Placentation in bovids: can we learn more?

Princeton University Press 2016 ISBN-13: 9780691167176

Field guide or doorstopper? Just published as a Princeton Field Guide, this tome runs to 664 pages and weighs 1.3 kg. It aims to be, "The first comprehensive field guide to all 279 bovid species." Where did that total come from when Mammal Species of the World recognizes half the number?


Johns Hopkins University Press 2011 ISBN-13: 978-1421400938

The answer is the above book on ungulates (hoofed mammals) with a revised taxonomy based on the authors' Phylogenetic Species Concept (PSC). A useful comparison between old and new species can be found at the ultimateungulate site. 

Ungulate Taxonomy was criticised by Frank E. Zachos and colleagues both in a letter to Nature (here) and in a detailed critique (here). They argued that splitting of species was a worrying trend with unfortunate implications for conservation efforts.

Bovid placentation

I bought both these books because bovid placentation deserves further study. Two major clades are recognized. Bovinae include domestic cattle (Bos taurus) and the zebu (B. indicus) - the latter was raised to species status by Groves and Grubb, which should please my Brazilian colleagues.

Antilopinae is less well studied although it does include domestic sheep (Ovis aries). A large amount of antelope material is available in The Harland W. Mossman Collection together with detailed field notes by the principal collector Archie S. Mossman.

Placenta of a klipspringer (Oreotragus oreotragus) with a binucleate cell
From Comparative Placentation courtesy of Dr. Kurt Benirschke

There is much to be done. And which of the rival terminologies should we use? I chose this rather fuzzy image of a klipspringer because Groves and Grubb chose to split it into no less than 11 species. Zachos et al. call this, "a prime example of rash taxonomic conclusions derived from inappropriate data." Even if their judgement is too harsh, the fact remains that this San Diego Zoo specimen cannot be assigned with confidence to any one of those  11 species. We might be on better ground with the Mossman material as it was collected in the wild at known localities and many of the "new" species have clearly defined (often restricted) ranges.

Placentome of a sable antelope (Hippotragus niger)
From Comparative Placentation courtesy of Dr. Kurt Benirschke

Hradecky wrote several papers on placentation in antelopes based mainly on the Mossman material and partly on specimens supplied by Benirschke (e.g. here). A set of his slides is in the Mossman Collection and some reproduced on the Benirschke web site.
 

Handbook of the Mammals of the World

PSC may be a valid taxonomic approach inasmuch as the premisses are defined and understood by experts. But there was renewed controversy when the Groves and Grubb taxonomy was incorporated in Volume 2 of Handbook of the Mammals of the World. Heller et al. (here) criticised PSC and concluded, "Conveying the message to the public that global diversity is on the decrease ... is unnecessarily confounded when the number of bovid species has just doubled without sufficient justification."

Perhaps the same criticism could be levelled at the new field guide. It does, however, have the virtue of supplying an illustrated version of Groves and Grubb - a book that was strangely lacking in pictures (as noted here). Trophy Hunters will find it a useful aid to bagging yet more species.

 

  

  

Treasure houses under threat

The Field Museum Chicago
by Juanfibarra Wikimedia Commons CC BY 2.5

Museums house vast collections of specimens. For major museums of Natural History, these can be numbered in tens of millions. The specimens of greatest interest to embryologists will be in the wet collection and preserved as a rule in alcohol. Curating these specimens is an expensive business. When Chicago's Field Museum built a new Collections Resource Center the bill ran to $65 million and so stretched the budget that it resulted in cuts to museum staff (here).

Cross section through placental disc of a web-footed tenrec
(Limnogale mergulus) from Enders et al. (here). FMNH 165440

Now museum collections in the US are under further threat as the National Science Foundation has suspended its funding for the maintenance of biological research Collections (here). This is a matter of great concern.

Thanks to the Field Museum were able to describe the placenta from a rare specimen of an aquatic tenrec (above). We also used Field Museum specimens when reviewing the reproductive organs of bats (here).

Gravid uterus of a chimpanzee (Pan troglodytes) from the Hill Collection
currently housed at Museum für Naturkunde Berlin

Some museums house dedicated collections of embryological material. The J. P. Hill Collection is a good example and we have used it for several projects, including the first description of deep trophoblast invasion in a non-human primate (here).

