Don't blame the dinosaurs

I love this sort of thing! It is the reason it was inevitable that I would become a skeptic. I Have always enjoyed clever explanations that challenge popular knowledge.

I bet your cannot find similar graphs and charts by creationists who say that the world is less than 10,000 years old.

I'm curious. Is this a knock against the "punctuated equilibrium" hypothesis?

I see what you did there. Well played.

No, this doesn't detract from punctuated equilibrium at all.

I think this got a blurb on cnn.com. I'm going to lobby to talk about it in our Evolution Discussion Group next week (today we're talking about yeast interactomes, which is a bit yeast-y and protein-y for my taste)...

I don't suppose there's a nice big vector-based PDF available for us to post our (very) extended family trees on our walls, is there? I think phylogenetic trees are some of the most beautiful and compelling images we get from science; it would be nice if I could print up a huge copy of that. It's legible in its current form, but it's not, you know, boss.

CLEARLY, 'evolutionistas' are in big trouble. Or at least have a fever, according to this opinion.
http://www.americanthinker.com/blog/2007/03/evolutionary_rumblings_the_…

The "American Thinker" blog. Boy, PZ should start a post on just that concept.

Awesome, so who's responcible for hosting the Family Reunion this time?

The Carnivori? Lagomophi? Whoever it is, they'd better get on sending the invites soon, or some of us will be extinct before we can RSVP.

Grendelkahn -

I think there's something that should do the trick on the bbc's website. Look at

http://news.bbc.co.uk/1/shared/bsp/hi/pdfs/28_03_07_mammalstimeline_pdf…

That's the message of a new paper in Nature that compiled sequence data from 4,510 mammalian species

No, they did not.

They took the literature, compiled a supertree from the (hopefully) phylogenetic analyses they found there, got sequences of 66 genes for as many mammals as possible, and then used those sequence data plus 30 calibration points to estimate some divergence dates on that supertree.

That's right: apart from its size, it's just yet another attempt at molecular dating.

And not a very good one. The age of the basal divergence (between the monotremes and the rest) was fixed at a rather arbitrary date out of the range of ages the oldest known fossil on the monotreme side of the split could have. The other ages were only used as minimal ages; maximal ages were not used, thus providing no protection against too old divergence date estimates. Of course maximal ages cannot be derived from the fossil record as easily as minimal ages, but the fossil record from some epochs is good enough to let us interpret absence of evidence as evidence of absence with more than 50 % confidence.

There are only three outgroups, increasing the risk that the lengths of these branches could have detrimental effects on the branch lengths in the ingroup...

No, it is not an earth-shattering paper, despite having been published as an "Article" (rather than "Letter") in Nature.

The KT extinction was devastating for just those animals we are attuned to recognize most readily, but may not have been quite so troubling to others; the bacteria didn't even notice, insects would have gone on buzzing (except those with dependent parasitic relationships), plants may have seen one minor class of leaf-nibblers disappear, the rat-like and lizard-like creatures of the undergrowth might well have found their environments relatively unchanged. That transient period of intense trauma might not have been as disturbing to the overall life of the planet as we big apes might like to imagine.

Not so. Studies of bite, mining, etc. marks on leaves around the Cretaceous-Paleogene boundary have shown that herbivorous insects suffered massively. Among mammals, one of the three groups of multituberculates disappeared, as did several clades of relatives of marsupials and placentals, and all but apparently one of the dryolestoid fauna of South America (Dryolestoidea being Yet Another Mammal Clade). The lizards were (as expected) hit less severely, but still suffered (for example a herbivorous clade died out). The turtles were decimated enough that a close relative of the alligators that was apparently a specialized turtle-eater died out. And so on.

And don't get me started on the Strangelove Ocean...

I should also have mentioned that, among the plants, the low-latitude conifers (Cheirolepidiaceae) vanished completely. There's also a mass extinction in angiosperm pollen types.

Darn, David Marjanovic beat me to it. Yup, it was a supertree analysis rather than an exhaustive new analysis.

Also as David pointed out the study focused on dating divergence times. What he didn't add was that there has been a lot of controversy over molecular clock calibration in both mammalian and avian phylogenies in a great many studies. At first the molecular estimates seemed completely incongruous based on the fossil evidence. But it seems like these days we keep finding Cretaceous ancestors of many extant orders. So I think that although there are still questions about divergence timing we will see that as we fill in the fossil record that ghost lineages will be less and less of a problem.

I agree completely that this is not an earth-shattering paper, and my point is that seeing a mammalian radiation prior to the K/T boundary should not be a surprising result -- that extinction had a greater effect on larger organisms than small ones, and that we ought to expect a great deal of interesting evolutionary phenomena to have gone on in the less mega, more creepy-crittery fauna.

As for the technical details, I didn't want to get into all the gory minutia, which was why I said they "compiled" the data -- I hope no one had the impression that this one group sequenced many genes from over 4,000 species, all for this one paper!

But it seems like these days we keep finding Cretaceous ancestors of many extant orders.

Such as?

