When did modern placental mammals diversify?

February 3, 2014 • 1:36 pm

by Greg Mayer

Almost exactly a year ago, I reported in two posts here at WEIT on a paper in Science by Maureen O’Leary and colleagues on the radiation of placental mammals. Placentals are one of three major groups of living mammals, the others being the marsupials (dominant in Australia, plus a fair number in South and Central America, and a few in North America) and the monotremes (the egg-laying playtpus and spiny anteaters: a handful of Australasian species). Placentals are by far the most species rich and abundant of the mammals, including the cats, dogs, cattle, deer, and us that are the dominant land animals of our world today.

What O’Leary et al. argued for was a view of placental evolution called the “Explosive Model” (see figure below). In fact, they argued for an ‘extra-explosivey’ model, since they thought the common ancestor of the modern placental orders of mammals arose after the extinction of the dinosaurs (i.e. in the Paleogene, not the Cretaceous); in the figure below by Ken Rose, the ‘explosive’ evolution begins at the very end of the Cretaceous).

Models of placental mammal radiation (Rose, 2006).
Models of placental mammal radiation (Rose, 2006); the thicker lines represent extant orders of placental mammals..

The O’Leary et al. study was widely misinterpreted by the press, which said they had discovered the common ancestor of mammals, a beast called Protoungulatum. This interpretation is completely wrong, and not what O’Leary et al. claimed. My earlier posts emphasized correcting this misinterpretation.

I also noted that O’Leary et al. used the fossil record in a quite literal way to infer dates of lineage splitting. But fossils only provide a minimum date of separation of lineages, and there may be a considerable unrecorded history predating the earliest known fossil. A new paper in Biology Letters (open access), a Royal Society publication, takes O’Leary and colleagues to task on precisely this issue.

Mario dos Reis and colleagues use various approaches to calibrate the molecular clock of placental divergence and accounting for the imperfections of the fossil record. Under all three methods they use (a, b, and c in the figure below), the divergence of the modern orders begins in the Cretaceous, their estimates ranging from 72 to 107 mya (the former, though, not very far from O’Leary et al’s 65 mya). O’Leary’s view is shown in panel d of the figure.

dos Reis et al. 2014, Figure 1.
dos Reis et al. 2014, Figure 1. a, b, and c are the estimates they contemplate; d is the view of O’Leary et al.

So, who’s right here? The first thing I would note is that although the Cretaceous-Paleogene boundary has great psychological weight (and is when a lot of things went extinct, including the dinosaurs), Rose’s depiction of the “Explosive” model had divergence beginning in the Late Cretaceous, and 72 to 107 mya is still Late Cretaceous (or very close to it). So while dos Reis et al. strongly object to O’Leary’s methodology, the results of the two papers are not very different: O’Leary has the most recent explosion, dos Reis has a somewhat earlier explosion, and both bracket the time of divergence depicted by Rose. dos Reis’s timing does have biogeographic implications differing from O’Leary’s, since an extra 25 million years allows for greater influence of plate tectonic events on mammalian distribution.

The second thing to note is that a defender of O’Leary’s might make the empirical retort that we have a fair number of Late Cretaceous mammal fossils, and none of them are clearly progenitors of the modern placental orders. Absence of evidence is not evidence of absence, unless, of course, you’ve looked where the evidence should be, and that’s what an O’Leary defender could argue.

And a third issue is that dos Reis et al. rely heavily on Bayesian statistics to make their inferences. It would be a very long and dry argument to explore this here, but suffice it to say that I find Bayesian statistics, in most cases, to be logically unjustified, and thus I’m not entirely sanguine about dos Reis’s inferences. It’s a fairly arcane issue in the logic of scientific inference, so I’ll just point in the references below to two sources (Royall and Sober) that I have found helpful.

In one of my original posts, I asked

[I]sn’t using the literal fossil record a pretty crude way of determining ages of taxon splits, since such ages are always minimum ages? And shouldn’t the richer information available in molecular sequence data that is time-calibrated by securely known fossil dates be used? Well, the critics will answer “yes” to both questions, and will also point out that the fossil record is imperfect, so to say we don’t have any fossils dated to the Cretaceous is different from saying no such animals existed then. O’Leary et al. might reply that all molecular dating requires geological calibration, so that the fossil data is primary, not the molecular extrapolation; and that we have lots of Cretaceous mammal fossils, and none of them are obviously the varied precursors of the Cenozoic placental radiation.

