The Placental mammal saga; special summer double episode

Flickr_-_ggallice_-_Rodent

As I wrote in a previous post last winter, O’Leary et al. added their oar into the Placental Mammal origins debate. For anyone who missed that episode, they argued, with the backing of masses of morphological data, that placental mammal orders appeared right after the extinction of non-avian dinosaurs (also known as the explosive model). This was in opposition to two other views based on DNA data which argue that placentals appeared way before (long-fuse model) or slightly before (short-fuse model) the Mexican dinosaurs had to deal with some meteorite… Again, have a look at this previous post criticizing O’Leary et al.’s paper and how they “forgot” to use (ignored?) state-of-the-art phylogenetic inference methods.

While I was away feeding mosquitoes in Finland – and wondering whether the lack of fishes for dinner was due to my poor fishing skills or the absence of fishes in the river – Science published two new episodes of the placental saga. Of the two, Springer et al. took the decision to properly criticize the methods of O’Leary et al.’s work. Amongst their detailed methods review, they particularly underlined the inaccuracy of O’Leary et al.’s explosive model; such a hypothesis would imply that the early placental mammals had a rate of molecular change similar to that of retroviruses. For over ten years it has been widely accepted that molecular rates (i.e. the number of DNA changes that are transmitted to descendants) vary among lineages through time. Knowing that, one can estimate these rates (or call it speed if you’re more comfortable with that) of evolution by calibrating phylogenetic trees with fossils. So, in this case, the amount of evolution needed to evolve from the late Cretaceous (~65 myr) non-placental mammals to the first placental mammals (~58 myr) has to be as high as evolutionary rates more characteristic of retroviruses to realistically explain this evolution.

Herein lies the eternal debate between palaeontologists and molecular biologists. The former base their estimations on the morphological changes they can see in the fossil record (even though some, as O’Leary et al. also include molecular data) while the latter calculate their evolutionary rate estimations on the molecular changes that they infer from living species’ DNA. Fundamentally, each method is valid but they are describing slightly different things ; palaeontologists infer the rates of changes between morphospecies (i.e. species that are separated based on their morphology) while molecular biologists study the rates of changes between surviving genetic pools (i.e. the populations leading to living species). My guess is that the true evolutionary history (i.e. the morphological and molecular changes of all the populations –fossils and living– through time) is to be found somewhere between these two approaches.

And that’s what I think O’Leary et al. demonstrated in their response to Springer et al.’s comments. Through a kind of a dodgy answer in reply to the technical points that Springer et al. underlined as the “retrovirusesomorph” rates, O’Leary’s team reran the analysis and found that yes, maybe the explosive model is not very realistic regarding the molecular data but neither is the long-fuse model regarding the palaeontological data. So which one should we choose? Hmmm, why not just go for the middle way with the short-fuse model? OK let’s do that – without calling it a short-fuse model though (they called it an “explosive model” in figure 2-B but to my mind at least, it’s getting closer to the short-fuse one).

So all that for what? Nobody can either deny O’Leary et al.’s amazing work nor claim that the long-fuse model is realistic; the consensual short-fuse model remains pretty well supported among both moderate palaeontologists and molecular biologists. However, I still cherish this paper because it shows how I think good science should always work; find the two extreme scenarios and then study the median one…

Author

Thomas Guillerme: guillert[at]tcd.ie

@TGuillerme

Photo credit

Wikimedia commons

Palaeo-poetry and placental mammals

Furry_ball_by_aerox21

 

Recently Science published O’Leary et al.’s – new load of oil to fuel the burning debate on the origins of placental mammals.

Just to be clear: there is an important distinction between mammals in general that includes many fossils from the Jurassic as well as the extant platypus, kangaroo and your grandma; and placental mammals that includes your grandma and the armadillo (but not kangaroos or the platypus) and no fossil before 65Myr. For readers that are not used to the debate concerning the first placental mammal here’s the main question: did the first placental mammals diversify before or after 65Myr (the important KT boundary)?