In the meantime, I downloaded the first part of the supplementary information. Table 3 of http://www.nature.com/nature/journal/v446/n7135/extref/nature05634-s1.p… lists the calibration points. It contains (at least) the following mistakes:

- Monotrematum is probably not a crown-group monotreme. Thus, Monotremata may be younger than 63.6 Ma.
- Tribosphenomys is far from being a crown-group rodent! Rodentia (unlike Rodentiamorpha) is younger than 57.25 Ma (...and I wonder where they got such a precise date...). Note that the reference Bininda-Emonds et al. cite makes this quite clear (it coins the name Rodentiamorpha).
- Not that I knew anything, but I'd be quite surprised if Eodendrogale were a crown-group scandentian. Thus, the crown-group of Scandentia may well be younger than 44.5 Ma.
- Same for Dendrotherium being a crown-group dermopteran.
- The genus Tarsius is 44.5 Ma old? Difficult to believe. I'd say a name change is in order.
- Diacodexis is a paraphyletic series of species around the base of Cetartiodactyla (which means that at least some of those species should get new genus names). Putting "Diacodexis sp." into Suiformes does therefore not look defensible to me, but I'll try to find the reference.
- Obviously, Pakicetus is not a crown-group whale. The crown-group of Cetacea (Autoceta) is much younger.
- Eomanis is far from a crown-group pangolin...
- I'd be very surprised if Ageinia turned out to be a crown-group bat. Thus, chances are high that the crown-group of Chiroptera is younger than 52.2 Ma.
- I'd be surprised if Riostegotherium turned out to be a crown-group dasypodid. But that's outside my area of knowledge.
- The crown-group of Tubulidentata consists only of Orycteropus. Obviously Myorycteropus can't be part of that...
- Nortedelphys was indeed described as a didelphimorphian, but I don't buy it. It's "the tooth, the whole tooth, and nothing but the tooth" (as usual in the Mesozoic). In any case, considering it a crown didelphimorphian really stretches it.
- Paucituberculata... all extant paucituberculates are caenolestids, and the fossil is most likely not one of those...
- I bet the fossil notoryctid is outside the crown-group.

Much sloppier work than I imagined.

Sorry for a dumb newbie question - but why did the dinosaurs die out completely (including marine and flying dinosaurs), and not reptiles, birds, mammals, etc?

I wouldn't say that small creatures as such had no problems at the end of the Cretaceous. As I recall (wow! a sixty five million year memory!) there was a 'fern spike' or in other words lots of ferns grew where they hadn't before, because competing plants died, due in large part to extreme acidification of soils as far from Yucatan as Australia.

and my point is that seeing a mammalian radiation prior to the K/T boundary should not be a surprising result --

But a placental and a marsupial radiation in the Cretaceous are surprising results, and therefore I'm not surprised to find so much miscalibration in the paper. Both groups are currently completely absent from the Cretaceous (except for Nortedelphys and a few more problematic crumbs), no matter how common the remains of other mammals are, and no matter how small those are.

Dave,

Dinosauria (= all descendants of the common ancestor of Iguanodon and Megalosaurus did NOT die out completely! Birds (the group Aves) are just as much a part of Dinosauria as are tyrannosaurs or brachiosaurids or ceratopsians.

So the question is: why did only one small part of Dinosauria survive? And that does remain an interesting problem. It may have to do with overall smaller body size, but there were groups of other birds (broadly defined), such as hesperornithines and enantiornithines, that utterly perished at the same time as their giant cousins.

Also, I suspect that the "flying dinosaurs" you refer to are pterosaurs, and the "marine dinosaurs" are ichthyosaurs, plesiosaurs, mosasaurs, and the like. None of these are dinosaurs under the scientific definition of that term.

Sorry for a dumb newbie question - but why did the dinosaurs die out completely (including marine and flying dinosaurs), and not reptiles, birds, mammals, etc?

Those others died out almost completely. :-) The survivors seem to have had the common advantage that they didn't directly depend on green plant parts or on herbivores.

BTW, neither the marine nor the flying ones (except the birds) were dinosaurs!

(Sorry I didn't mention the birds earlier. Mesozoic birds were a wonderfully diverse bunch. Cenozoic birds -- from ostrich to penguin to vulture and back -- are all the same by comparison.)

as far from Yucatan as Australia.

And New Zealand, and Japan, and and and... :-)

David - is there another use of the term "crown" in the picture?

Dave - your idea of what became extinct could be phrased better. The flying dinosaurs are still with us. Pterosaurs and marine reptiles were not dinosaurs. Lots of marine species went extinct, perhaps due to acidification of the sea, or perhaps there was a dark 'nuclear winter' and the phytoplankton crashed.

A complete account and explanation of what survived and what didn't is not possible yet, but David will doubtless relate what can be related.

PZ: Thanks for posting the image. It may not be a groundbreaking paper, but it's a wonderful visual that I will probably put into a PPT some day.

David, others: Why did some lineages survive, and others didn't? In general, I think you will find that bigger isn't better. The megafauna don't survive the KT event, and the smaller the organism, the greater its chance of survival. The higher your trophic level, the more energy you require to sustain yourself, the greater chance you will go out of business when there is a major environmental disturbance. So, the big dinosaurs pretty much all went out of business and what survived were species lower on the trophic level, which also happened to be smaller and (in the case of the dinosauria) avian, or at least proto-avian. Just my two cents....SH

David - is there another use of the term "crown" in the picture?

No. For example, you'll see they put divergence between Tachyglossidae and Ornithorhynchidae ( = the origin of crown-group Monotremata) very shortly after the K-Pg boundary; clearly the Paleocene Monotrematum was considered an ornithorhynchid (or a tachyglossid, but there's no way to compare two isolated teeth to an echidna, so they clearly didn't do that).

A complete account and explanation of what survived and what didn't is not possible yet, but David will doubtless relate what can be related.

If possible I'll avoid it. I'd get stuck in details and keep writing for hours. :-)

David, others: Why did some lineages survive, and others didn't? In general, I think you will find that bigger isn't better. [...]

