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).

A colugo genome at last

Phylogenetic placement of colugos  (Scandentia) in the lineage of primates
From Mason et al. Sci Adv 2016 (here) CC BY-NC

Used to be that tree shrews (Scandentia) were regarded as the closest relatives to primates as cogently argued by Wilfrid Le Gros Clark. Molecular phylogenetics have brought that into question with some proposing colugos  or "flying lemurs" (Dermoptera) as a better alternative. But there have several competing hypotheses (see Martin). Choosing the right one has been difficult in the absence of a colugo genome.

Now that has been rectified in a comprehensive study by Mason and colleagues (here) who sequenced the genome of a Sunda colugo and compared it with genomes from 21 mammals. The result clearly came out in favour of colugos as the closest relatives to primates, supported by  20 shared indels and 16 shared retrotransposons.

There are many morphological similarities between tree shrews and colugos but the tree constructed by Mason et al. implies these are due to convergent evolution. Within Euarchontoglires they find tree shrews as the sister to Glires (rodents and lagomorphs).

Museomics and hidden biodiversity within colugos

Colugo fetus and placenta at term; ys = yolk sac;
pat = patagonium From Hubrecht 1894 (here)

Current reference works recognize no more than two species of colugo: Sunda Colugo (Galeopterus variegates) and the Phillipine Colugo (Cynocephalus volans). Mason et al. conclude that there may be as many as 6 Sundaic species and 2 Phillipine ones. They reached this conclusion by extracting DNA from museum specimens of known provenance. As an example, the Eastern and western populations on Borneo are highly divergent consistent with topographical features creating barriers to dispersal.

Currently we are re-examining the placenta and fetal membranes of colugos. We too have had to rely on museum specimens such as those collected by A.A.W. Hubrecht.

The importance of museum collections has been highlighted before in this blog. It is nice that scientists other than morphologists have discovered their value and coined the term museomics for studies of DNA from ancient specimens. Those in the current study ranged from 28 to 121 years old. The oldest specimen from the Raffles Museum of Biodiversity Research is contemporaneous with those collected by Hubrecht for his study of the fetal membranes and now housed at Museum für Naturkunde in Berlin. 

Placentation in colugos

Colugo fetus near term from Hubrecht (1919)

Colugos (once known as flying lemurs) are of interest because of their close relationship to primates. Dermoptera (colugos), Scandentia (tree shrews) and Primates group together as Euarchonta.

Dilated maternal blood spaces in a colugo placenta

Hill Collection micrograph courtesy of Allen C. Enders

Their placentation is of interest because it seems to be intermediate between a labyrinthine and villous form. Starck referred to it as a Zwischenform and Wislocki compared it to the trabecular placenta of Neotropical primates. This not withstanding, we still lack a complete description of the term placenta. Mossman (previous post) could not reconcile his own observations with unpublished drawings by Luckett and urged further study. 

Hubrecht (previous post) accumulated 182 uteri of the Sunda colugo (Galeopterus variegatus). His thorough description of early fetal development, published posthumously (Verhandelingen der Koninklijke Akademie van Wetenschappen 1919), stopped at the establishment of the definitive placenta. J. P. Hill collected specimens of the Sunda colugo and the Philippine colugo (Cynocephalus volans) but did not describe them. Nor did Amoroso (previous post) who apparently borrowed most of Hill's slides. The time is ripe for a thorough study of colugo placentation.