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).

Decidual and endometrial macrophages

Generic macrophage (Wikimedia Commons)

Macrophages are ancient cells. There are multiple lineages in mammals, some of which originate in the yolk sac rather than being the progeny of bone marrow-derived monocytes (reviewed here).

Macrophages constitute some 25% of the leukocyte population in the human uterus. Because there is cyclical recruitment of macrophages to the uterus, they are thought to be recruited from Ly6c⁺ inflammatory monocytes. Interestingly, however, when monocytes are differentiated in vitro, the cells resemble but are not identical to decidual macrophages (here).

One of the factors acting on decidual macrophages is human leukocyte antigen G (HLA-G) derived from trophoblast.  An HLA-G homodimer can bind to the LILRB1-Fc fusion protein on the surface of macrophages. However, HLA-G is a novel member of MHC Class I found only in higher primates, so this mechanism is not relevant to all mammals.

Ruminants

Macrophage differerentiation from Oliveira et al. (here) CC licence

Macrophages are abundant in the endometrial stroma of the bovine uterus especially in the regions between placentomes. There is evidence that these belong to the alternatively activated macrophage category (M2 pathway) and are endowed with immunosoppressive properties (here).

Genome of the Coelacanth

West Indian Ocean coelacanth (Latimeria chalumnae) Wikimedia Commons

I remember how exciting it was when the second specimen of a coelacanth was caught in 1952. This "living fossil" was widely reported in the newspapers. Perhaps it was a formative moment.

Now the coelacanth genome has been sequenced and annotated (here).

The coelocanth is oviviviparous. Five fully developed young with attached yolk sacs were found in the right oviduct of a female specimen at the American Museum of Natural History (here). There was no indication of placentation but it is but a short step from ovoviviparity to placental viviparity - the more critical step being evolution of intromission.

The new report applied phylogenomics to look for genes that might have been significant in the transition from water to land. A number of developmental genes present in the coelocanth were lost in tetrapods. However, Hox genes, which determine overall body plan, were well conserved. An interesting exception was Hoxa14 and hereby hangs a tale. A conserved non-coding element associated with Hoxa14 in the coelacanth (HA14E1) was retained in tetrapods. It is speculated that it might have been recruited to coordinate nearby genes (Hoxa13, Hoxa11 and Hoxa10) that are critical in formation of mammalian fetal membranes.

Placentation in the American moles

Eastern American Mole (Scalopus aquaticus) Wikimedia Commons

Harland Mossman was an astute observer. When he reported that the Eastern mole (seen above) had a diffuse epitheliochorial placenta, people took notice. It was 40 years before the evidence was laid out (here) and ever since it has been controversial.

Malassiné and Leiser (here) examined the placenta of the European mole (Talpa europaea) and found it was endotheliochorial. A recent study of a related species (T. occidentalis) (here) arrived at the same result.

So do European and American moles differ in their placentation? A side by side comparison of electron micrographs (found here) opens the possibility that different labels were given to analagous structures.

The Prasad thesis

M.R.N Prasad Wikimedia Commons

Mossman had quite a collection of American mole placentas and entrusted them to a graduate student M.R.N. Prasad. But is clear from Prasad's 1958 thesis and from the annotated versions of an unpublished manuscript that his findings did not support Mossman's interpretation. The story is told in detail elsewhere (here). Prasad was a Fulbright scholar and later had a distinguished career as a reproductive endocrinologist and WHO expert. The Indian National Science Academy has a Professor MRN Prasad Memorial Lecture.

Prasad claimed the initial stages of placentation were invasive with loss of the uterine epithelium. This was at odds with Mossman's theoretical framework. Later in development, however, Prasad found signs of a re-establishment of the uterine epithelium. The placenta of Scalopus started off endotheliochorial (as later described for Talpa) but reverted to epitheliochorial. This interesting interpretation cries for re-examination using more sophisticated methods than were available to Prasad.

Evolution of oxytocin and the oxytocin receptor

Evolution of vasopressin and oxytocin family of nonapeptides

From Gwee et al. (here) © 2008 Gwee et al; licensee BioMed Central Ltd.

Delivery of the fetus and placenta depends in part on the action of oxytocin (a pituitary hormone) on oxytocin receptors in the myometrium. Duplication of the vasotocin (VT) gene of lampreys was the basis for the evolution of oxytocin (OT) and arginine vasopressin (VP).

A fresh study (here) confirms this scenario but takes a closer look at the evolution of the receptors. There are three receptors for vasopressin and one for oxytocin. In essence the hypothesis is that these arose during the whole genome duplications that are thought to have occurred early in the evolution of vertebrates. It is noted that these two rounds of duplication would in theory have produced four vasotocin genes. If so, three were lost and the fourth only later gave rise to the oxytocin gene by a separate tandem duplication event. The gist of the argument is that the receptor evolved first.

Whilst oxytocin acts on the mammary glands and uterus of mammals, vasopressin acts on the kidney. In addition, both peptides act as neurotransmitters in the brain. Yamashita and Kitano suggest the neurotransmitter role came first. Only later were receptors expressed in peripheral organs such as the uterus and the peptides secreted as hormones from the posterior pituitary.

Alfred Russel Wallace

Alfred Russel Wallace from the frontispiece of Darwinism 1889 



The current issue of Nature (here) carries an appreciation of Alfred Russel Wallace, who independently of Darwin hit upon the principle of natural selection. He had a firm grasp of the species concept based on his experiences in Amazonia. In 1852 he reported on the distribution of Neotropical primates writing, "I soon found that the Amazon, the Rio Negro and the Madeira formed the limits beyond which species never passed" (On the monkeys of the Amazon Proc Zool Soc Lond 1852; 20: 107-110).

Humming-bird fertilizing Maregravia nepenthoides

from Darwinism 1889 

Wallace was based on Barra at the confluence of the Amazon and the Rio Preto. During the subsequent rubber boom it was transformed to the prosperous city of Manaus with a world class opera house. It is now home to the prestigious National Institute of Amazonian Research (INPA). Wallace's expedition, however, ended with the loss of many of his specimens in a fire on the ship that was to have carried him back to England.

The man who knew islands

Next Wallace went to Indonesia. His work there is recounted in The Malay Archipelago (1869), as reviewed in a companion article in Nature by Richard Quammen. Wallace is regarded as the father of biogeography. Quammen devoted a long chapter to him in the prize winning book Song of the Dodo (reviewed here). Among his legacy is the concept known as the Wallace Line, a water barrier that separates the Southeast Asian and Australasian flora and fauna. If you are planning a trip to Bali remember to include the Gili Isles and you will cross the Wallace Line as you go. 

To finance his travels, Wallace collected many specimens of the same species. As Quammen writes, "one effect of this redundant, commercial collecting was that he saw intraspecific variation laid out before him." This led him to the principle of natural selection, which Darwin was slow to gestate.