Temerity of the tenrec

Lesser hedgehog tenrec © Peter J Stephenson

After human and mouse the tenrec was one of the first mammals to be sequenced (link here). When this was still in the works, the popular science magazine ScienceNews put a tenrec on the cover. The caption to the article read, "They're sequencing a what?" (here). 

Sadly the tenrec has had it's 15 minutes of fame. When Nature News and Comment ran a report on a recent study from the Chavan lab., it was headlined, "Armadillo, hedgehog and rabbit genes reveal how pregnancy evolved." Once the editors realized Echinops telfairi was a tenrec, this was shortened to "Armadillo and rabbit genes..."

The irony to this was that a previous paper from the lab. (OA here) wrote that their hypothesis - about implantation evolving from an inflammatory reaction - could be tested by looking at the basal eutherian clades Afrotheria and Xenarthra. The lecture on which Nature News and Comment was reporting showed this had now been addressed in a tenrec (Afrotheria) and an armadillo (Xenarthra).

The temerity of a tenrec dressing up like a hedgehog! 

Placentation in lizards and a new syncytin

The South American skink Mabuya mabouya 

Mark Stevens from Warrington, UK CC BY 2.0

Viviparity is common in lizards and some have evolved quite complex placentas. One of the first to be studied was Chalcides chalcides. Daniel Blackburn, Luana Paulesu and others have just written an interesting historical account of the 1891 paper by Giacomini (here).  

Placentome and paraplacentomal region in Mabuya sp.

From Cornelis et al. PNAS 2017 (here)

An even more complex placenta is found in South American species of the genus Mabuya. Martha Ramirez-Pinilla, a reproductive biologist from Colombia, has authored several papers on Mabuya placenta (e.g. here). Now she has joined forces with the group at Gustave Roussy in Paris to look for syncytins (here).

As explained in previous posts (e.g. here), syncytins are the products of endogenous retroviral genes. The envelope (env) genes of retroviruses function to promote fusion of the viral membrane with the plasma membrane of a host cell. Syncytins are derived from env genes and are expressed in the placenta, where they promote fusion of cytotrophoblasts with the syncytiotrophoblast. Hitherto they have been identified in six orders of eutherian mammals and in one marsupial (previous post).

Cornelis et al. first determined the transcriptome of Mabuya placenta and identified four env genes. One of these (named Mab-Env1) was highly expressed in placenta and with the highest expression of RNA and protein occurring at the fetal-maternal interface including in a maternal syncytial layer. Importantly, Mab-Env1 was fusogenic in an ex vivo assay, which is an essential criterion for designating the protein as a syncytin. The receptor for Mab-Env1 was also identified in this study. 

Tree shrews move from branch to branch

Species tree by three coalescent-based approaches
from Esselstyn et al 2017 © The Author 2017

In an heroic effort to resolve some of the difficult nodes in the mammalian tree, Esselstyn et al. used data from published genomes and added new data for a total of 100 mammals. Focussing on ultraconserved elements, they analysed all this by a battery of techniques, These included the classical maximum likelihood (ML) on concatenated data and three coalescent-based approaches. How did they do?

The first problem was to resolve the root of the eutherian tree. Here they did rather well. Both the ML tree and two of the coalescent-based methods gave strong support to the Atlantogenata hypothesis, i.e. a sister relationship between Afrotheria (elephants, dugongs, tenrecs and hyraxes) and Xenarthra (sloths and armadillos) with a common ancestor basal to Boreoeutheria (all other eutherian mammals).

South American Tapir (Tapirus terrestris)

Photo by Bernard Dupont CC BY-SA 2.0

They did almost as well with the second problem: the sister group to horses, rhinos and tapirs (Perissodactyla). In most analyses the found Cetartiodactyla (cetaceans and even-toed ungulates) as sister to Perissodactyla. However, they could not rule out one of the alternative hypotheses, which had bats (Chiroptera) as the sister group.

Whereas horses and cetartiodactyls (including ruminants, pigs, dolphins) all have epitheliochorial placentation, no bat does, so I am happy with their majority finding!

