Mammal tree of life still not resolved

Lesser hedgehog tenrec (Echinops telfairi)
A member of the superordinal clade Afrotheria
Photo by Wilfried Berns CC BY-SA

My studies of placental evolution were stimulated by the large-scale molecular phylogenetic analyses of mammals that appeared 15 years ago (e.g. here). Especially riveting was the revelation of four superordinal clades, among them Afrotheria. 

An excellent review of the progress made in molecular phylogenetics and phylogenomics in the last 15 years recently appeared under the heading "Mammal madness" (by Foley, Springer and Teeling here). 

Competing hypotheses on the root of the mammalian tree
From Mess and Carter (here) based on Springer (Chapter here)



Some of the uncertainties arising from the earlier work remain. Most striking is the failure unequivocally to root the tree. The three competing hypotheses shown above are still in play. While consensus is tipping in favour of Model A above, retroposon analysis provides similar support for all three.

This is not all. There remains uncertainty about the branch order within Laurasiatheria, which includes bats, carnivores, pangolins and even- and odd-toed ungulates.

Such uncertainties make it difficult to plot the evolution of fetal membranes and placentation. Thus the likelihood that the common ancestor of extant eutherians had an endotheliochorial placenta is greater under Model A than the other two hypotheses (shown here).

Concatenation and coalescence

Analysis of large data sets involves some fancy statistics. Foley et al. give a fair account of the pitfalls in concatenation, used in all the early papers, and coalescence. Coalescent methods require much more computer time and are not applicable to large data sets unless short cuts are taken. So far this has not worked out too well.

An article just appeared in Cladistics (here), which seems to demand a "correction," in reality a retraction, of a paper in PNAS based on a coalescent approach. The authors doth protest too much, methinks. As Foley et al. point out, some pretty weird results appeared in the early days of DNA studies, too.

Morphology and molecules

The attitude of some researchers to morphological data could also be more generous. Attempts to integrate morphology and molecules, such as O'Leary et al. (previous post) do throw up some counterintuitive results. But there are examples where fossils have been useful in bolstering hypotheses based on molecular data - the position of whales is a case in point (previous post). Similarly, Afrotheria is not well supported by morphology, but we have published an apparent synapomorphy in the form of the allantoic sac (here).

Moreover fossil calibrations are the key to solving another conflict, which concerns the timing of ordinal diversification of mammals. Deservedly this is given close attention in Foley et al.'s excellent review. The sort of fossils we are talking about are too old to yield ancient DNA so we have only morphology to go on.

Foley et al. finish on an optimistic note and predict the next 20 years of phylogenetic research "should result in the resolution and dating of the mammal tree of life."

 



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. 

Evolution of altriciality

Kangaroo Joey inside the pouch
Photo by Geoff Shaw, Zoology, Melbourne, Australia CC BY-SA 3.0)

Marsupials and so-called placental mammals share a common ancestor yet pursue very different reproductive strategies. This led Ingmar Werneberg and colleagues to ask what reproduction was like in the common ancestor of marsupials and placentals (here).
They sampled data from the literature and examined specimens in the Hill and Hubrecht Collections at Museum für Naturkunde in Berlin. (In published sources they found examination of photographs and drawings more reliable than verbal descriptions.) There is a huge data set in the Supporting Information.


Altricial and precocial neonates exemplified by the
mouse (above) and guinea pig

It was estimated that the last common ancestor of placental mammals had a gestation of around 4 months and a litter of 3-5 young. The newborn were altricial and had closed eyes and almost naked skin at birth. The precocial lifestyle of hoofed mammals and the guinea pig is a derived feature (previous post). The newborn of marsupials are, of course, highly altricial.

A reconstruction was attempted of the neonate of the therian ancestor. This suggested it was anatomically more like extant placentals than extant marsupials. In contrast, the preweaning period was very long compared to intrauterine gestation and thus infancy in this ancestor was more marsupial-like. The relative timing of eye opening was between that of placental and marsupial mammals. Gestation lasted 31 days in this hypothetical ancestor. It was reduced to 21 days in the marsupial lineage while increasing fourfold in the placental lineage.