Placentation in sloths

Placenta and fetal membranes of Hoffmann's Two-toed
Sloth (Choloepus hoffmanni) from Turner 1872

Two recent papers cast light on the evolution of sloths. Delsuc and colleagues obtained mitochondrial genomes from living and extinct sloths (here) while Presslee and colleagues used proteomics to describe Type I collagen - likewise from extant and extinct species (here). They agree that notions of sloth evolution based on morphology need revision. 

It was confirmed that two-toed and three-toed sloths are not closely related and group with different forms of ground sloths. A third group with a suspensory life style was found to have diverged even earlier. These sloths crossed a land bridge to the Greater Antilles and went extinct just a few thousand years ago.

Interhaemal barrier of the pale-throated three-toed sloth
(Bradypus tridactylus) Courtesy of Allen C. Enders

Together with anteaters and armadillos, sloths belong to the ancient superorder Xenarthra. Armadillo placenta has been studied in some detail. It is villous haemochorial (discussed here). Anteater placentation is rather similar (previous post). Sloths are different. As shown by Turner, the placenta is lobulated in appearance. It is labyrinthinre and endotheliochorial (here).

Given current opinion on the relations between sloths (Folivora), anteaters (Vermilingua) and armadillos (Cingulata), parsimony dictates that their common ancestor would have had a villous haemochorial placenta. Thus the sloth placenta represents a derived state. The most recent common ancestor of two-toed and three-toed sloths lived >25 million years ago whereas sloths diverged from anteaters >50 mya. 

Lagoa Santa skulls still perplex Danes

Peter Wilhelm Lund (1801-1880)
Danish National Library (public domain)

When Peter Lund excavated human remains from Sumidouro Cave he was thoroughly perplexed. Not least because they were jumbled together with the bones of an extinct megafauna. This was in 1840 so well before Darwin had published On the Origin of Species (which cites Lund's work).

The skeletons were shipped to Copenhagen and examined there by several distinguished anthropologists (Lund never returned to Denmark). The consensus that arose was that "Lagoa Santa Man" was unrelated to present-day Native Americans. 

Springer 2017: ISBN 978-3-319-57465-3

Research and debate was renewed in the last century with new excavations in the caves near Lagoa Santa (now a suburb of Belo Horisonte). A key find was Luzia, a skull feared lost in the recent fire at the National Museum in Rio de Janeiro (previous post) (it survived but suffered heat damage). This skull was dated to 11,000 years ago.

Comparisons have been drawn between the features of the Lagoa Santa skulls and those of Australasian peoples such as Andaman Islanders. What can genomics tell us? A first set of clues hinted at an early wave of migrants designated "Population Y" who left a genetic signature that is strongest in some isolated Brazilian communities (see my review of David Reich). 

Skull from Sumidouro Cave excavated by Peter Lund

Now a Dane has ventured into the Lund Collection and extracted ancient DNA from a 10,400 year-old skull. The results appeared in Science last December (here). Eske Willeslev and his group found a clear Australasian genomic signature that was absent in other ancient remains from the Americas. They concluded this signal, "implies that an early group possessing it had disappeared or that a later-arriving group passed through North America without leaving any genetic trace." A conclusion echoed by the lead author, José Victor Moreno-Mayar, who simply said (here), "How did it get there? We have no idea."

It seems the Lagoa Santa remains are just as perplexing to Willerslev as they were to Lund and for a similar reason: they do not neatly fit into the scheme of things.

Postscript

The Willerslev paper is really worth reading. It builds on earlier work to confirm that Native Americans (other than Inuits) derived from a group that split from East Asians and resided in Beringia (Ancient Beringians). As they advanced into the Americas at the end of the Ice Age there was an early split into Northern (NNA) and Southern Native Americans (SNA). The SNA dispersed rapidly south of the remaining ice some 14,000 years ago. In a later phase there was admixture from a population in Mesoamerica that migrated both north and south. Another paper on ancient DNA from the Reich group also found evidence for rapid expansion into South America (here), but did not have Lagoa Santa in the data set.

Why Luzia was important

Cast of the skull known as Luzia as displayed at
National Museum of Natural History Washington DC
Photo by Ryan Somma CC BY-SA 2.0

Luzia was excavated from Lapa Vermelha, Minas Gerais, Brazil and was the oldest human fossil from South America. She was found in strata dated to 11,000 years ago. Whilst casts of the skull exist elsewhere the original was lost (at best severely damaged) in the catastrophic fire that destroyed the National Museum in Rio de Janeiro. 

Luzia Woman belonged to an ancient population formerly known as Lagõa Santa Man or Paleoamerind. The first to excavate such skulls was the Danish Naturalist Peter Lund, who found them as far back as 1840. Based on the classical craniometric criteria used by anthropologists until well into the twentieth century, this population clearly diverged from all others in North and South America.

