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).

Tree shrews move from branch to branch

Species tree by three coalescent-based approaches
from Esselstyn et al 2017 © The Author 2017

In an heroic effort to resolve some of the difficult nodes in the mammalian tree, Esselstyn et al. used data from published genomes and added new data for a total of 100 mammals. Focussing on ultraconserved elements, they analysed all this by a battery of techniques, These included the classical maximum likelihood (ML) on concatenated data and three coalescent-based approaches. How did they do?

The first problem was to resolve the root of the eutherian tree. Here they did rather well. Both the ML tree and two of the coalescent-based methods gave strong support to the Atlantogenata hypothesis, i.e. a sister relationship between Afrotheria (elephants, dugongs, tenrecs and hyraxes) and Xenarthra (sloths and armadillos) with a common ancestor basal to Boreoeutheria (all other eutherian mammals).

South American Tapir (Tapirus terrestris)

Photo by Bernard Dupont CC BY-SA 2.0

They did almost as well with the second problem: the sister group to horses, rhinos and tapirs (Perissodactyla). In most analyses the found Cetartiodactyla (cetaceans and even-toed ungulates) as sister to Perissodactyla. However, they could not rule out one of the alternative hypotheses, which had bats (Chiroptera) as the sister group.

Whereas horses and cetartiodactyls (including ruminants, pigs, dolphins) all have epitheliochorial placentation, no bat does, so I am happy with their majority finding!

Pen-tailed tree shrew (Ptilocercus lowii)

From Wolf 1848 via Wikipedia Commons

On the third thorny problem the exercise failed. Tree shrews used to be thought the closest relatives to primates but have been toppled from this position in favour of colugos (previous post). Because some previous studies did not even include colugos, the present authors sought a remedy in including two colugos and three tree shrews, including the pen-tailed tree shrew above. The hope was that high taxon coverage would give a sounder result. But they were forced to conclude that placement remains uncertain. Tree shrews may be sister to rodents and lagomorphs (Glires) or to colugos plus primates (Primatomorpha).

Fortunately they could confirm colugos as sister to primates, which was the basis for my recent paper with Andrea Mess on the evolution from labyrinthine to villous placentation (here).

South American fossil ungulates are related to modern horses

Macrauchenia - an extinct South American native ungulate
Drawn by Kobrina Olga (Wikimedia Commons CC BY 3.0)

South American mammals either arrived recently during the Great American Interchange, came to South America by rafting (previous post), or have a shallow fossil record (xenarthrans). In contrast, South American native ungulates (SANU) have a deep fossil record. Though the lineage is now extinct, genera such as Macrauchenia (above) and Toxodon survived into the Late Quaternary. The conditions under which these fossils were conserved did not favour survival of their DNA. However, a paper just out in Nature (here) shows how proteomics can be used to probe their phylogenetic affinities.

The authors used MALDI-TOF mass spectrometry to determine the amino acid sequences of the alpha chains of type I collagen extracted from fossil bones. They then performed a phylogenetic analysis. This showed that Macrauchenia and Toxodon form a monophyletic group. Interestingly, this resolved as the sister group to modern Perissodactyla, i.e. horses, tapirs and rhinoceroses. Together they form a taxon named Panperissodactyla.

The modern species have an epitheliochorial placenta so perhaps this type was present in the sister species Macrauchenia  and Toxodon.

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).

Horses from the permafrost and beyond

Remarkably it has proven possible to sequence the genome of a Middle Pleistocene horse from a bone preserved for 700,000 years in the Canadian permafrost (summary and links here). Comparison with the genomes of modern horses and a more recent fossil yielded several interesting results. Among them, Przewalski's horse was shown to be a wild subspecies uncontaminated by domestic breeds.

Placenta and implantation site of Przewalski's horse

From the Benirschke web site (here)

Przewalski's horse was once listed as extinct in the wild but a successful captive breeding and release program has changed its status to endangered. There are several images of the placenta of Przewalski's horse on Benirschke's web site (see previous post). The equine placenta is epitheliochorial and has microcotyledons as pictured above.

Soft tissues usually are not preserved for posterity but a putative placenta accompanies a Middle Eocene fossil of the equid genus Propalaeotherium (cited here).