And concluded by asking

Who’s right? I don’t know. But that’s what the upcoming arguments will be about.

Indeed, dos Reis et al. have made a sharp statement in this ongoing argument.


dos Reis, M.,  P.C.J. Donoghue, and Z. Yang. 2014. Neither phylogenomic nor palaeontological data support a Palaeogene origin of placental mammals. Biology Letters 10. pdf

O’Leary, M.A., et al. 2013. The placental mammal ancestor and the post-K-Pg radiation of  placentals. Science 339:662-667. (abstract)

Rose, K.D. 2006. The Beginning of the Age of Mammals. Johns Hopkins University Press, Baltimore. (Google Books)

Royall, R. 1997. Statistical Evidence: A Likelihood Paradigm. Chapman & Hall, London. (Google Books)

Sober, E. 2002. Bayesianism — its scope and limits. in R. Swinburne, ed., Bayes’ Theorem, Proceedings of the British Academy 113:21-38. pdf

More on placental mammals

February 11, 2013 • 3:00 pm

by Greg Mayer

There have been a number of interesting comments by readers on my post on the recent paper on the radiation of placental mammals by Maureen O’Leary and colleagues. I want to respond briefly to a few of them here.

Biogeography. Does this paper imply that the origin and geographic distribution of the  major lineages of placental mammals are not well correlated with the breakup of the Mesozoic super-continents? Yes, it does. The authors explicitly say so, and therefore would invoke more dispersal events to account for mammalian distribution. Now their cladogeny and timing may be wrong, and lack of congruence with plate movement might be a reason for preferring an alternative phylogeny, but the authors do correctly recognize the biogeographic implications of their phylogeny.

G.G. Simpson, one of the founders of the Modern Synthesis, was also one of the most influential mammalogists of the 20th century, who often dealt with large scale issues of mammalian history. He delayed accepting plate tectonics until much later than most other zoogeographers, in part because many major continental movements took place well before the diversification of modern mammals, and thus plate tectonics seemed ‘unnecessary’ as part of an explanatory schema. He might well have been pleased by this aspect of O’Leary and her colleagues’ work.

Publication venue. I criticized the publication as a short paper in Science of a work that clearly deserves and requires monographic treatment. There is an obviously correct place to publish this work: in the Bulletin of the American Museum of Natural History. Many of the authors hold positions at the American Museum, and the Bulletin is explicitly designed for the publication of monographic works. Indeed, Simpson published one of his most important monographs on mammalian classification in the Bulletin. As the preceding link shows, the AMNH, quite admirably, makes all its publications available as free pdf’s, so there would be no question of access. In fact, access would be much greater, since all the material would be in a single freely available work, and not dependent on accessing a variety of websites of unknown permanence and varying cost.

Some readers have noted the tyranny of popularity and attention that journals like Science and Nature exert, and I can certainly sympathize with the authors’ desire to have their work widely read. But ultimately, scientific work must be judged by its data, methods, and conclusions, and publication in Science hampers the paper’s evaluation as a work of science. Science has published summary papers that present the main conclusions of monographic works; Jared Diamond’s 1973 paper in Science summarizing his 1972 monograph on New Guinean birds is an example. As Diamond wrote, “A recent book discusses in detail many of the examples summarized here”, but the monograph to explicate O’Leary’s work may never appear. Perhaps Science no longer does this, but a near simultaneous publication of short summary and Bulletin would have been far preferable.

Are the conclusions correct? This is the $64,000 question. I think the initial critiques come in two parts. First, don’t we already have fossil representatives in the Cretaceous of several of the modern orders of placental mammals? Well, a number of fossils have been so identified, but O’Leary et al. (and others) would dispute these identifications. Their paper does not include a careful analysis of these cases, and their fossil sample is not exhaustive, but does include most of the very well known Cretaceous mammals. Many fossil mammals are preserved only as teeth and thus hard to identify conclusively; O’Leary et al. commendably included only the most completely known forms so as to be able to observe as many as possible of the large number of characters they used. They do agree that there are basal placentals in the Cretaceous. (Or, to use the term they would probably prefer, “non-placental eutherians”. Eutherian and placental are treated as synonyms by some, but they formally distinguish the Placentalia as only members of the least inclusive clade that includes all living placental mammals; these taxon name questions are not important for their main points.) But these Cretaceous forms are, by their estimation, not in general ancestral to the Cenozoic forms– they believe only a single placental lineage survived into the Cenozoic.