The history of this collection is instructive. After Hill's death in 1954 it was stored in the attic of Dixon Boyd's house in Cambridge. It subsequently found what seemed to be a permanent home at the Hubrecht Laboratory in Utrecht. Together with the Hubrecht Collection it was eventually kept in a purpose built facility of a new building. With a change of director this space was seen as more suitable for -70 freezers and the future of the collection remained uncertain until it was removed to Berlin. The director subsequently became President of the Royal Netherlands Academy of Arts and Sciences! 

Genome of the spotted gar

Spotted gar (Lepisosteus oculatus)
Brian Gratwicke  CC BY 2.5 (Wikimedia Commons)

Not all bony fish are teleosts. Teleostei is an infraclass of ray-finned fish (Actinopterygii) with bichirs, sturgeons and gars (some 50 species) all basal to to the more numerous teleosts (some 30,000 species). The phylogeny of bony fishes has been largely resolved by Near et al. (open access).

Alligator gar (Atractosteus spatula) Moon Lake, Mississippi. March 1910, Photographer D. Franklin,
American Museum of Natural History (public domain)

 

Romer's Man and the Vertebrates did not make much of garpikes, but did include a great photo (shown above) of the largest species. My yellowing copy predates the genetic code yet alone genomics.

What we now know is that teleosts are characterized by the Teleost Gene Duplication (TGD). This event was followed by rapid sequence evolution that may explain their success as a group. It can, however, make it difficult to identify orthologs to tetrapod genes and frustrate interpretation of data obtained in zebra fish (Danio rerio). To provide a bridge, Braasch et al. have sequenced and have just published the genome of the spotted gar (open access).

To my knowledge no living species of the gar family is viviparous.

Placenta of the gray four-eyed opossum

The gray four-eyed opossum (Philander opossum) by André de Souza Pereira
Wikipedia Commons CC BY-SA 3.0

The gray four-eyed opossum (Philander opossum) is widely distributed in South and Central America. Its placentation has been described from animals caught on Barro Colorado Island in Panama (here).

Yolk sac of Philander opossum. The sinus terminalis marks the transition
between the avascular and vascular portions.
Courtesy of Dr. Allen C. Enders

As in the Virginia opossum, the yolk sac is comprised of avascular and vascular portions. The avascular part follows the contours of the uterine epithelium (at left in the figure). The vascular portion attaches to it (at right).

Semi-thin section of vascular yolk sac (at top) and fold in the uterine
wall (below) in Philander opossum.
Courtesy of Dr. Allen C. Enders

The study of Philander by Enders and Enders was the first to show invasive trophoblast in a marsupial. In the figure there is a fold of uterine wall with intact epithelium at left and right, but this has disappeared at the centre of the fold, which is occupied by large trophoblast cells. Subsequently invasive trophoblast has been described in another opossum (Monodelphis domestica) and in an Australian marsupial (Sminthopsis crassicaudata).

Photomontage of a section through one uterus of Philander opossum.
The two fetuses share a common yolk sac, but each has its own
allantoic sac one of which can be seen.
Courtesy of Dr. Allen C. Enders

An unusual feature in Philander is that two or more fetuses share a common yolk sac. However, each has its own allantoic sac. The allantois never makes contact with the trophoblast (it remains within the small exocoelom). It may serve as a receptacle for urine secreted by the mesonephros. 

Placentation in opossums

Embryo of Virginia Opossum (Didelphys virginiana) at 6 days
of gestation. Opened to show the vessels of the trilaminar yolk sac
and free-floating allantoic sac. From Selenka 1886.

Emil Selenka did not confine himself to rodents and primates (previous post and recent review). He also gave the first detailed description of embryonic development in a marsupial, the Virginia opossum. He bred them in the laboratory and thus had dated pregnancies.

All marsupials have a yolk sac placenta with both two-layered and three-layered areas (bilaminar and trilaminar omphalopleure); the latter has blood vessels that radiate from a sinus terminalis as can be seen in Selenka's illustration.