Correct. Except maybe for some terrestrial crocs, nothing terrestrial heavier than 25 kg or something survived, probably for the reasons you mention.

Scott,

No "pro-" about it: the particular birds that survived the K/T extinction were full-on, honest-to-goodness, modern-type (that is, crown-group) birds. Granted, none were species that currently exist today, but they included in their number members of lineages that are still around.

Birds (the group Aves) are just as much a part of Dinosauria as are tyrannosaurs or brachiosaurids or ceratopsians.

Thanks - I knew this was a hypothesis a decade or more ago, but I didn't know it was now considered fact.

Also, I suspect that the "flying dinosaurs" you refer to are pterosaurs, and the "marine dinosaurs" are ichthyosaurs, plesiosaurs, mosasaurs, and the like. None of these are dinosaurs under the scientific definition of that term.

Ok, I didn't know that. But it would certainly be less confusing if they dropped the "saur" suffix :)

"Such as?"

Well David, I am not as familiar with the literature as I ought to be and so you might be correct. I am just a muddle-headed neontologist. However the lack of fossil evidence for obviously diagnosable crown group members of extant orders does not disqualify the molecular conclusions out of hand. It doesn't mean the lineages didn't exist either as ghost lineages or as morphologically nonderived lineages that appear to be members of stem clades.

The calibration points though. . . well dating techniques are only as good as their calibration points. I often mistrust the calibration in these studies. So I guess I'll hedge (or Hedges and Kumar) my bets for now.

And PZ: I doubt anyone thought this one group collected al the data but it is possible that some of your readers might have thought that the authors combined the sequence data from previous research and done their own new analysis. The difference between doing this and creating a supertree using the pre-existing trees themselves is not trivial.

This is the first time that I am exposed to the results and conclusions of such a thorough work. It might have been previously published in less thorough papers, but the thing that struck me the most was that our closest relatives, other than the rest of the primates, are rodents and rabbits/hares. Talk about serendipity in choosing model animals, other than primates, for biomedical research when none of this was known.

What about birds? The K-T boundaray is infamous for the extinction of dinosaurs, but a fair portion of them, namely birds, did not go extinct. Could birds have played a role in preventing mammals from expanding to fill the niches left open by the extinction of other dinosaurs?

I think lifestyle (niche) diversification within already-existing taxa is as at least as interesting - and ecologically and evolutionarily important - as taxonomic diversity within a group of small mammals within a narrower range of niches, and not simply dismissible as anthropocentric perceptual bias. Those species occupying extreme niches within current radiations may give rise to novel higher-order taxa (e.g. origin of tetrapods, amniotes).

Talk about serendipity in choosing model animals, other than primates, for biomedical research when none of this was known.

Quite so!

(The general shape of the tree by Bininda-Emonds et al. is quite robust; since 2001 all molecular analyses have found that shaped, except when they were so plagued by long-branch attraction that the authors themselves pointed that out.)

However the lack of fossil evidence for obviously diagnosable crown group members of extant orders does not disqualify the molecular conclusions out of hand. It doesn't mean the lineages didn't exist either as ghost lineages

That's of course correct. But we have pretty large mammal faunas from several places in the world in the Late Cretaceous; the fact that they all lack placentals and marsupials makes it quite improbable that those groups were actually present in the diversity predicted by Bininda-Emonds et al..

Of course, several Cretaceous mammals have been suggested at one point or another to be placentals or marsupials. For all of those (except the recently described Nortedelphys and friends) alternative suggestions are at least as well supported, however.

or as morphologically nonderived lineages that appear to be members of stem clades.

Here, however, you (and plenty of molecular biologists, unfortunately) are saying that all fossilizable innovations of the crown-groups evolved at least twice within the crown-group in question. This is mighty unparsimonious.

What about birds?

The fossil record of birds is too bad to tell exactly when all those groups died out, but lots of bird clades were present in the Late Cretaceous and have not been found in younger strata.

However, crown-group birds were present in the Cretaceous. For example, Vegavis is a crown-group anseriform, more closely related to the ducks + geese + swans than to the screamers and even the magpie goose. That said, Anseriformes is close to the base of the bird crown-group (Neornithes).

Talk about serendipity in choosing model animals, other than primates, for biomedical research when none of this was known.

I don't think it is the rodent's close relationship to primates that makes them good models for biomedical research. Of far greater importance is their size, rapid maturity, large breeding capacity, ease of husbandry etc. Non-rodent mammals are used in research (relativly common = cats, dogs and ferrets and uncommon = horses, sheep) but it is not their distance from the primates that makes them less commonly used.

James Orpin

I don't think it is the rodent's close relationship to primates that makes them good models for biomedical research. Of far greater importance is their size, rapid maturity, large breeding capacity, ease of husbandry

I agree with you. It was the ease of husbandry and the other characteristics you cite that were the decision factors back then. What I'm saying is that we are lucky to have used mice, rats and rabbits. I wonder how much harder would progress in drug development and human molecular biology, to cite just two, have been if extrapolations weren't so easy, due to philogenetic distance from the models

Interesting stuff. A few questions:

Is it possible that the KT event destroyed many niches and thereby reduced the ability of mammals to radiate?

