A Denisovan signature in modern Tibetans

Tibetan family attending a horse festival (CC) Antoine Taveneaux 

Tibetans are adapted to life at high altitude. Compared to more recent arrivals, notably Han Chinese, they have much lower rates of fetal growth restriction and fewer pregnancy complications (reviewed here).

For non-adapted populations, long-term residence and high altitude can lead to chronic mountain sickness, which is characterized by high levels of haemoglobin. However, the erythropoietic response to low ambient oxygen is blunted in Tibetans. Recent studies have ascribed this to a variant allele of EPAS1, the gene that encodes hypoxia-inducible factor 2alpha (HIF2a) (here).

In the current issue of Nature, Huerta-Sanchez and others confirmed that the gene had a highly unusual haplotype in Tibetans (here). It occurred rarely in Han Chinese and was entirely absent in a larger set of worldwide populations. Interestingly, however, it could be detected in the genome af an ancient hominin population, the Denisovans (see previous post). The conclusion drawn is that the EPAS1 haplotype of Tibetans derives from admixture between modern humans and Denisovans.  

A downside to long gestation periods

Giraffe with calves - John Storr (Wikimedia Commons)

Giraffes (Giraffa camelopardalis) and the forest-dwelling okapi (Okapia johnstoni) are the survivors of a much broader radiation. Recently Clauss and Rössner (here) used the New and Old Worlds (NOW) data base of fossil mammals to examine the prevalence of various types of ruminant over time.

Rise and fall of tragulids 

The most basal group is Tragulidae, represented by present day chevrotains or mouse deer. In the Early Miocene they were the most prevalent ruminants but were subsequently displaced by the pecorans. The principal difference was the evolution in pecorans of an additional forestomach, the omasum, and this seems to have given them the edge over tragulids. 

Both tragulids and pecorans have synepitheliochorial placentation where binucleate trophoblast cells fuse with uterine epithelial cells at the fetal-maternal interface. However, tragulids lack the cotyledons typical of the placenta in pecorans.

Rise and fall of giraffoids

Among pecorans, Giraffidae is basal to both Bovidae (cattle, sheep, antelopes) and Cervidae (deer). Looking at the equivalent fossil clades, Clauss and Rössner found that Giraffoidea were much more  abundant in the later Early to Middle Miocene but then steadily declined to be supplanted by Bovoidea in Africa and by Bovoidea and Cervoidea in Eurasia. Why?

Based on extant species, the most striking difference between giraffids and other pecoran ruminants is their extremely long gestation - in excess of a year. Assuming this also was the case in fossil species, could that explain their decline? Clauss and Rössner argue that they were unable to develop a seasonal breeding pattern. This put them at a disadvantage compared to other pecorans with shorter gestation times such as bovids and cervids.  

Perhaps in support of this narrative, fossil giraffoids occupied a much greater range of ecological niches and many were grazers. The giraffes grew a long neck and survived as browsers in a special niche. The okapi is highly adapted to its restricted forest habitat.

Placentation in the giraffe has recently been described (see previous post).   

Menstruation in elephant shrews

Etendeka Round-eared Elephant Shrew or Sengi Macroscelides
micus. Image credit John P. Dumbacher
 

This post is prompted by the discovery in Namibia of a new species of elephant shrew or sengi, the smallest yet of the 19 species in the Order Macroscelidea. Elephant shrews are so named because of their mobile proboscis.





Midgestation conceptus of the Four-toed Elephant Shrew Petrodomus
tetradactylus. The embryo and fetal membranes are enclosed in the embryo
chamber by the decidua pseudocapsularis. Reproduced from
Oduor-Okelo et al. (here) (c) 2004 with permission from Elsevier

The report (here) mentions two pregnant females carrying one fetus in each horn. This suggests they may resemble other elephant shrews in that implantation of the blastocyst occurs in a preformed embryo chamber as shown above for Petrodumus tetradactylus. There is one such chamber in each horn. 

 

Should a female fail to become pregnant, the chamber is discarded in a process akin to menstruation. In most mammals transformation of the endometrial stroma to decidua occurs only following implantation. Exceptions are the catarrhine primates, including humans; if pregnancy does not ensue the decidua is shed together with blood and fluids (see previous post). In the 1940's, when human menstruation was poorly understood, Professor C. J. van der Horst of the University of Witwatersrand proposed using elephant shrews as a model. His suggestion was not followed as the establishment of a breeding colony of macaques at the Carnegie Institution of Washington provided a better alternative.

 

Placentation in elephant shrews was studied by van der Horst and others and more recently has been described by Dominic Oduor-Okelo (here and here). The placental disc has a labyrinth with a haemochorial structure and a spongy zone. In addition there is a paraplacenta. The allantoic sac is large and divided into four lobes. This last feature is a synapomorphy for the superordinal clade Afrotheria (discussed here).



Placental hormones and syncytins in the blind mole rat

A blind mole rat Spalax ehrenbergi
(Wikimedia Commons)

Mole rats (Spalacidae) occupy a basal position in the superfamily Muroidea. The blind mole rats, Spalax spp., are highly adapted to a subterranean lifestyle. They are resistant to both spontaneous cancer and carcinogens. For all these reasons they are widely studied and now we have a description of the genome of one species S. galili and the placental transcriptome both of that species and of S. carmeli (here).