Second, critics ask, isn’t using the literal fossil record a pretty crude way of determining ages of taxon splits, since such ages are always minimum ages? And shouldn’t the richer information available in molecular sequence data that is time-calibrated by securely known fossil dates be used? Well, the critics will answer “yes” to both questions, and will also point out that the fossil record is imperfect, so to say we don’t have any fossils dated to the Cretaceous is different from saying no such animals existed then. O’Leary et al. might reply that all molecular dating requires geological calibration, so that the fossil data is primary, not the molecular extrapolation; and that we have lots of Cretaceous mammal fossils, and none of them are obviously the varied precursors of the Cenozoic placental radiation.

(There are also questions about the exact sequence of splits in their phylogeny, and how molecular and morphological data agree or disagree. These discussion will be of most intense interest to specialists in the various groups, although there is considerable general interest in them as well.)

Who’s right? I don’t know. But that’s what the upcoming arguments will be about.

The orders of modern placental mammals originated after the extinction of the dinosaurs

February 9, 2013 • 2:46 pm

by Greg Mayer (Updates below.)

A new study just published in Science by Maureen O’Leary and colleagues examines the phylogeny of 40 fossil and 46 extant mammals based on a very large data set of morphological and molecular characters (the latter only from the living taxa). The study has gotten a fair amount of attention in the press, where it seems to have been misinterpreted; more on that later. First, let’s see what they were trying to do and what they found.

There are three major groups of mammals alive today: the egg-laying monotremes (the platypus and the echidnas), the marsupials (opossums, kangaroos, bandicoots, etc.: a few hundred species) and the placentals (cats, dogs, cattle, deer, and all the rest, including primates: several thousand species in about 18 orders in all). The placentals are the overwhelming majority of extant mammals, and dominate the mammalian fauna of all parts of the world except Australia, which has mostly marsupials. (There are a fair number of marsupials in South and Central America, but they are still outnumbered by placentals.)

In the fossil record, although basal placentals are known from the Cretaceous (some of these fossils are disputed, including by O’Leary et al., but all agree there were some), the great radiation of placental mammals did not occur until the early Cenozoic, after the extinction of the dinosaurs (at least those that had not evolved into birds) at the end of the Cretaceous, about 65 mya. Although the first two-thirds of mammalian history had occurred during the Mesozoic (the “Age of Reptiles”), they really broke out, biodiversity-wise, in the Cenozoic (the “Age of Mammals”).

There’s been considerable debate over whether the placental lineages that radiated in the Cenozoic arose just before the radiation (the “explosive model”), had existed since earlier in the Cretaceous but did not radiate until the Cenozoic (the “long-fuse model“), or had undergone considerable diversification in the Cretaceous (the “short-fuse model“). The latter model would require that the fossil record be seriously incomplete, but has been supported by various molecular phylogenetic studies that estimate various splits among the extant placentals to have occurred well before 65 mya.

Models of placental mammal radiation (Rose, 2006).
Models of placental mammal radiation (Rose, 2006).

The chief question O’Leary and colleagues addressed was which of these models is correct. To do so, they scored over 4000 morphological characters (including soft-tissue characters generally not scorable in fossils) and utilized 27 nuclear gene sequences to estimate the branching sequence. They then added in the known stratigraphic range of the fossils to get a phylogenetic tree (their Fig. 1) that looks very much like the explosive model above, except that the common ancestor of extant placentals (the “P” in the figure) occurred jut over the line, in the earliest Cenozoic rather than the Cretaceous, making it even a little bit more explosive-y. “Explosive it is, sir!”, as Apu on the Simpsons might have put it.

They make two further interesting inferences from their tree. First, they use their morphological data set to estimate what this earliest Cenozoic common ancestor of all placental mammals looked like. It looks like this:

Hypothetical early placental mammal (O'Leary et al., 2013).
Hypothetical early placental mammal (O’Leary et al., 2013).

With such a large data set this is interesting, but it does look pretty much like what people have long thought early placentals would look like. Remember, this is a hypothetical common ancestor, not a newly found fossil.