Is it possible to have open niches that were not filled at all? If so, how do we know there is a niche if nothing is filling that niche?

every once in a while I have a slight twinge of regret that in the 8th grade I put away my books on paleontology in favor of physics, This would be one of those moments.

thanks.

the interesting thing to me is how evolution is blind to the future, whereas intelligent design would not be. In a very stable environment, one useful evolutionary strategy is to make huge efficient creatures without regard to whether that makes them unusually susceptible to small environmental change. Consider the enormous aircraft people build in a quest for a few percents of efficiency. If some legislation appeared banning all flights of more than one hundred miles, these planes would disappear but helicopters and cessnas would not

Obviously, Pakicetus is not a crown-group whale. The crown-group of Cetacea (Autoceta) is much younger.

Wow, that is a huge mistake. Are we sure they weren't using Pakicetus to give a minimum age for the divergence of the Cetecea *stem* group? That would make a lot more sense.

Anyway, an additional problem with all this is that people are missing that mammal diversity *did* spike after the K-T event, it's just that this spike was mostly not organisms falling within modern crown groups. Why should this be surprising? Crown groups are *defined* based on a more-or-less arbitrary sample of what is existing at one slice of time -- namely, the present. Even on a *pure* null model where speciation and extinction are **completely random events**, we should *expect* that crown group lineages will encompass represent less and less of the fossil diversity as we look back in time. If extinction occurs, which we know it does, this is utterly unavoidable.

This study would be more impressive if they had compared the crown group frequency to some kind of null model.

Just to slightly pick at one of Mr. Marjanovic's points, although I will fully admit I know far less about the subject than he seems to...

The relative lack of placentals and marsupials in known mammal faunas from the late cretaceous doesn't really seem tome to provide a strong case that such groups did not exist. Assuming Eomaia scansoria is a proper Eutherian (and Mr Marjanovic did not seem to argue that point), then we know Eutherians were around 125 million years ago. If there are comparatively few fossil examples of eutherians in the mesozoic record, then we have little information about what this particular lineage was doing during the mesozoic. Proto-placentalians may have been minor members of the fauna, as Mr. Marjanovic indicates, but they still could have been divided into several lineages that gave rise to different modern placental orders after the age of the dinosaurs. Even assuming that all mesozoic eutherians should be treated as outgroups to modern placentals, my impression is that the fossil record of the lineage leading to modern placentalians is not in violent confllict with the molecular dates.

Anyway, that is my naive view....

If you want a Texas-sized tree that includes all of life - including cephalopods - go to http://www.zo.utexas.edu/faculty/antisense/DownloadfilesToL.html

It may be a bit outdated, but hey, it has 3000 species, and it's designed to be printed on 54-inch-wide paper.

David Marjanović thinks

a placental and a marsupial radiation in the Cretaceous are surprising results

in seeming ignorance of the tectonic timetable for isolation of South America from Australia.

When I looked at the diagram, almost the first thing I noticed (and double checked because I don't memorise such details) was that didelphimorphia and paucituberculata had to be American opossums.

I would like to recommend to people the paper that John Hunter and I published earlier this year in the Journal of Mammalian Evolution, that extensively summarizes the fossil record evidence (or lack thereof) for a significant radiation of crown group placentals much before the start of the Cenozoic. If more/different fossil evidence were to become apparent, I would readily change my opinion.

Note that the authors of this paper do not "show" that placentals were diversifying in the mid Cretaceous, they have *extrapolated* this conclusion from their data, which is not quite the same thing. Of course, the actual age of fossils in rocks is an extrapolation (or inference) as well, but one that I consider to be on a bit stronger footing.

Wow, that is a huge mistake. Are we sure they weren't using Pakicetus to give a minimum age for the divergence of the Cetecea *stem* group? That would make a lot more sense.

Yes, but look at the tree: they put the divergence between baleen whales and toothed whales into what seems to be the Eocene. Or have a look at their calibration point for Monotrematum, the only known Paleocene monotreme -- the divergence between Tachyglossidae and Ornithorhynchidae is right after the K-Pg boundary, fitting the age of Monotrematum, so Bininda-Emonds et al. seem to consider M. an ornithorhynchid.

This study would be more impressive if they had compared the crown group frequency to some kind of null model.

I agree.

Note how little time passed between reception and acceptance (just over 3 months) and between acceptance and publication (just under 2). That's very fast.

The relative lack of placentals and marsupials in known mammal faunas from the late cretaceous doesn't really seem tome to provide a strong case that such groups did not exist. Assuming Eomaia scansoria is a proper Eutherian

Indeed it is. It is close to the base of Eutheria, however, while Placentalia is the crown-group of Eutheria. It can be used to calibrate the split between Placentalia and Marsupialia (or rather Eutheria and Metatheria), which Bininda-Emonds et al. did; it has no bearing on the time of origin of Placentalia.

If there are comparatively few fossil examples of eutherians in the mesozoic record

This, however, is not the case. Non-placental eutherians are pretty common in the Late Cretaceous of central Asia (from Uzbekistan to Mongolia), western North America, and Europe (though very few Late Cretaceous mammals are known from Europe in total, so this may not count). Possible placentals (cimolestans, taeniodonts) are rare, and certain placentals are absent so far.

The same holds for non-marsupial metatherians and marsupials.

Proto-placentalians may have been minor members of the fauna, as Mr. Marjanovic indicates, but they still could have been divided into several lineages that gave rise to different modern placental orders after the age of the dinosaurs.

This is of course correct; neither the fossil record nor our current knowledge of it are complete. But have another look at the tree: I count not two, not five, not ten, but forty-two lineages of Cretaceous placentals and marsupials, and those are just those that happen to have left extant descendants. That so many lineages were present in the Cretaceous but are so far absent from the fossil record is not probable. (I can't do the math off the top of my head, but it can be done -- a paper has recently been submitted which does something like this for amphibians.)

in seeming ignorance of the tectonic timetable for isolation of South America from Australia.

