Reproduction in domestic ruminants

ISBN13: 9781899043637

Every four years there is a conference on reproduction in domestic ruminants. The latest was held this August at Obihiro, which is on Hokkaido, the North Island of Japan. The accompanying book (details here) is a useful collection of reviews covering most aspects of male and female reproductive biology.

The opening chapter Ruminant phylogenetics: a reproductive biological perspective by William J. Silvia is an excellent overview that integrates molecular phylogenetics with morphology including various aspects of placentation.

There are several chapters on placentation including Early placentation and local immune regulation by Kazuhiko Imakawa and colleagues. This deals with transcriptional regulation of IFNT the gene coding for interferon-tau, which is secreted by the trophectoderm at the blastocyst stage and results in maternal regulation of pregnancy. Another topic is syncytins (previous post) in ruminants. In addition, I have contributed a chapter on Evolution of placental structure and function in ruminants.

Previous volumes in this series have appeared under the imprint of the journal Reproduction. Although the current volume conforms to that journal's format, it has been published in book form by Context. As far as I can make out, it is not possible to purchase individual chapters.

Placenta-derived exosomes and the immune response to pregnancy

Placental exosomes at the maternal-fetal interface
Reproduced with permission from Mincheva-Nilsson and Baranov Am J Reprod Immunol 2014
(c) 2014 John Wiley & Sons A/S

Exosomes are tiny vesicles (30-100 nm) released from living cells that facilitate intercellular communication (previous post). Exosomes are assembled by and released from the syncytiotrophoblast of human placenta. They carry molecules that could be of critical importance for suppression of the maternal immune response, which might otherwise cause rejection of the fetal allograft.

A brand new review by Lucia Mincheva-Nilsson and Vladimir Baranov (here) summarizes several mechanisms that might be involved and suggest "the placenta is surrounded by a cloud of exosomes that creates a beneficient and protective mileau for its existence." Among these mechanisms (summarized in the Figure) are reduced NK-cell cytotoxicity (through down regulation of the NKG2D receptor), impaired T-cell signalling, apoptosis of activated lymphocytes and effects mediated by TGF-beta that might include recruitment of regulatory T-cells (previous post).

There is more. The syncytiotrophoblast also releases much larger particles (0.2-2 micrometers) often referred to as STBM (for syncytiotrophoblast-derived microparticles). They are not carefully assembled as are exosomes but resemble a form of cellular debris. Importantly, they are pro-inflammatory with the potential to activate the immune system. Mincheva-Nilsson and Baranov hypothesize that placental exosome production may counterbalance the deleterious effects of STBM. They argue that determination of a normal range for the STBM/exosome ratio should be a research priority as it could lead to development of new diagnostic tools.

The Blakiston line

Thomas Wright Blakiston (1832-91)

Thomas Blakiston spent 23 years in Hakodate, one of the Japanese Treaty Ports opened to foreign trade in 1858. He failed in his original enterprise, to establish a saw mill, but flourished as a merchant. More importantly he made many observations as an ornithologist.

Blakiston was the first to observe that fauna of the northern island of Hokkaido differed from that of Honshu. Thus the Strait of Tsugara formed a zoogeographical barrier of a type similar to the Wallace Line (previous post). It is referred to as the Blakiston Line.

Blakiston's Fish Owl (Bubo blakistoni)

There is a memorial to Thomas Blakiston atop Mount Hakodate. In addition the former British Consulate, now a museum in the historic quarter of Hakodate, commemorates his several contributions. Blakiston's Fish Owl was named in his honour.

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.