A colugo genome at last

Phylogenetic placement of colugos  (Scandentia) in the lineage of primates
From Mason et al. Sci Adv 2016 (here) CC BY-NC

Used to be that tree shrews (Scandentia) were regarded as the closest relatives to primates as cogently argued by Wilfrid Le Gros Clark. Molecular phylogenetics have brought that into question with some proposing colugos  or "flying lemurs" (Dermoptera) as a better alternative. But there have several competing hypotheses (see Martin). Choosing the right one has been difficult in the absence of a colugo genome.

Now that has been rectified in a comprehensive study by Mason and colleagues (here) who sequenced the genome of a Sunda colugo and compared it with genomes from 21 mammals. The result clearly came out in favour of colugos as the closest relatives to primates, supported by  20 shared indels and 16 shared retrotransposons.

There are many morphological similarities between tree shrews and colugos but the tree constructed by Mason et al. implies these are due to convergent evolution. Within Euarchontoglires they find tree shrews as the sister to Glires (rodents and lagomorphs).

Museomics and hidden biodiversity within colugos

Colugo fetus and placenta at term; ys = yolk sac;
pat = patagonium From Hubrecht 1894 (here)

Current reference works recognize no more than two species of colugo: Sunda Colugo (Galeopterus variegates) and the Phillipine Colugo (Cynocephalus volans). Mason et al. conclude that there may be as many as 6 Sundaic species and 2 Phillipine ones. They reached this conclusion by extracting DNA from museum specimens of known provenance. As an example, the Eastern and western populations on Borneo are highly divergent consistent with topographical features creating barriers to dispersal.

Currently we are re-examining the placenta and fetal membranes of colugos. We too have had to rely on museum specimens such as those collected by A.A.W. Hubrecht.

The importance of museum collections has been highlighted before in this blog. It is nice that scientists other than morphologists have discovered their value and coined the term museomics for studies of DNA from ancient specimens. Those in the current study ranged from 28 to 121 years old. The oldest specimen from the Raffles Museum of Biodiversity Research is contemporaneous with those collected by Hubrecht for his study of the fetal membranes and now housed at Museum für Naturkunde in Berlin. 

Evolution of altriciality

Kangaroo Joey inside the pouch
Photo by Geoff Shaw, Zoology, Melbourne, Australia CC BY-SA 3.0)

Marsupials and so-called placental mammals share a common ancestor yet pursue very different reproductive strategies. This led Ingmar Werneberg and colleagues to ask what reproduction was like in the common ancestor of marsupials and placentals (here).
They sampled data from the literature and examined specimens in the Hill and Hubrecht Collections at Museum für Naturkunde in Berlin. (In published sources they found examination of photographs and drawings more reliable than verbal descriptions.) There is a huge data set in the Supporting Information.


Altricial and precocial neonates exemplified by the
mouse (above) and guinea pig

It was estimated that the last common ancestor of placental mammals had a gestation of around 4 months and a litter of 3-5 young. The newborn were altricial and had closed eyes and almost naked skin at birth. The precocial lifestyle of hoofed mammals and the guinea pig is a derived feature (previous post). The newborn of marsupials are, of course, highly altricial.

A reconstruction was attempted of the neonate of the therian ancestor. This suggested it was anatomically more like extant placentals than extant marsupials. In contrast, the preweaning period was very long compared to intrauterine gestation and thus infancy in this ancestor was more marsupial-like. The relative timing of eye opening was between that of placental and marsupial mammals. Gestation lasted 31 days in this hypothetical ancestor. It was reduced to 21 days in the marsupial lineage while increasing fourfold in the placental lineage.



Wombs with a view

ISBN 978-3-319-23567-7

"Illustrations of the Gravid Uterus from the Renaissance through the Nineteenth Century," compiled by Lawrence D. Longo and Lawrence P. Reynolds.

This book contains several iconic images and many that are less well known. Each with a text about the author, artist and engraver as well as an analysis of the influence of the book on contemporary science and midwifery.

Great pains have been taken with reproduction of the images. No doubt many were taken from rare books in Larry Longo's own library. It is a pity he did not live to see the result in print (previous post).

Afterbirth of the sheep with four neat rows of cotyledons
From Girolamo Fabrizio De Formato Foetu 1604

There are plenty of images of the placenta including a few from animals. Anatomists who had dissected the gravid uteri of ruminants and dogs sometimes represented human placenta as cotyledonary or zonary in shape.

I am enjoying this book. It is a pity that the publisher (Springer Nature) did not employ a copy editor. There are many more typos than might be expected in a work of such high quality.

Tidying up the tenrecs

Dobson's shrew tenrec (Nesogale dobsoni)
Photo (C) Peter J. Stephenson

A fresh phylogenetic analysis (here) based on sequence data from all living tenrecs and one otter shrew allows a re-evaluation of tenrec systematics.

The study confirmed the web-footed tenrec (Limnogale mergulus) is nested in the genus Microgale and should henceforth be referred to as M. mergulus.

However, the authors also suggest resurrecting the generic name Nesogale for two species hitherto placed in Microgale. These are Dobson's shrew tenrec (N. dobsoni) and Talazaci's shrew tenrec (N. talazaci). Support for this included a 4-codon deletion shared only by these two species and a separate 9-codon deletion lacking in these species but found in the remaining Microgale. They concluded that this lineage had diverged from other shrew tenrecs in the Miocene.