Granted, the entire terrestrial fossil record from the Late Cretaceous of Australia is currently limited to one dinosaur bone. Anything could have been present or absent. And you are right that the didelphimorphians and paucituberculates are South American marsupials.

However, you have overlooked four important things.

One is the fossil record of South America. Plenty of mammals are known from its Late Cretaceous layers. What mammals? Dryolestoids all over the place, plus a few gondwanatheres. That's it. No metatherians, no eutherians except maybe one tooth.

Another is the fossil record of Madagascar. South America and Madagascar had almost the same dinosaurs in the Late Cretaceous because they were connected for much or maybe all of that time via Antarctica, India, and the Seychelles. There are fossil mammals known from the Late Cretaceous of Madagascar: a gondwanathere, an unpublished weirdo known from a complete skeleton or something, and one tooth that was initially interpreted as a metatherian but has been reinterpreted as a probably non-placental eutherian.

This brings us to India. One gondwanathere; a few teeth and ankle bones of what seem to be non-placental eutherians.

Now for the fourth. Metatheria did not originate in Gondwana but in Laurasia. There's a plethora of Mesozoic metatherians in Asia and North America, from the very base of their tree (Sinodelphys) to the end-Cretaceous "pediomyids" (shrew-like) and stagodontids (Tassie-devil-like). Indeed, superficially opossum-like metatherians survived the K-Pg boundary, temporarily even spread into Africa, and died out in the northern continents pretty late in the Miocene. In South America and Australia, Marsupialia (and the slightly larger group Notometatheria as a whole) appears in the Paleocene. Clearly, the ancestors of Notometatheria came from North to South America sometime around the K-Pg boundary (perhaps shortly before, as for example the hadrosaurid dinosaurs did), then had their initial radiation there and entered Australia via Antarctica in the early or middle Paleocene.

Note that the authors of this paper do not "show" that placentals were diversifying in the mid Cretaceous, they have *extrapolated* this conclusion from their data, which is not quite the same thing.

This extrapolation would be pretty robust if the calibration points were reliable and if the effect of maximal ages had been explored...

I'll try to get your paper, thanks for alerting me. :-)

I should have mentioned that the only certain fossil ornithorhynchids are Miocene and younger. There are no known fossil tachyglossids (apparently the group evolved in the underexplored New Guinea). There are no known fossil monotremes from the Eo- or Oligocene (or for that matter the Late Cretaceous... there are several from the Early Cretaceous, however). Thus, Bininda-Emonds et al. have obviously used Monotrematum to calibrate the divergence between Ornithorhynchidae and Tachyglossidae.

Oops, there are known fossil tachyglossids, but only from the Pleistocene and (I forgot) maybe the Pliocene, which doesn't change my point.

Oops... I didn't quite answer the question. Complete separation of Australia and Antarctica, eastern Antarctica icing over: apparently 45 Ma ago (mid-late Eocene). Separation of South America and Antarctica, western Antarctica icing over: some 37 Ma ago (late Eocene). Earliest marsupials in Australia: over 55 Ma ago (late Paleocene). Earliest marsupials in South America: up to 65 Ma ago (early Paleocene).

The Hunter & Janis paper is here; even if you don't have full access, you should be able to read the abstract. (I have read the paper a couple of months ago. It's very good. Of course, it inevitably suffers from the continuing lack of a morphological analysis of placental phylogeny of reasonable size.)

"That so many lineages were present in the Cretaceous but are so far absent from the fossil record is not probable. (I can't do the math off the top of my head, but it can be done -- a paper has recently been submitted which does something like this for amphibians.)"

This HAS been done --- see Foote et al. Science 1999.

Also --- a point that nobody seems to have realised. Even if it was true that we could trace the lineages of modern placentals back into the mid Cretaceous, it remains the case that no Mesozoic mammal is larger than around 5 kg (raccoon size), and most were much smaller. We don't see larger mammals, and ecological specializations such as true herbivory (multituberculates were too small to have been eating just leaves) or larger predators until some time into the Paleocene. So, in some way, the presence of dinosaurs must have been suppressing the *disparity* of mammals, if not the diversity.

A literal interpretation of the paper would be that, because modern placental lineages were there at the time of the dinosaurs, even without dinosaur extinction they would have carried on evolving into the types of large mammals that we see around today. This is highly unlikely, and there certainly is absolutely no evidence for that notion (supertrees don't reveal destiny!)

Is it possible that the meteor strike killed the large plants.
This would eventually do in the large herbivores, and then of course that would wipe out the large carnivores.

Perhaps it took some time for larger plants to grow, causing many mammals to grow larger so they could enjoy eating from the taller trees.

Just my little theory based on my limited knowledge of science.

Again, forgive my continued poking, but this is a fun subject to discuss.

As far as I am aware, zalambelestids and zhelestids are probably the closest outgroups to placentalia we currently know of (Taking the conservative view that these are outgroups and not actual placentalians), and the earliest members of these groups are 85-90 million years old. If this is so, then one could take the view that the _initial_ inerordinal divergences (i.e. between afrotheria and xenarthra) among placentalians could have occurred anytime between 65 million years ago and 90 million years ago, and maybe even a little further back. For that reason, I don't see an issue with creating the earliest divergences in the late creatceous, at least. Of course, I would change my feelings if there were fossils that landed between zhelestids and placentalians on a caldogram and dated back around 75 million years ago, are there such things?