Second, because much of the breakup of the Mesozoic super-continents had occurred by the early Cenozoic, they infer that a lot of dispersal occurred in the placental radiation, and not just passive floating around on the drifting continental plates. The exact arrangement of lineages in the tree is also of interest, and will be discussed and debated by mammalogists. It’s not clear to me that a huge data set is necessarily an advantage in inferring this large scale phylogeny, because we don’t understand the dynamics of conservatism and lability of morphological characters in the way we do for genetic sequence data. Our understanding of the latter allows us to select genes and use methods of analysis appropriate for a particular question. Using thousands of morphological characters seems a bit too reminiscent of the old pheneticists’ hope that if they could score enough characters, “parametric overall similarity” could be known (phenetics didn’t pan out as hoped). I hasten to add that morphological characters are more difficult because they are more complex and more crucial to the organism, and consequently more interesting– indeed, what most biologists are really interested in– not because there is something wrong with studying morphology.

In the media, there has been considerable confusion about this study, in part because the distinction between mammals and placental mammals has not always been kept clear. The  New York Times initially led with the headline:

“Common Ancestor of Mammals Plucked from Obscurity”;

but, of course, the study is not about the common ancestor of mammals, but only placentals. And furthermore, there is no particular known fossil which is being identified as or compared to this placental common ancestor; the ancestor in the picture, as stressed here, is hypothetical. Yet, the Times article identifies Protungulatum as the ancestral placental, O’Leary et al. most definitely do not do do: they identify Protungulatum as a member of the lineage that gave rise to (most) hoofed mammals (i.e. quite far from the common ancestor of all placentals). Protungulatum is the oldest known member of the clade that includes all extant placentals, but that does not make it the common ancestor.

This misunderstanding has infected the news media, and spread widely. Gizmodo labels a picture of the hypothetical form (a version of the figure above) as Protungulatum, and states

This rat with way too many sharp teeth is your great x 4 x 10^6-grandmother. That’s what scientists have discovered after six years of research—the Protungulatum donnae is the common ancestor to all mammals, from humans to horses to lions.

This is pretty much completely wrong. And UPI labels the same figure as

An artist’s rendering of Protungulatum donnae,

which it isn’t at all. The Times, at least, subsequently changed its headline to

“Rat-Size Ancestor Said to Link Man and Beast”,

which is still pretty obscure, but not actually wrong. But the article retains its misstatements about Protungulatum (at least last I checked). The Times did correct another error. They had initially stated that only a single mammalian lineage had survived the end-Cretaceous extinction, but it is known that there were at least four surviving lineages (one monotreme, one marsupial, one placental, plus one multituberculate– a now extinct mammal group which survived the end-Cretaceous extinction, but died out in the Oligocene). The article has now been corrected to say that the study concludes only one placental mammal survived (which is indeed what its major conclusion is).

The article in the BBC was better, getting the headline right:

“Earliest placental mammal ancestor pinpointed”

and not mentioning Protungulatum at all. The BBC front page headline, however, was off:

“Earliest mammal ancestor pinpointed”.

For a mildly critical take on the study (not the news coverage) by a more molecularly oriented mammalogist, see Anne Yoder‘s Perspective in Science.

UPDATE. I had left the following comment out, because I thought I was saying it too often, but this paper really shouldn’t have been published in Science. There is much too much data, methods, analysis, and discussion left out of the paper because of Science‘s severe length limits. There are two online “supplements”, one at Science and another at morphobank.org. The one at Science is 132 pages long. The morphobank supplements are not organized as a file, so it’s hard to tell how much is there, but it’s a lot. Now some of this material (e.g. lists of which authors examined which specimens) need not be published, but it’s simply impossible to fully understand or critique the paper with out referring to a great deal of this material, which is not readily available to someone in possession of a copy of the paper. The authors have shortchanged themselves and their readers by publishing in such a venue. I was moved to add this update after an alert reader noted an error in my statement of the number of species included, and I had to pore though the supplements to verify the correct numbers because of ambiguous wording in the paper. I was able, while doing so, to confirm that the same extant 46 species were used for the genetic and morphological analyses. (And since I’m kvetching, I’ll note that the authors substitute the grotesque, poorly defined, and unnecessary word “phenomic” for “morphological” (or a similar word) throughout their paper.)

UPDATE 2. The errors in the media coverage do not stem from SUNY Stony Brook’s press release, which correctly summarizes the claims of the paper.