Lagõa Santa skull excavated 1840 by Peter Wilhelm Lund

There is an interesting correlate in modern genomic data. David Reich and colleagues postulate an ancient Population Y corresponding to a genetic signal borne by the Surui people of the Amazon region (discussed here - see previous post for Reich's book where this is further discussed). The interesting thing about this signal is that it is shared with the faraway Andaman Islanders and natives of New Guinea and Australia.

We already know of two branches to the population that crossed the Bering Strait and peopled North and South America - thanks to work by Eske Willerslev's group (here). Was there a third branch that gave rise to the Paleoamerinds or even a separate and earlier migration?

To piece this together it would have been useful to extract ancient DNA from the Luzia skull. That had not been done prior to the fire. There are other skulls around including those excavated by Peter Lund and now housed in Copenhagen. They may yet yield new pieces to complete the puzzle.

Who We Are and How We Got Here

Oxford University Press 2018
ISBN 978-0-19-882125-0

In little more than a decade, studies of ancient DNA have transformed our knowledge of human history. A recurrent theme is the migration of people over long distances to mingle with and often to replace existing populations. Often the immigrants brought with them new technologies and languages. Although there are also examples of skills dispersing without migration (spread of the Beaker culture from Iberia) and succesive waves of migrants adopting local languages (southwest Pacific islands).

All this and much more is related in David Reich's new book. Although his prose is stilted at times, that is more than compensated by the breadth of material presented and by excellent diagrams. These include maps showing the probable origin, direction and timing of human migrations. 

Skull from Lapa Vermelha, Lagōa Santa, Brazil
Photo by Ryan Somma CC BY-SA 2.0

Although Reich delights in disproving established concepts, it is interesting to find that some long-standing ideas receive support. For example, there is a clear genomic evidence of two waves of migration into Central and Southern America. The first wave of migrants designated "Population Y" left a genetic signature that is strongest in some isolated Brazilian communities (Tupí). This finding lends support to the concept of an ancient people called Palaeoamericans by Neves (here) and named a century ago as Palaeo-Amerind by Haddon (previous post). These ideas were fostered by excavations at Lagõa Santa, Brazil, started 175 years ago by the Danish scientist Peter Lund and continued until this day.

Similarly, present day peoples of India derive much of their genetic makeup from two previous populations. One of these described as "Ancestral South Asians" bears a striking resemblance to the "Pre-Dravidians" postulated by Haddon.

There has been some animus engendered by Reich's book - exacerbated by an opinion piece he wrote for The New York Times. Part II of the book has chapters on the origins of Europeans, South Asians, Native Americans, East Asians and Africans. Inevitably this division reflects the broad racial categories of the past. The flight from racial stereotyping in the last 50 years is laudable, but a mist of political correctness can make recent studies hard to decipher. Reich's book disperses the mist and inevitably invites controversy. 

Przewalski's horse an also-ran

Przewalski's horse Photo by Claudia Feh

CC BY-SA 4.0 

Przewalski's horse has long been seen as the last population of wild horses. No more. A new attempt to find the origins of domestication using ancient DNA is full of surprises (here). 

The Botai Culture of Central Asia has been tied to domestication of horses some 5500 years ago. Ancient DNA was extracted from the bones of Botai horses and the genomes compared with those of other ancient and modern horses.

Cord at term of Przewalski's horse

From Benirschke Comparative Placentation

The first surprise was that Przewalski's horse clustered with the Botai horses. The inescapable conclusion is that Przewalski's is a feral population descended from those domesticated at Botai.

The second finding was that all other horses descend from a separate branch. This was foreshadowed in a previous study (previous post). The most parsimonious explanation is that there was a second centre of domestication yet to be identified.

Benirschke has several images of the placenta of Przewalski's horse (see also previous post).

Insectivores endemic to the Caribbean

Puerto Rican Nesophontes (N. edithae)
Reconstruction by Jennifer Garcia CC BY SA 3.0

The Caribbean is home to two endemic families of insectivores. The Nesophontidae are recently extinct. Their demise is attributed to the introduction of rats by Spanish Explorers though some believe the genus survived into the 20th Century.

To establish their phylogenetic position, scientists recently extracted DNA from a specimen preserved in an ancient owl pellet (here). This was no mean feat as the specimen was 750-years-old and DNA degrades rapidly in the tropics.



Hispaniolan Solenodon (S. paradoxus)
Biodiversity Heritage Library CC BY 2.0

The main finding was that Nesophontes shares a common ancestor with Solenodon. There are two species of this insectivore both listed as threatened by IUCN. A common origin had not been predicted on anatomical grounds not least because Nesophontes and Solenodon have different patterns of tooth occlusion (here). Together these families represent the oldest branch of the insectivores (Order Lipotyphla).

Placenta of Solenodon paradoxus
Wislocki (1940)

Despite its rarity, the placentation of S. paradoxus has been described (here) and we later compared it with that of other insectivores (here). Interesting features are remnants of capsular decidua, elaborately branched yolk sac villi and a sheath that superficially resembles that of crociduran shrews.