I do agree skepticism is warranted for having so many lineages in the mesozoic, and I do think the author's statements about ecological diversification were odd, at best.

I have a very different set of reactions to this paper. I like the paper a lot, but I disagree with it. The fossil record indicates a post KT diversification of mammals. That does not go away with this molecular analysis.

Also, aside from this, I suspect the role of giant birds as the primary predator in many systems during the Paleocene results in some of the patterns we see.

Naturally, I've blogged on this:

http://gregladen.com/wordpress/?p=594

PZ wrote:

"We just didn't pay much attention to them until some subset of their descendants grew large enough to trample us or eat us."

Or numerous enough to eat up our food supply....

Baconeatingatheistjew wrote:

"Is it possible that the meteor strike killed the large plants.
This would eventually do in the large herbivores, and then of course that would wipe out the large carnivores."

Elephants do rather well on grass....

Seriously. I enjoyed the article and I rather like the tree. While I make no claims of being an expert, certainly not knowledgeable enough to critique the science, it appears from the comments that the relationships shown in the tree are fairly accurate, just the dates in question. I find it very curious that the bovines and cervines are closer to the cetaceans than to the equids, and that all of those are closer to the carnivora and chiroptera that to the rodentia!

"We just didn't pay much attention to them until some subset of their descendants grew large enough to trample us or eat us."

Or be us, of course. :)

Woodsong: One of the areas that may be contested on this is the position of the bats.

And you are right, that is of course one of the great findings of the last couple of decades, how the whales fit in. While it's probably true that one species is usually going to evolve into something that is not too different, when you get these major transitions such as terrestrial to aquatic, lots of stuff happens!

But as I say above, don't believe this paper yet. It's good, its important, but it is not the case that we can separate mammalian radiations from the KT event at this time!

Greg:

Whale evolution is indeed a fascinating subject. I had read that their ancestry was (surprisingly) closer to the hoofed mammals than to elephants, but I had thought of horses when I read that, not cattle. It's the placement of Carnivora in the same superfamily but not Rodentia that startled me. Or is that placement also in question?

In my comment above about "numerous enough to eat up our food supply", perhaps I should have written:

Or when they move into the cave with us and eat up our food... How much attention (and money) do we spend on rats?

This HAS been done --- see Foote et al. Science 1999.

Yes, but it should probably be updated. (I don't think the conclusion would change, though.)

I agree with post 46, Repenomamus giganticus from the middle Early Cretaceous being the exception that proves the rule.

Is it possible that the meteor strike killed the large plants.

This seems to be what happened, but keep in mind that trees are "large plants", and that you can't grow when you've starved to death... or what do you mean? ~:-|

As far as I am aware, zalambelestids and zhelestids are probably the closest outgroups to placentalia we currently know of

Things like Cimolesta and Leptictida are probably much closer, and present in the last stage of the Cretaceous but AFAIK not earlier. (They are seemingly still not inside the crown-group, but there's no good phylogenetic analysis of that part of the tree...)

If this is so, then one could take the view that the _initial_ inerordinal divergences (i.e. between afrotheria and xenarthra) among placentalians could have occurred anytime between 65 million years ago and 90 million years ago, and maybe even a little further back.

Fine -- but 42 such divergences is clearly too much.

Also, aside from this, I suspect the role of giant birds as the primary predator in many systems during the Paleocene results in some of the patterns we see.

The latest word on the gastornithids -- Diatryma is a junior synonym of Gastornis -- is that they were herbivores, eating e. g. palm hearts.

it appears from the comments that the relationships shown in the tree are fairly accurate, just the dates in question.

Yep. Part of the reason is that most of the tree is simply not new -- that's why it's called a supertree: it's a combination of trees that have already been published elsewhere.

I find it very curious that the bovines and cervines are closer to the cetaceans than to the equids, and that all of those are closer to the carnivora and chiroptera that to the rodentia!

That's normal. Every molecular analysis that doesn't suffer from obvious problems has found these relationships (using different combinations of different genes and different methods). Morphological analyses have since confirmed the sister-group relationship of hippos and whales (leaving the position of the ruminants as the only difference between morphology and molecules in the cetartiodactyl tree) and are so far inconclusive on the rest, though AFAIK monophyly of all herbivorous placentals has never been suggested.

What do elephants and whales have in common? Did you confuse the whales with the sea cows?

On the phylogenetic position of the bats, I'll try to dig up the link to the Pegasoferae paper (which is free-access). Pegasoferae is what the clade composed of Perissodactyla, Chiroptera and Carnivora (and by implication Pholidota) has been named. It is the sister-group of Cetartiodactyla. :-)

"What do elephants and whales have in common? Did you confuse the whales with the sea cows?"

No, but I seem to remember an article (sorry, I don't remember enough to find it again, although it was probably in the MSN Science News page) some years ago that mentioned a link between dugongs and elephants, commented on the morphological similarity between whales and dugongs (superficial, like the resemblance between dolphins and sharks), and went on to say that whales were (counter-intuitively) closer to the hoofed mammals than the apparently similar dugongs. It has been a few years, and I could be misremembering, but I think that was the gist of it.

I'd be interested in reading the Pegasoferae paper--I've (literally) found bats fascinating since I was a year old.

Looks like the download link is broken PZ. Either that or Firefox has really crapped out on me.