O’Leary, M.A., et al. 2013. The placental mammal ancestor and the post-K-Pg radiation of  placentals. Science 339:662-667. (abstract)

Rose, K.D. 2006. The Beginning of the Age of Mammals. Johns Hopkins University Press, Baltimore. (Google Books)

Yoder, A.D. 2013. Fossils versus clocks. Science 339:656-658. (abstract)

Your ear bones came from your jaws

October 15, 2009 • 6:22 am

by Greg Mayer

Although the mammals and reptiles most people know are quite distinct– mammals are hairy, warm-blooded, live-bearers, that suckle their young, while reptiles are scaly, cold-blooded, egg-layers– a wider knowledge of the modern forms reveals that the differences are less absolute. There are many live-bearing reptiles, for example, and platypuses and echidnas lay eggs and are nipple-less. And it has long been known that mammals are descended from a particular group of fossil reptiles:  both the great British anatomist Richard Owen and the American paleontologist and zoologist Edward Drinker Cope noted this in the 1800s (Cope doing so in a paper with the wonderful title “The theromorphous Reptilia”, “theromorphous” meaning, roughly, “beast-shaped”).

Because the vertebrate fossil record consists mainly of bones, paleontologists need an osteological distinction between mammals and reptiles, and the definition of mammals is that our jaw joint is between the squamosal bone of the skull and the dentary bone of the lower jaw, while in reptiles the joint is between the quadrate and the articular.

Mammal and reptile jaw joints
Mammal and reptile jaw joints, from Wikipedia by Philcha

The stages in the picture above were about all that were known to Cope and Owen, but they could still see the connection between the groups. (The lower picture is of a pelycosaur, an early type of synapsid reptile, the synapsids being the group of reptiles from which mammals eventually evolved; Dimetrodon was a pelycosaur). Cope’s identification of early synapsids as the ancestors of mammals could be considered a prediction that intermediate forms would be found (I leave out Owen, because his views on evolution were equivocal). Later work has abundantly confirmed this, and the reptile-mammal transition is now probably the best documented of all higher level transitions in the vertebrates. A classic paper by A.W. ‘Fuzz’ Crompton and Farish Jenkins, teachers of mine from grad school, summarized the first 100 years of work on the subject.

Here’s a diagram of one of the intermediate forms. Note that it has a double jaw joint, and the bones in the lower jaw have become much smaller. If you look above to the mammal, you will see that these bones have become even smaller still, and detached from the lower jaw.

Double jaw joint
Double jaw joint from Wikipedia by Philcha. This figure is not quite right. The dentary/squamosal contact is actually much nearer to the quadrate/articular contact. The two joints are lateral and medial to one another, not anterior-posterior.

What has happened is that two bones of the lower jaw (the angular and the articular), and the quadrate of the upper jaw, of reptiles have become (some of) the ear bones of mammals– the tympanic, malleus, and incus, respectively (mammals have another ear bone, the stapes, which is the only ear bone in reptiles). This reduction in size and detachment from the jaw occurred in many gradual steps over many millions of years, all documented in the fossil record. Clifford Cuffey has a nice set of figures of some of these, and Karen Peterson of the University of Washington has posted class notes with some very nice figures. What makes this even neater is that the jaws themselves are derivatives of the anteriormost parts of the branchial (gill) arch skeleton, a subject I’ve mentioned before, and thus we can trace the history of these bones from the branchial apparatus to the ear by way of the mouth.

Just as Matthew was inspired to post about sponges after lecturing about them to one of his classes, I bring up the ear bones because I was lecturing to my vertebrate zoology class about the branchial skeleton and its derivatives this past Tuesday. It was also the very day that the New York Times had an article by Natalie Angier on the evolution of the mammalian ear bones inspired by a recent paper in Science (subscription required for full article) by Qiang Ji and collaborators. They describe the jaw of an early Cretaceous mammal that had a persistent reptile-like connection of the ear bones to the jaw.  The authors propose, quite reasonably, that this is a paedomorphic condition, that is, that it is the retention into the adult of an embryonic condition: mammalian embryos pass through a stage in which their jaw/ear bones resemble those of reptiles.

The working out of the history of these bones is one of the great triumphs of vertebrate comparative anatomy. Neil Shubin (sorry Jerry!) summarizes the highlights nicely in chap. 10 of Your Inner Fish.