of Fishes
by William Buelow Gould (1801-53)

Viviparity in seahorses involves incubation of the embryos in the brood pouch of the male. A new study (abstract here) analyses the transcriptome of the brood pouch of the pot-bellied seahorse for genes that are upregulated during pregnancy and in transition to the post partum state.

Many of the same genes or their homologs are upregulated during pregnancy in mammals and other viviparous taxa. Placentologists will want to scan the tables for their favourite genes. I found it interesting that genes involved in lipid transport and iron transfer are upregulated.

The authors suggest the possibility that a common toolkit of genes is recruited to support pregnacy in mammals, reptiles and live-bearing fish.

Monotreme fetal membranes

Short-beaked Echidna (Tachyglossus aculeatus) Barossa Valley,
South Australia. It has tucked in its beak at the end by the tuft of grass

The three species of echidna and the duck-billed platypus constitute the order Monotremata. They produce milk and thus are mammals but they lay eggs. The aborigines knew this as reported by Caley in 1803 but their accounts were distrusted. It was not until 1884 that Caldwell could send his famous cable to the British Association: " Monotremes oviparous, ovum meroblastic."

Drawing of the echidna by Charles-Alexandre Lesueur 1802-3

The first description of an echidna, in 1792, was by Captain William Bligh of Bounty fame. The drawing above was made during the French Baudin expedition in 1802-3.

Because they lay eggs, one might suppose monotremes to lack a placenta. Yet two-thirds of embryonic development takes place in the uterus and the embryo is nourished in part by endometrial secretions. These are taken up by the yolk sac through the egg shell membrane, which is porous and able to stretch as the embryo grows in size. This state of affairs is best described as matrotrophy (explained here), although it has been argued that the yolk sac of monotremes ought to be regarded as a placenta (here).

Baltimore: The John Hopkins University Press 2004
ISBN 0-8018-8052-1 (pbk.) 

 For a fascinating and well illustrated account of early work on the embryology of monotremes, the above book can be recommended.

Defining the genus Homo

Reconstruction of Homo erectus georgicus by Élisabeth Daynes
Licensed under CC BY-SA 3.0 via Wikipedia Commons

A thought provoking essay in the current issue of Science (here) asserts definitions of the genus Homo and the species assigned to it remain "as fuzzy as ever." They drive home their point by showing, on the one hand, specimens attributed to Homo with australopithecine features and, on the other, australopithecine fossils with features hitherto claimed to be confined to Homo.

This is a brief but instructive read. The take home message is that hominid systematics needs to be rethought. In the process we may need to scrap "the iconic list of names in which fossil specimens have historically been trapped."

Cover of Third Edition 1956

One name that may have to go is Homo habilis (previous post), the handy man. Louis Leakey, it is suggested, was keen (perhaps too keen) to identify this fossil as the maker of simple tools following the dictum of Man the Toolmaker. It was a pleasant surprise to find Kenneth P. Oakley's booklet cited as an influence on previous and current thinking. My well thumbed copy dates from my schooldays.

Viviparity in extinct reptiles

Mesosaur - an aquatic reptile from the Palaeozoic
Nobu Tamura (CC BY 2.5 via Wikimedia Commons)

Dan Blackburn and Christian Sidor have written an interesting paper (here)summarizing the fossil evidence for viviparity in the Late Palaeozoic and Mesozoic Eras. They document a minimum of six separate evolutionary origins of viviparity. Most are aquatic reptiles including mesosaurs (picture), sauropterygians, ichthyopterygians, choristoderans and mosasauroids. The sixth example is a Cretaceous lizard Yabeinosaurus.



Mosasaurus hoffmannii - an aquatic reptile from the Late Cretaceous
 Nobu Tamura (CC BY 3.0 via Wikimedia Commons)

 It cannot be established with certainty that the fetuses were supported by a placenta, since soft tissues usually do not fossilize. The probability is great, however, given the advanced stage of development at birth and by analogy with present day snakes and lizards. Some have extremely complex placentas an example being the New World lizard Mabuya (here).

Materpiscis attenboroughi - a live-bearing fish from the Late Devonian 
Sularko - Museum Victoria (Licensed under CC BY-SA 3.0 via Wikimedia Commons)


My own article on fossil evidence for viviparity (here) was prompted by the discovery of an extremely well preserved fish with a putative umbilical cord (here).