Pen-tailed tree shrew (Ptilocercus lowii)

From Wolf 1848 via Wikipedia Commons

On the third thorny problem the exercise failed. Tree shrews used to be thought the closest relatives to primates but have been toppled from this position in favour of colugos (previous post). Because some previous studies did not even include colugos, the present authors sought a remedy in including two colugos and three tree shrews, including the pen-tailed tree shrew above. The hope was that high taxon coverage would give a sounder result. But they were forced to conclude that placement remains uncertain. Tree shrews may be sister to rodents and lagomorphs (Glires) or to colugos plus primates (Primatomorpha).

Fortunately they could confirm colugos as sister to primates, which was the basis for my recent paper with Andrea Mess on the evolution from labyrinthine to villous placentation (here).

Marsupial and eutherian placentation

Placenta of the tammar wallaby showing the bilaminar (BOM)
and trilaminar (TOM) omphalopleure. From Guernsey et al.
eLife 2017 CC The Authors

A brand new paper compares the transcriptomes of marsupial (tammar) and eutherian (mouse and human) placentas and mammary glands (here). It confirms that marsupials have fully functional placentas expressing many of the same genes as eutherian ones.

There is evidence for a division of function between the two parts of the yolk sac placenta, with the nonvascular part (BOM) being responsible for uptake and metabolism of nutrients and the vascular part (TOM) for respiration. I am not sure how much oxygen the tiny marsupial embryo needs. Perhaps the TOM is more important for removing CO₂ and regulating the acid-base balance of the embryo. The tammar has an embryonic-type hemoglobin more capable of sequestering oxygen (protecting the embryo from reactive oxygen species) than transporting it to tissues.

A fascinating detail is that the yolk sac endoderm of the tammar has assumed functions, especially to do with trafficking of nutrients, that in eutherians are served by trophoblast.

Genes expressed in mammary gland and placenta
of marsupials and eutherians. From Guernsey et al.
eLife 2017 CC The Authors

Because much of development in the wallaby is supported by lactation, it is interesting to find considerable overlap in the transcriptomes of marsupial mammary gland and eutherian placenta.

My only criticism of this paper would be: the mouse has a yolk sac that supports early embryonic development and continues to function alongside the placenta right up to term. Perhaps the authors could not identify a data set on mouse yolk sac transcriptome, but they should have referenced the eutherian yolk sac in their discussion. An interesting theory by Claudia Freyer et al. (here) is that the stem species of therians (marsupials and eutherians) had both types of placentation.

For additional remarks on this paper see Nature News and Comments (here).

Hermann von Ihering and polyembryony in armadillos

Uterus of the mulita (Dasypus hybridus) with 9 identical
embryos. From Fernandez Morph Jahrb 1909; 39:302-333

In 1886 Hermann von Ihering opened the uteri of two pregnant armadillos. Both contained 9 fetuses of the same sex. Each fetus had its own amnion but all were enclosed in a common chorion (placenta). He was the first to propose that the embryos were derived from a single fertilized egg with splitting into separate embryos occurring early in development.

Arrangement of fetal membranes in the mulita (Dasypus hybridus).
From Fernandez Morph Jahrb 1909; 39:302-333

Ihering had studied the mulita or Southern Long-Nosed Armadillo (Dasypus hybridus). Later Fernández demonstrated that splitting occurred at the embryonic shield stage in the mulita. Newman & Patterson, working with the nine-banded armadillo (D. novemcinctus), came to a similar conclusion. Fernández, however, was the first to obtain early stages before splitting occurred. More recently, the nine-banded armadillo was the object of elegant studies by Allen Enders (summarized here). Specific polyembryony is known only from Dasypodinae and is thought not to occur in the two other subfamilies of armadillo.

Hermann von Ihering (1850-1930)
CC BY-SA 3.0 Wikimedia Commons

Hermann von Ihering was a German zoologist who relocated to Brazil in reaction to his family's disapproval of his marriage to a widow with a child. This was in 1880. His first years were spent as a collector in the southern state of Rio Grande do Sul, based on an Island known as Ilha do Doutor (Doctor's Island). In 1893 he became the first director of Museu Paulista (State Museum of Sao Paulo) and held this post for 23 years.