One major consequence of this study is of course that the Evolution of Homer
video has to be corrected. You clearly see rodent Homer waiting for the moment the Dino's are gone before he can evolve further.
I mean- otherwise it is completely accurate.

So, assuming that the Nature article is full of ($#)it, does Nature usually print a retraction, or does the full discussion get printed?

The K/T event sure sets the imagination on fire!

That's the message of a new paper in Nature that compiled sequence data from 4,510 mammalian species

No, they did not.

They took the literature, compiled a supertree from the (hopefully) phylogenetic analyses they found there, got sequences of 66 genes for as many mammals as possible, and then used those sequence data plus 30 calibration points to estimate some divergence dates on that supertree.

That's right: apart from its size, it's just yet another attempt at molecular dating.

And not a very good one. The age of the basal divergence (between the monotremes and the rest) was fixed at a rather arbitrary date out of the range of ages the oldest known fossil on the monotreme side of the split could have. The other ages were only used as minimal ages; maximal ages were not used, thus providing no protection against too old divergence date estimates. Of course maximal ages cannot be derived from the fossil record as easily as minimal ages, but the fossil record from some epochs is good enough to let us interpret absence of evidence as evidence of absence with more than 50 % confidence.

There are only three outgroups, increasing the risk that the lengths of these branches could have detrimental effects on the branch lengths in the ingroup...

No, it is not an earth-shattering paper, despite having been published as an "Article" (rather than "Letter") in Nature.

The KT extinction was devastating for just those animals we are attuned to recognize most readily, but may not have been quite so troubling to others; the bacteria didn't even notice, insects would have gone on buzzing (except those with dependent parasitic relationships), plants may have seen one minor class of leaf-nibblers disappear, the rat-like and lizard-like creatures of the undergrowth might well have found their environments relatively unchanged. That transient period of intense trauma might not have been as disturbing to the overall life of the planet as we big apes might like to imagine.

Not so. Studies of bite, mining, etc. marks on leaves around the Cretaceous-Paleogene boundary have shown that herbivorous insects suffered massively. Among mammals, one of the three groups of multituberculates disappeared, as did several clades of relatives of marsupials and placentals, and all but apparently one of the dryolestoid fauna of South America (Dryolestoidea being Yet Another Mammal Clade). The lizards were (as expected) hit less severely, but still suffered (for example a herbivorous clade died out). The turtles were decimated enough that a close relative of the alligators that was apparently a specialized turtle-eater died out. And so on.

And don't get me started on the Strangelove Ocean...

I should also have mentioned that, among the plants, the low-latitude conifers (Cheirolepidiaceae) vanished completely. There's also a mass extinction in angiosperm pollen types.

But it seems like these days we keep finding Cretaceous ancestors of many extant orders.

Such as?

In the meantime, I downloaded the first part of the supplementary information. Table 3 of http://www.nature.com/nature/journal/v446/n7135/extref/nature05634-s1.p… lists the calibration points. It contains (at least) the following mistakes:

- Monotrematum is probably not a crown-group monotreme. Thus, Monotremata may be younger than 63.6 Ma.
- Tribosphenomys is far from being a crown-group rodent! Rodentia (unlike Rodentiamorpha) is younger than 57.25 Ma (...and I wonder where they got such a precise date...). Note that the reference Bininda-Emonds et al. cite makes this quite clear (it coins the name Rodentiamorpha).
- Not that I knew anything, but I'd be quite surprised if Eodendrogale were a crown-group scandentian. Thus, the crown-group of Scandentia may well be younger than 44.5 Ma.
- Same for Dendrotherium being a crown-group dermopteran.
- The genus Tarsius is 44.5 Ma old? Difficult to believe. I'd say a name change is in order.
- Diacodexis is a paraphyletic series of species around the base of Cetartiodactyla (which means that at least some of those species should get new genus names). Putting "Diacodexis sp." into Suiformes does therefore not look defensible to me, but I'll try to find the reference.
- Obviously, Pakicetus is not a crown-group whale. The crown-group of Cetacea (Autoceta) is much younger.
- Eomanis is far from a crown-group pangolin...
- I'd be very surprised if Ageinia turned out to be a crown-group bat. Thus, chances are high that the crown-group of Chiroptera is younger than 52.2 Ma.
- I'd be surprised if Riostegotherium turned out to be a crown-group dasypodid. But that's outside my area of knowledge.
- The crown-group of Tubulidentata consists only of Orycteropus. Obviously Myorycteropus can't be part of that...
- Nortedelphys was indeed described as a didelphimorphian, but I don't buy it. It's "the tooth, the whole tooth, and nothing but the tooth" (as usual in the Mesozoic). In any case, considering it a crown didelphimorphian really stretches it.
- Paucituberculata... all extant paucituberculates are caenolestids, and the fossil is most likely not one of those...
- I bet the fossil notoryctid is outside the crown-group.

Much sloppier work than I imagined.

and my point is that seeing a mammalian radiation prior to the K/T boundary should not be a surprising result --

But a placental and a marsupial radiation in the Cretaceous are surprising results, and therefore I'm not surprised to find so much miscalibration in the paper. Both groups are currently completely absent from the Cretaceous (except for Nortedelphys and a few more problematic crumbs), no matter how common the remains of other mammals are, and no matter how small those are.

Sorry for a dumb newbie question - but why did the dinosaurs die out completely (including marine and flying dinosaurs), and not reptiles, birds, mammals, etc?

Those others died out almost completely. :-) The survivors seem to have had the common advantage that they didn't directly depend on green plant parts or on herbivores.