The chicken or the egg

 As an afterthought it is of interest that the original amniote egg had a leathery shell like many reptiles today. A calcified shell was evolved at least four times (here) including in the dinosaur lineage that led to the birds. The calcified egg came before the chicken!    

Human evolution: brain, birthweight and the immune system

The Royal Society recently published a special issue of Philosophical Transactions B entitled Human evolution: brain, birthweight and the immune system, edited by Graham J Burton, Ashley Moffett and Barry Keverne. The interesting theme is summarized as follows:

"The complexity of the human brain is unique amongst mammals. However, the large size of the brain at birth poses risks to mother and offspring due to constraints on pelvic architecture and uterine perfusion imposed by bipedalism, the so-called ‘obstetric dilemma’. The growth of the human brain in utero is believed to be permitted by our unique highly invasive form of placentation. The structure of the placenta varies to a greater extent between different mammalian species than any other organ. In particular, there is a spectrum of invasiveness of the fetal tissues into the wall of the uterus, even amongst the apes. Invasion poses unique immunological challenges as the migrating trophoblast cells expressing paternal genes intermingle with cells of the maternal immune system in the uterine wall that must be negotiated. Recent advances have also revealed important insights into the genetic and epigenetic links between the regulation of placental and brain growth, centred on imprinted genes that are expressed in a parent-of-origin manner. This complex network of interactions regulating brain development is explored in this Theme Issue in the light of new concepts in placental evolution, the immune system at the maternal-fetal interface, and genomic imprinting."

The table of contents can be found here. Disclosure: I co-authored one of the papers.

South American fossil ungulates are related to modern horses

Macrauchenia - an extinct South American native ungulate
Drawn by Kobrina Olga (Wikimedia Commons CC BY 3.0)

South American mammals either arrived recently during the Great American Interchange, came to South America by rafting (previous post), or have a shallow fossil record (xenarthrans). In contrast, South American native ungulates (SANU) have a deep fossil record. Though the lineage is now extinct, genera such as Macrauchenia (above) and Toxodon survived into the Late Quaternary. The conditions under which these fossils were conserved did not favour survival of their DNA. However, a paper just out in Nature (here) shows how proteomics can be used to probe their phylogenetic affinities.

The authors used MALDI-TOF mass spectrometry to determine the amino acid sequences of the alpha chains of type I collagen extracted from fossil bones. They then performed a phylogenetic analysis. This showed that Macrauchenia and Toxodon form a monophyletic group. Interestingly, this resolved as the sister group to modern Perissodactyla, i.e. horses, tapirs and rhinoceroses. Together they form a taxon named Panperissodactyla.

The modern species have an epitheliochorial placenta so perhaps this type was present in the sister species Macrauchenia  and Toxodon.

Placentalia - a subgroup of placental mammals

Sir Richard Owen (1804-1892)

The current literature abounds with the term "placental mammals;" it often appears in a paper's title. Even though marsupials have a yolk sac placenta - and several a chorioallantoic placenta - they are not included in the definition of Placentalia. This is a constant source of irritation to marsupial biologists and a pitfall for those wishing to stay their friends (see between Scylla and Charibdis).

Placentalia was relaunched by McKenna and Bell in their influential volume Classification of Mammals above the Species Level (New York 1997). It is attributed to Sir Richard Owen (pictured above).

Owen 1837 [sic] page 903

This is the passage cited by McKenna and Bell. It may well be the first usage of Placentalia but is far from being a definition.

In its current usage, Placentalia defines a crown group of mammals comprising extant species and their ancestors. It is not the same as Eutheria, which includes lineages that do not have living descendants. Placentalia therefore is popular in molecular phylogenetics and phylogenomics. The reason is evident: when working with DNA sequences from living species, inferences can be drawn only about character evolution in the crown group.

When looking for the Owen reference I found that McKenna and Bell had got the date wrong. Robert B. Todd commenced publication of The Cyclopaedia of Anatomy and Physiology in 1837 but Owen's article is in volume 4 part 2 published 1849-52 (full reference below).

Owen R. Teeth. In Todd R.B. (Ed.) The Cyclopaedia of Anatomy and Physiology Vol. 4 Part 2, pp. 864-935. London: Longman, Brown, Green, Longmans and Roberts, 1849-1852. McKenna and Bell Refer to page 903.

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.