Placental hormones

Placental-specific genes known from mouse and rat (Muridae) include cathepsins, placental lactogens (derived through duplication of the prolactin gene) and pregnancy-specific glycoproteins (reviewed here). Orthologues of many of these genes were present in Spalax and given the basal position of Spalacidae this indicates they had started to diversify in the last common ancestor of the muroid rodents.

Syncytins

Syncytins are endogenous retroviral envelope proteins thought to be essential for the formation of syncytiotrophoblast (previous post). Two such genes are known from mouse, rat (Muridae) and hamster (Cricetidae). Both are present in the Spalax genome although only Synb was confirmed in the placental transcriptome. This extends the timing of the env gene capture further back in time to an estimated 45 Mya.

Globin genes

Beta globin genes code for the two chains of haemoglobin molecules. One of them HBG is expressed in the embryo of most mammals but in the fetal haemoglobin of higher primates (discussed here). The HBG of Spalax shows evidence of rapid sequence evolution under positive selection. It is not clear to what extent this affects its affinity for oxygen.

Placentation in a marmot: the woodchuck

Woodchuck or groundhog (Marmota monax)
CC Wikimedia Commons

Not much has been written about placentation in squirrels and other sciuromorph rodents - at least in comparison to myomorphs (e.g. mouse, hamster) and hystricomorphs (e.g. guinea pig, capybara). Marmots belong with chipmunks and ground squirrels in the Tribe Marmotini. The most complete description is for the thirteen-lined ground squirrel (Ictidomys tridecemlineatus) (Mossman & Weisfeldt Am J Anat 1939;64:59-109). It was based largely on specimens collected a century ago by Thomas George Lee (background here).

Interhaemal region in the labyrinth of a woodchuck placenta
Marmota monax Courtesy of Dr. Allen C. Enders

The woodchuck has a labyrinthine, haemochorial placenta. In the above section the large channels with maternal red cells are lined by syncytiotrophoblast. A fetal capillary is seen to the right.

Early Development of the placenta in the Colorado chipmunk
Tamias quadrivittatus Courtesy of Dr. Allen C. Enders

There are several ways to make a haemochorial placenta (discussed here). Squirrels go through a transient endotheliochorial phase. The figure is from a chipmunk and shows a maternal capillary in which part of the endothelium has been replaced by syncytiotrophoblast whilst two endothelial cells remain intact (further figures here). In the first instance this creates the equivalent of the spongy zone found in other rodent placentas.

Later the fetal mesoderm grows into the trophoblast bringing with it the fetal capillaries. To start with the outgrowths are fingerlike (villi) as can be seen in a recent publication on the woodchuck (here). Nearer term, however, the labyrinth occupies most of the depth of the placenta. The spongy zone is then very thin and occupied by syncytiotrophoblast with clumps of nuclei as well as mononucleate giant cells (Dr. Allen C. Enders, personal communication).

Syncytins are endogenous retrovirus envelope genes (previous post). Two occur in murid rodents and another in South American hystricomorphs. Now a search of the genome of the thirteen-lined ground squirrel has turned up several candidates and further work in the woodchuck has shown one of them to be a bona fide syncytin. By in situ hybridization the gene was not expressed in the labyrinth but rather in the part of the spongy zone that had yet to be reached by the fetal vessels.

Evolution of Neotropical primates

Geoffroy's spider monkey (Ateles geoffroyi)
Wikimedia Commons

Derek Wildman's Group at Wayne State University have re-examined the evolution of Neotropical primates (here). Using genomic data from 36 species they derive a tree with few surprises but better support than in other recent analyses.

What I found interesting is their attempt to place platyrrhine evolution in a biogeographical context. They suggest that the most recent common ancestor of extant species lived in what today is the Amazon rain forest, Guiana Shield and Northern Andes. Then, however, this was largely an area of lowlands and mountains. In support of their interpretation, known fossil sites are within this region. They further suggest that diversification of platyrrhines occurred with the establishment and development of the Amazon rain forest. 


Placenta of the white fronted capuchin (Cebus albifrons)
From Carter and Mess (here)

The founder of the Neotropical primates arrived in South America during the Oligocene when the continent was completely isolated from other land masses. Personally I favour the view (espoused here) that they came by a transatlantic route. However, Jameson Kiesling et al. suggest they may have come directly from Asia. In support they cite the occurrence of all the early fossils on the west side of the continent and recent evidence that platyrrhines may have emerged in Asia rather than Africa. In either case the means of dispersal was most likely by rafting (see previous post on sweepstakes distribution).




Homo habilis - fiftieth anniversary

Homo habilis the handy man (Wikimedia Commons)

An article in the current issue of Nature (here) reminded me that 50 years have passed since Louis Leakey, Phillip Tobias and John Napier published their controversial paper, "A new species of the genus Homo from Olduvai Gorge" (here). Until then most fossil hominins had been accomodated in the genera Australopithecus and Pithecanthropus. Whether or not the new fossils justified the title of Leakey's paper was disputed then and remains contentious.

As I wrote at the time, "There are two criteria that might be used to define man: his ability to make tools and the size of his brain. Homo habilis scores on the first point but not on the second" (Carter AM. A new ancestor for man. The Humanist 1964; 79: 198-201).

Happy Birthday Jane Goodall

I was reading anthropology while the paper was being written and was taught by both Phillip Tobias and John Napier. I also met Louis Leakey on one of his visits to Cambridge - probably angling for a job - and was introduced to his protégée, the then unknown Jane Goodall (whose 80th birthday is today).