(1) After Katie

One view suggests that early mammals lived in the shadow of dinosaurs and the demise of these mighty creatures allowed our rat-like ancestors to take over the earth, the seas and the skies “Save yourself mammals”. This idea was proposed by Simpson in the 1950’s and is supported by the fossil record; many dinosaurs (both big and small) were present before the 65 Myr KT boundary, then a catastrophic meteorite impact marked the KT limit and placental mammals radiated after that. This sequence of events seems to be very straightforward but reality appears not to be so simple. Increasing numbers of mammal species from the late Cretaceous are being discovered, (including rather big ones feeding on dinosaurs) and not many species in general are found in the fossil record before 55Myr when all groups of placental mammals seem to suddenly appear (for a full story see Luo’s 2007 Nature review).

(2) Before Katie

In contrast, another group of people, mainly assisted by molecular dating methods, found out that post-KT placental mammalian diversification may just be an artefact of the fossil record (like Meredith et al 2011 in Science again). Their DNA evidence seems to say that placental mammals evolved before the KT limit and that either palaeontologists failed to find them or else the fossil record failed to preserve them. One major criticism that moderate people argue is that there are still problems associated with molecular dating methods. I won’t go into the details (yes I’m trying hard not to) but molecular dating relies on DNA on the one hand (sampling quality and modelling) and on the fossil record on the other hand. So if the people using DNA criticise the fossil record and want to improve the DNA dating estimates, they have to rely on the same fossil record that they are criticising. The snake bites his own tail.

So what about O’Leary and colleague’s paper? They basically support the first theory (placental mammals evolved after KT). Fair enough, it was led by a number of great palaeontologists and based on a massive morphological data set (~4500 characters introduced as phenomics (from the phenotype) as opposed to genomics (from the genome) data) collected on 40 unambiguous fossils and 46 extant placental mammals. Genomic data based on 26 genes of these extant placental mammals was also included. This paper is the result of an impressive and unique collaborative work, but – Ned Stark from Games of Thrones said “nothing someone says before the word “but” really counts” –  but this paper is criticisable…

First of all, the data set: although the morphological data is impressive, the taxa sampling effort seems a bit weak, especially for extant placental mammals. Meredith et al used the same genomic data (26 genes) but based on ~164 mammals to answer the same question. Why couldn’t O’Leary use all of this already published mammal DNA? For the second criticism, I’m just going to quote Yoder’s review published in the same issue “Today, sophisticated theoretical and computational methods are used to estimate and calibrate molecular phylogenetic branch lengths (which represent time). Together with improved methods for integrating fossil and molecular data, dates derived from molecular phylogenies have inched closer to those implied by the fossil record. Is the approach used in the O’Leary et al. study directly comparable to these recent molecular phylogenetic studies? Not really, as it turns out.”

No wonder this paper supports the first theory, it is just a precise and massive analysis of the 40 species of the placental mammals fossil record. Personally, I’m really frustrated by how they managed to publish this paper. Since it’s part of my PhD research, I automatically get excited when I see fossils mixing with extant species so I really hoped this paper would link the two approaches instead of supporting the old fashioned view of evolution (the dinosaurs dying and the mammals taking over). I’d like to think that the history of life is a bit more complex and exciting…

A last comment to justify my title and which will be my main critique to this paper is that O’Leary et al. tried to recreate the “hypothetical placental mammal ancestor”.

ancestral_placental

As I said, this paper could be seen as a summary of the placental mammal fossil record. So why did they break the first rule that keeps palaeontology away from palaeo-poetry (i.e. going too far with palaeontological hypotheses)? Here they reconstructed a whole creature using their morphological data. What they made was essentially a mean (average) placental mammal (a primitive rat-like creature) – a throw-back to the early stages of palaeontological views of mammalian evolution. What did the ancestor of a duck and a beaver look like? Something in between – a platypus for example? As Olaf Bininda-Edmonds said on Ed-Yong’s Nature post “comparing the two estimates is like comparing “apples and oranges”, they haven’t really done anything to resolve this on-going dispute”.

This paper has also caused controversy on twitter. I’ll just cite two opinions.

Gavin Thomas (@Phalaropus)

“The reconstruction is fun – I’d love to see a picture based on 95% CIs for the ancestral states.”

and Rich Grenyer’s answer (@rich_)

“yes indeed. Something like this” (see our title image).

Many parts of the online science community got excited about this paper, you can see further discussions on Jerry A Coyne’s blog (here and here), on Ed Yong’s one (here and here or there) or else on the twitter feed #placental.

Author

Thomas Guillerme: guillert@tcd.ie

Photo credit

http://aerox21.deviantart.com/