Placentation

Villous area of the placenta of Dobson's shrew
tenrec (Nesogale dobsoni) stained for cytokeratin (brown)

We included N. talazaci and N. dobsoni in our study of placentation in shrew tenrecs (here). As in Microgale and Oryzorictes there was both a central labyrinth and a more peripheral villous area. We did not notice any differences that would set Nesogale apart.

Human development - the first 13 days

Human embryo Carnegie Stage 5c (Carnegie Embryo #7700)
Photomicrograph courtesy of Dr. Allen C. Enders

A system created for cultivating mouse blastocysts has been applied successfully to describe the development of the human embryo for 13 days after in vitro fertilization. This is a step towards opening the black box in our understanding of human embryology (reviewed here). Hitherto we have been confined to interpreting the histological sections of embryos in the Carnegie Collection.

Papers by two groups were just published: Shahbazi et al. in Nature Cell Biology and Deglincerti et al. in Nature. They used appropriate molecular markers to identify epiblast, primitive endoderm (hypoblast) and trophectoderm. In addition they used cytokeratin 7 and human chorionic gonadotrophin as markers for cyto- and syncytiotrophoblast.


Day 13 embryo of the rhesus macaque (Macaca mulatta)
Courtesy of Dr. Allen C. Enders

Both groups showed the appearance of cavities corresponding to the amnion and primary yolk sac as known from studies in the rhesus macaque by Enders, Schlafke and Hendrickx. In the macaque, the yolk sac (at bottom in the figure) is outlined by visceral endoderm (beneath the epiblast) and the more squamous parietal endoderm. These tissues were identified by Shahbazi et al. in human embryos and shown to express the endoderm marker GATA6.  Deglincerti et al. found the GATA6 signal was low in the parietal cells and that they expressed the trophectoderm marker CDX2. This is an interesting observation but hardly justifies them calling these cells "yolk sac trophectoderm." The term was criticized by Janet Rossant in the accompanying News and Views (here)  and it must be hoped it does not gain currency.

As in the macaque, amnion formation was by cavitation. This is nicely described by Shahbazi et al. Unfortunately they use the term pro-amnion, which is appropriate in the mouse but not in primates (contrasted here).

Differentiation of trophectoderm into cytotrophoblast and multinucleated syncytiotrophoblast was confirmed with appearance of lacunae in the latter as appropriate for Carnegie Stage 5c.

A placenta pioneer from Philadelphia

Newborn and afterbirth of six-banded armadillo
(Euphractus sexcinctus) from Chapman 1901

Some of the earliest studies of placenta in the United States were those of Henry C. Chapman published in Proceedings of the Academy of Natural Sciences of Philadelphia (available on JStor). His observations on the placenta of a six-banded armadillo (Euphractus sexcinctus) were published in 1901 and went unsurpassed for over a century. Importantly, Chapman noted that polyembryony, known from the more widely studied nine-banded armadillo (Dasypus novemcinctus), did not occur in Euphractus.

Fetal membranes of a kangaroo (Macropus giganteus).
Note the small allantois. From Chapman 1881

Chapman is notable for an early study of the fetal membranes of the Eastern grey kangaroo (Macropus giganteus). He noted that there was a large yolk sac but a relatively small allantois that did not form a placenta.

Zonary placenta of an African elephant (Loxodonta africana)
From Chapman c. 1880

Chapman got his armadillo and kangaroo specimens from the Philadelphia Zoo, but his African bush elephant (Loxodonta africana) placenta was from Cooper and Bailey’s London Circus. His was one of several early descriptions of elephant placentation, including a paper by Assheton (here), but there was then a hiatus until the classical work by Amoroso and Perry in 1964 (here). Based on the records of the elephant keeper, Chapman was able to estimate gestation to 650-655 days.

Henry Cadwalader Chapman (1845-1910)

Chapman came from a prominent Philadelphia family. His grandmother was a Biddle and her sister had married a Cadwalader, which may explain his middle name. He studied medicine then spent three years in Europe under Richard Owen in London and Alphonse Milne-Edwards in Paris.

Chapman’s work has been cited by Mossman, Amoroso, Wislocki and Enders (here), but is in danger of being forgotten. When the next paper on Euphractus appeared in 2012 (here), Chapman’s earlier contribution was not acknowledged.

Placentation in the Tasmanian bettong

Tasmanian bettong (Bettongia gaimardi cuniculus)
By JJ Harrison (CC BY-SA 3.0) via Wikimedia Commons
 

Now regarded as a subspecies of Eastern bettong (the mainland subspecies is extinct), the fetal membranes of this small kangaroo were described in 1930 by Theodore Thomson Flynn.

Trilaminar omphalopleure (vascular yolk sac) of Tasmanian bettong
From Flynn Proc Linn Soc NSW 1930; 55: 506-531

The yolk sac comprises a vascular portion (trilaminar omphalopleure) and a non-vascular portion (bilaminar omphalopleure). The sketch above shows trophoblast of the vascular yolk sac (troph) absorbing secretions from a uterine gland (gl ep). It is unclear whether there is exchange between the capillaries on the maternal (m cap) and fetal (foet cap) sides.

Bilaminar omphalopleure (non-vascular yolk sac) of Tasmanian bettongFrom Flynn Proc Linn Soc NSW 1930; 55: 506-531

Trophoblast of the non-vascular yolk sac (bilaminar omphalopleure) was implicated in the uptake of cellular material (cm) and red blood cells (haem). In current terminology (here) it is heterophagous.

Theodore Thomson Flynn (right) with his son the actor Errol Flynn

Theodore Thomson Flynn was a marine biologist and professor at the University of Tasmania. He named a fish Gibbonsia erroli after his son Errol Flynn the film actor.