Steller's sea cow

Reconstruction of Steller's sea cow (Hydrodamalis gigas)
By Emőke Dénes (Natural History Museum in London) (CC BY-SA 2.5)

When first described by Steller in 1741, the range of this sirenian was already restricted. Intensification of hunting led to extinction of the species within another 27 years.

A recent paper with a "stellar" cast of authors (here) uses molecular data to firmly establish the position of Steller's sea cow within crown Afrotheria; with additional morphological data it also shows shows how the species fits into the fossil record.

Steller's sea cow (Hydrodamalis gigas) belongs with the dugong (Dugong dugon) in Family Dugongidae whereas the three species of manatee belong to Trichechidae. Together they make up the Order Sirenia, which is sister to the elephant Order Proboscidea.

Endotheliochorial placenta of the Amazonian manatee

Fetal (fc) and maternal (mc) capillaries are present

Elephants have an endotheliochorial placenta. Therefore it perplexed us that Wislocki had described the placenta of the West Indian manatee (Trichechus manatus) as haemochorial. Therefore we reopened the matter by studying placentas from the Amazonian manatee (T. inunguis). We were able to demonstrate two sets of capillaries (shown above) and conclude this placenta to be endotheliochorial (here).

The allantoic sac of elephants and manatees has four chambers and we have shown this to be a shared, derived character of the superorder Afrotheria (here).

Clan of the cave bear: researching ancient DNA

Reconstruction of a cave bear (Ursus spelaeus)
Uploaded by Sergiodlarosa to Wikimedia Commons (CC)

The proceedings of a Royal Society discussion meeting on ancient DNA have just been published (here). Three reviews in particular captured my interest.

Ancient DNA: the first three decades by Hagelberg, Hofreiter and Keyser (here) is a lucid account of the history of the field (a major advance was shotgun sequencing as applied to the cave bear). It highlights not only high profile papers from Nature and Science (some of them reviewed in my blog), but also gives credit to important follow up studies from specialist journals. A very useful ressource indeed!

Ancient genomics by Der Sarkissian et al. (here) is from the renowned Centre for GeoGenetics in Copenhagen. This review is especially strong on the technical advances in the field and even includes a user's manual. With the techniques initially available it would have required 180 kg of material and 130 million amplicons to generate a first draft of the cave bear genome. A lot has happened since then. They conclude that even "Looking back 5 years, no one could have predicted the current state of current genomics."

Almost 20 years of Neanderthal palaeogenetics by Sánchez-Quinto and Lalueza-Fox (here) does a remarkably good job of surveying what has been learned from the DNA of Neanderthals from various geographical locations. It covers more than just their relations to and interbreeding with Denisovans and modern humans (previous post). A great deal can be inferred about their demographics, population size and ultimate extinction.

ISBN 0-517-54202-1

 The title of this post is of course an homage to the fiction of Jean M. Auel. The clan of the cave bear are Neanderthals who interact (and interbreed) with modern humans. First published in 1980 it far anticipated the scientific evidence given in the above reviews.

Domestication of horses

Przewalski's horse - no longer seen to be a direct
ancestor of domestic breeds. Photo by Chinneeb (CC)
 

A large consortium has just reported on the genome of horses (Equus caballus) from the Siberian permafrost (here). The two specimens were estimated to be 16 and 42 thousand years old. Thus they were from before the start of domestication as known from the archeological evidence.

Horse phylogenetic relationships from Schubert et al. (here)
(c) The Authors

The phylogenetic analysis showed as expected that the ancient specimens (purple) are basal to all living members of the E. caballus species. However, while most genes present in domesticated breeds were found in the ancient genomes, many were missing from the Przewalski horse genome. It is perhaps a distant cousin rather than a direct ancestor of the domesticated horse (see commentary here).

Section through umbilical cord of Przewalski's horse
From the Benirschke web site (here)

So there have been two paths of selection: one through selective breeding (resulting in both desirable and deleterious traits) and the other through natural selection resulting in Przewalski's horse.

 

Placenta and implantation site of Przewalski's horse.
From the Benirschke web site (here)

These conclusions are in line with those made after sequencing the genome of a really old horse from the Middle Pleistocene (see previous post).

Was Homo erectus the fourth hominin?

Skull of Homo erectus (Wikimedia Commons)

The current issue of Nature has a comprehensive analysis of the genome of Neanderthals and comparisons with modern humans and Denisovans (here). The supplementary material alone fills 16 Mb but there is an excellent summary (here) entitled "Four makes a party." As it says, "it does seem that Eurasia during the Late Pleistocene was an interesting place to be a hominin, with individuals of at least four quite divergent groups living, meeting and occasionally having sex."

The fourth hominin was alluded to in a previous post and is inferred from analysis of the Denisovan genome (previous post). The current study estimates that this putative hominin's ancestor diverged from other hominins 0.9-1.4 million years ago. This date is compatible with the unknown hominin being Homo erectus a hominin well known from the fossil record.