Hermann von Ihering´s principal area of expertise was mollusks. He also became an expert on the birds of the State of Sao Paulo, of which he observed 695 species and subspecies. For my Brazilian readers there is an excellent recent biography by Hitoshi Nomura (open access here). It lists 338 of his publications.

His son Rodolpho von Ihering (1883-1939) was also a zoologist. He was appointed vice director of Museu Paulista, which led to the accusation of nepotism that was to force Hermann's resignation. Rodolpho was an expert on fish and is credited with founding Brazilian pisciculture with stations at Porto Alegre in Rio Grande do Sul and Pirassununga, S.P.

References: Biol Zentralblatt 1886; 6:532-9 and Arch Physiol 1886; pp. 443-50

Foetus or fetus?

Human Fetus drawn by Leonardo da Vinci

There was a recent spate of tweeting about the correct spelling in British usage of fetus - or foetus. As the Oxford Dictionary makes clear, the spelling foetus has no etymological basis.

A similar debate 50 years ago was initiated by James Dixon Boyd and William James Hamilton in connection with the first edition of their influential textbook Human Embryology (previous post). This was in the BMJ. Coincidentally Bernard Towers (later Professor of Anatomy and Pediatrics at UCLA) raised the issue in Arch Dis Child. Earlier, Lionel Everard Napier had argued for "fetus" in The Lancet.

The thrust of their arguments was that "fetus" was the only spelling in use until 600 A.D., "foetus" being introduced by Isidorus of Seville on the basis of an erroneous etymology.

Statue of Isidorus of Seville in Madrid
Photo by Luis Garcia CC BY-SA 2.5

Boyd and Hamilton solicited opinion on the subject and the resulting letters fell out 5 to 1 in support of "fetus." Among the supporters was J.H.M. Pinkerton, later Professor of Midwifery and Gynaecology in Belfast. The counter argument, "Foetus is a word of respectable antiquity and lineage," was advanced by Hugh Gault Calwell who is known to have been skilled in Greek and Latin. Sadly, when Human Embryology appeared, it used "foetus" rather than "fetus."

References: BMJ 1967 (5337): 425, (5539): 568, (5540): 631, Arch Dis Child 1967; 42:224, Lancet 1952; 260: 885-6.

From antelope placenta to the chi square distribution

The Four-horned Antelope (Tetracerus quadricornis)
Philip Sclater The Book of Antelopes 1894

Despite its appearance, this Indian species is not a true antelope, but belongs to the subfamily Bovinae. Its placenta was described in 1884 by Raphael Weldon then a Scholar of St John's College, Cambridge.

Gravid uterus of the Four-horned Antelope
Weldon Proc Zool Soc London 1884

There was a fetus in each horn and Weldon was struck by the relative paucity of placentomes (30 and 22, respectively).

One extremity of the chorion of the Four-horned Antelope
Weldon Proc Zool Soc London 1884 

Weldon thought the interplacentomal regions resembled the diffuse placenta of the pig. This may have been overinterpretation. There seem to be no subsequent descriptions of placentation in this species.

The Nilgai (Boselaphus tragocamelus)
Rufus46 (Wikimedia Commons) CC BY-SA 3.0

Together with the Nilgai, the Four-horned Antelope forms its own tribe. Benirschki examined a couple of Nilgai placentas (here). He did not find an unusual number of cotyledons but remarked they were not as neatly arranged in rows as in other species. So perhaps Weldon was on to something.

Raphael Weldon is not remembered for his placental research. He became a marine biologist and was professor of Zoology first at University College London then at Oxford. At UCL he collaborated with the mathematician Karl Pearson and founded the science of biometrics. Famously, he rolled a set of 12 dice no fewer than 26,306 times. The results showed a bias towards fives and sixes (more here). These data were used by Karl Pearson in the latter's seminal paper on the chi-square statistic.