The origin of apes



The Rift Valley Kenya (Wikimedia Commons)

Trees based on molecular data often predict divergence points at odds with the fossil record. Thus the divergence between Old World monkeys (Cercopithecoidea) and apes (Hominoidea) has been dated to 25-30 Mya, implying a long ghost lineage for both superfamilies. New fossils from the East African Rift have now closed the gap (here). One (Nsungwepithecus gunnelli) is a cercopithecoid. The other (Rukwapithecus fleaglei) shares dental features with Miocene and extant hominoids that are not present in cercopithecoids.

Pregnant uterus of Hylobates agilis (rafflei) showing the decidua

capsularis (d.c.) reproduced by Hill (here) from Selenka

Implantation is superficial in Old World monkeys, whereas interstitial implantation occurs in all living apes including gibbons. This was shown more than a century ago by Emil Selenka. The illustration above is of Hylobates rafflei named in honour of Stamford Raffles (previous post) but now subsumed in H. agilis.

Trophoblast invasion by the interstitial route occurs neither in Old World monkeys nor in gibbons so post dates the origin of apes. This key feature of human placentation is shared by gorilla and chimpanzee (discussed here). No information is available for orang utan.

Placentation in the Laotian rock rat

The Laotian rock rat Laonastes aenigmamus
From Nicolas et al. 2012 (here)

Discovered in 1997, this rodent belongs to the family Diatomyidae that was thought to have died out in the late Miocene (background here). Molecular data place it basal to hystricognath rodents such as the guinea pig and capybara.

Cross section through the rock rat uterus, placenta and fetal membranes

Reproduced from Carter et al. © (2013) with permission from Elsevier 

The internal structure of the placenta was rather simple with a separate labyrinth and spongy zone. In contrast, the hystricognath placenta is highly folded with lobules of labyrinth separated by interlobular areas of spongiotrophoblast.

Thin section through the exchange area of a rock rat placenta

Reproduced from Carter et al. © (2013) with permission from Elsevier 

The interhemal barrier was hemodichorial, i.e. with two trophoblast layers. The maternal blood spaces (mbs) were lined by syncytiotrophoblast (syn tr) and below this was a layer of cytotrophoblast (ctr). This pattern is different from all other rodents that have been studied so far.

Some distinctive features of hystricognath placentation, such as the subplacenta, were not found in the Laotian rock rat. On the other hand this species does resemble hystricognaths in giving birth to a single precocial pup.

Disclosure: I am lead author of this paper and must acknowledge my colleagues Jean-Pierre Hugot (Paris), Allen C. Enders (Davis), Carolyn J. P. Jones (Manchester) and Par Kham Keovichit (Vientine).

More news from Denisova

Denisova Cave, Altai Mountains, Siberia

ЧуваевНиколай at ru.Wikipedia

At various times the Denisova Cave has been occupied by modern humans, Neanderthals and the eponymous Denisovans. For the latter we have too few bones to reconstruct a skeleton yet enough DNA to explore the genome (here). The results indicate that there was gene flow between Denisovans and modern humans as previously shown for Neanderthals.

In a preliminary report (here) we learn that a group led by Svante Pääbo has sequenced the genome of the Neanderthals that lived at Denisova. They were a population distinct from those in Croatia and the Caucasus (for which there also is genomic data). Interbreeding between humans and Neanderthals is more likely to have occurred in the Caucasus than at Denisova.

Intriguingly, however, the study found evidence of interbreeding between the local Neanderthals and the Denisovans and - even more remarkably - evidence of contribution to the Denisovan gene pool of yet another hominin.

Possible significance for human reproduction

The highly polymorphic HLA class-I antigens (HLA-A, -B and -C) play important roles in the immune response to infection as well as in reproduction. A previous study (here) showed that interbreeding with archaic populations, and subsequent conservation by natural selection, has made a significant contribution to the HLA system in human populations outside Africa.

Some of the introgressed HLA allotypes code for proteins that are ligands for killer-cell immunoglobulin-like receptors (KIRs) including ones thought to be important in relation to human reproductive failure (here).

Work is in train to align the genomes of the chimpanzee, Neanderthals, Denisovans and modern humans. The secrets revealed by the remains from Denisova may ultimately contribute to our understanding of human reproduction.

Elizabeth Maplesden Ramsey

Elizabeth Ramsey lecturing at Rotterdam in 1980

A legend in her lifetime Elizabeth Ramsey was always kind to young investigators and an inspiration to women scientists. She wrote a slim volume on The Placenta of Laboratory Animals and Man that offers valuable insight into the realm of comparative placentation. 