Neonate of Virginia Opossum. From Selenka 1886.

The Virginia opossum has a pretty short gestation even for a marsupial. The neonate above was born after 13 days. Development is supported largely by histotrophic nutrition, i.e. uptake of uterine gland secretions. The vascular part of the yolk sac is thought to be more important for gaseous exchange.

Note that the allantois makes no contact with the trophoblast. Unlike in the koala, wombat and bandicoots, there is nothing approaching chorioallantoic placentation. The allantois serves mainly as a receptacle for urine excreted by the mesonephros (here). 

Virginia Opossum (D. virginiana) by Cody Pope CC BY-SA 2.5
(Wikipedia Commons)
 

There are 87 species of didelphids in Central and South America, but the Virginia opossum is alone in extending its range to the USA and Canada.

Despite the species richness, placentation has been described for only five opossums; three from the same genus (D. virginiana, D. aurita and D. marsupialis) plus the gray short-tailed opossum (Monodelphis domestica) and gray four-eyed opossum (Philander opossum). I will save them for a later post.

Gorilla-human split - implications for the evolution of deep trophoblast invasion

Lowland gorilla (Gorilla gorilla) female and young
at the Bronx Zoo - Wikipedia Commons (CC-BY-SA 3.0)

The fossil Chororapithecus abyssinicus is the earliest known species of gorilla. A recent paper (here) dates this fossil and calculates that the split between the gorilla and human lineages occurred more than 8 million years ago (Mya). This agrees well with an estimate based on genomic data (here) putting the gorilla-human split at 7.6 to 9.7 Mya.

Placenta of Gorilla gorilla showing invasion of decidua (at left) by
trophoblasts (black stain) following the interstitial route;
villi and intervillous space  are at right

We have shown that trophoblast invasion in gorilla and chimpanzee resembles that in humans. For example there is invasion by the so called interstitial route which does not occur in monkeys or in lesser apes such as gibbons (reviewed here and previous post).

Fetus of Gorilla gorilla photographed by Louis Bolk
Courtesy of Dr. Laurens de Rooy, Museum Vrolik, Amsterdam

Gravid uteri of great apes are not easy to come by; one of the gorilla placentas we saw was collected by Louis Bolk in 1923. He described the fetus (here) and sent the placenta to J. P. Hill in London. 

We have not been able to find a gravid uterus of an orangutan. The split between orangutan and other great apes was as deep as 15-19 Mya (here). It would be interesting to know whether human-like trophoblast invasion evolved before or after that.

Marsupial frogs

Female Brazilian tree frog (Flectonotus pygmaeus) with
brood pouch enclosing the developing embryos
(Mauricio Rivera Correa ShareAlike 2.5)

What happens when frogs abandon their amphibious lifestyle for a more terrestial one? Frogs in the Family Hemiphractidae from South and Central America have evolved some ingenious solutions.

In hemiphractids, the embryo develops on the back of the mother either in a mucous-filled depression or in a closed pouch - as shown above for a Brazilian tree frog (the embryos are under the bumps).

Froglet of a marsupial frog (Gastrotheca ovipera) showing
the external gills. From Nathan 1932 (here)

The embryos may develop into tadpoles and be released to water-filled cavities in plants or skip the tadpole stage and develop directly into froglets. In species of the genus Gastrotheca, embryos have 1-2 pairs of external gills that serve for respiratory gas exchange with maternal tissues in the brood pouch. This would satisfy most people's definition of a placenta. The gills are shed around the time of birth.

Marsupial Frogs by William E. Duellman 2014
Johns Hopkins University Press ISBN 978-1-4214-1676-5

The biology of marsupial frogs is described in painstaking detail in this new book - the destillation of a lifetime's work by William E. Duellman (details here). It is superbly illustrated but at USD 120 a bit pricey. More than half the content comprises species accounts and no doubt it will find a place on the bookshelf of specialists. But it is well worth checking out for its insights into the reproductive biology of frogs. Who knew, for example, that the oocytes of Flectonotus pygmaeus have up to 2000 nuclei reduced during oogenesis to a single one?

For other fun facts on frog reproduction see this video.