Twenty years have passed since her death. As a researcher Elizabeth is best remembered for two things. At the very start of her career as a pathologist she discovered a very early human implantation site, the Yale embryo. This marked the start of her affiliation with the Carnegie Institution of Washington from 1934 until well beyond her retirement.

Corrosion cast of vessels in a rhesus monkey placenta. Maternal spiral artery red and fetal vessels white. The handwriting is Elizabeth Ramsey's

Second she studied the maternal placental circulation in the rhesus monkey and other primates beginning with 3D wax reconstructions of the blood vessels and proceeding through corrosion casts (above) to visualization of the blood flow by cineradioangiography. An appreciation of this work in its historical context has been written by Larry D. Longo and Giacomo Meschia (here).

My personal debt to Elizabeth dates back half a century when I was an undergraduate. In reply to my letter she sent many words of encouragement and reprints of her papers. It was typical of her generosity. 

Why are there more marsupials than placentals?

One answer could be that reproduction in marsupials with their choriovitelline placentation and highly altricial neonates put them at a disadvantage in competition with placentals. A thoughtful essay by Marcelo Sánchez-Villagra (here) challenges that interpretation.

First he argues that metatherians were more severely impacted by the mass extinction event at the Cretaceous-Paleogene boundary. Crown marsupials (the living species and their common ancestor) post date that event. In contrast crown placentals originated in the Cretaceous. (For Metatheria vs. Marsupialia and Eutheria vs. Placentalia please refer to my previous post).

An ungulate Theosodon garretorum and a carnivorous metatherian

Borhyaena tuberata from the Santacrucian (Early Miocene) of South America

Second the fossil record does not support the notion that one group of mammals out-competed the other. In the Late Cretaceous, for example, metatherians were more abundant than eutherians in the North American fauna. In South America, eutherians such as the native ungulates went extinct, whereas metatherians including crown marsupials survived. (Most of the present fauna, including rodents and Neotropical primates, arrived later, as discussed here.)

Third the metatheria that did survive into the Paleogene were (with very few exceptions) confined to the Southern continents of Antarctica, Australasia and South America. Major clades of placentals that show a comparable distribution are Xenarthra (armadillos, anteaters and sloths) and Afrotheria (including elephants, hyraxes and tenrecs). There are 35 extant species of xenarthrans and 83 afrotherians against 340 marsupials.

Thus the discrepancy in species richness between marsupials and placentals is due to the success of the remaining clades, Euarchontoglires and Laurasiatheria, that evolved mainly in the Northern continents and reached Africa and South America much later.

Perhaps the chorioallantoic placenta did give the edge to placental mammals. But Sánchez-Villagra argues convincingly that even if developmental biases exist those constraints can be circumvented. They cannot fully explain why there are 15 times more placentals than marsupials in the present day fauna.

Sir Stamford Raffles and the moonrat

Implantation site of the moonrat Echinosorex gymnura

(Raffles 1821) Hubrecht Collection

After Hubrecht had described placentation in the hedgehog (previous post) he travelled to Indonesia and obtained specimens of its relative the moonrat. As the micrograph shows, implantation occurred in a pocket in the endometrium, just as in the hedgehog. He published this finding in Annales du Jardin Botanique du Buitenzorg (1898 Suppl. 2: 159-167). Historically, Bogor or Buitenzorg was the summer residence of the Governor General of the Dutch East Indies.The botanical gardens at Bogor are among the largest in the world.

Sir Thomas Stamford Bingley Raffles FRS

There was a brief interlude when Java was under British rule with Sir Stamford Raffles as Lieutenant Governor. Raffles is best remembered for founding Singapore. He was also co-founder of the Zoological Society of London and its first president. A biography of Raffles by Victoria Glendinning appeared last year (reviewed here).

Memorial to Olivia Mariamne Raffles née Devenish

Bogor Botanical Gardens (Wikimedia Commons)

Raffles' sojourn on Java ended in misfortune: his first wife Olivia died there in November 1814. Raffles erected a memorial to Olivia in the Bogor Botanical Gardens. In the following year Raffles was relieved from his post.

Moonrat (Echinosorex gymnura) drawn by J Briois

Raffles Collection, British Library

In London Raffles was knighted and elected FRS, but his next posting, to Bencoolen on Sumatra, was in essence a demotion. However, with time on his hands, he could devote more of his zeal to natural history. Several species are named after him as is a genus of parasitic plants, Rafflesia, known for their smell as corpse flowers. The moonrat was described by Raffles in a "Descriptive Catalogue of a Zoological Collection, made on account of the Honourable East India Company, in the Island of Sumatra and its Vicinity, etc." (Trans Linnean Soc London 1821; 13: 239-74).

Apart from Hubrecht there is only one paper on placentation in the subfamily Galericinae, which comprises the moonrat and other gymnures (here).