BTW, neither the marine nor the flying ones (except the birds) were dinosaurs!

(Sorry I didn't mention the birds earlier. Mesozoic birds were a wonderfully diverse bunch. Cenozoic birds -- from ostrich to penguin to vulture and back -- are all the same by comparison.)

as far from Yucatan as Australia.

And New Zealand, and Japan, and and and... :-)

David - is there another use of the term "crown" in the picture?

No. For example, you'll see they put divergence between Tachyglossidae and Ornithorhynchidae ( = the origin of crown-group Monotremata) very shortly after the K-Pg boundary; clearly the Paleocene Monotrematum was considered an ornithorhynchid (or a tachyglossid, but there's no way to compare two isolated teeth to an echidna, so they clearly didn't do that).

A complete account and explanation of what survived and what didn't is not possible yet, but David will doubtless relate what can be related.

If possible I'll avoid it. I'd get stuck in details and keep writing for hours. :-)

David, others: Why did some lineages survive, and others didn't? In general, I think you will find that bigger isn't better. [...]

Correct. Except maybe for some terrestrial crocs, nothing terrestrial heavier than 25 kg or something survived, probably for the reasons you mention.

Talk about serendipity in choosing model animals, other than primates, for biomedical research when none of this was known.

Quite so!

(The general shape of the tree by Bininda-Emonds et al. is quite robust; since 2001 all molecular analyses have found that shaped, except when they were so plagued by long-branch attraction that the authors themselves pointed that out.)

However the lack of fossil evidence for obviously diagnosable crown group members of extant orders does not disqualify the molecular conclusions out of hand. It doesn't mean the lineages didn't exist either as ghost lineages

That's of course correct. But we have pretty large mammal faunas from several places in the world in the Late Cretaceous; the fact that they all lack placentals and marsupials makes it quite improbable that those groups were actually present in the diversity predicted by Bininda-Emonds et al..

Of course, several Cretaceous mammals have been suggested at one point or another to be placentals or marsupials. For all of those (except the recently described Nortedelphys and friends) alternative suggestions are at least as well supported, however.

or as morphologically nonderived lineages that appear to be members of stem clades.

Here, however, you (and plenty of molecular biologists, unfortunately) are saying that all fossilizable innovations of the crown-groups evolved at least twice within the crown-group in question. This is mighty unparsimonious.

What about birds?

The fossil record of birds is too bad to tell exactly when all those groups died out, but lots of bird clades were present in the Late Cretaceous and have not been found in younger strata.

However, crown-group birds were present in the Cretaceous. For example, Vegavis is a crown-group anseriform, more closely related to the ducks + geese + swans than to the screamers and even the magpie goose. That said, Anseriformes is close to the base of the bird crown-group (Neornithes).

Wow, that is a huge mistake. Are we sure they weren't using Pakicetus to give a minimum age for the divergence of the Cetecea *stem* group? That would make a lot more sense.

Yes, but look at the tree: they put the divergence between baleen whales and toothed whales into what seems to be the Eocene. Or have a look at their calibration point for Monotrematum, the only known Paleocene monotreme -- the divergence between Tachyglossidae and Ornithorhynchidae is right after the K-Pg boundary, fitting the age of Monotrematum, so Bininda-Emonds et al. seem to consider M. an ornithorhynchid.

This study would be more impressive if they had compared the crown group frequency to some kind of null model.

I agree.

Note how little time passed between reception and acceptance (just over 3 months) and between acceptance and publication (just under 2). That's very fast.

The relative lack of placentals and marsupials in known mammal faunas from the late cretaceous doesn't really seem tome to provide a strong case that such groups did not exist. Assuming Eomaia scansoria is a proper Eutherian

Indeed it is. It is close to the base of Eutheria, however, while Placentalia is the crown-group of Eutheria. It can be used to calibrate the split between Placentalia and Marsupialia (or rather Eutheria and Metatheria), which Bininda-Emonds et al. did; it has no bearing on the time of origin of Placentalia.

If there are comparatively few fossil examples of eutherians in the mesozoic record

This, however, is not the case. Non-placental eutherians are pretty common in the Late Cretaceous of central Asia (from Uzbekistan to Mongolia), western North America, and Europe (though very few Late Cretaceous mammals are known from Europe in total, so this may not count). Possible placentals (cimolestans, taeniodonts) are rare, and certain placentals are absent so far.

The same holds for non-marsupial metatherians and marsupials.

Proto-placentalians may have been minor members of the fauna, as Mr. Marjanovic indicates, but they still could have been divided into several lineages that gave rise to different modern placental orders after the age of the dinosaurs.

This is of course correct; neither the fossil record nor our current knowledge of it are complete. But have another look at the tree: I count not two, not five, not ten, but forty-two lineages of Cretaceous placentals and marsupials, and those are just those that happen to have left extant descendants. That so many lineages were present in the Cretaceous but are so far absent from the fossil record is not probable. (I can't do the math off the top of my head, but it can be done -- a paper has recently been submitted which does something like this for amphibians.)

in seeming ignorance of the tectonic timetable for isolation of South America from Australia.

Granted, the entire terrestrial fossil record from the Late Cretaceous of Australia is currently limited to one dinosaur bone. Anything could have been present or absent. And you are right that the didelphimorphians and paucituberculates are South American marsupials.

However, you have overlooked four important things.

One is the fossil record of South America. Plenty of mammals are known from its Late Cretaceous layers. What mammals? Dryolestoids all over the place, plus a few gondwanatheres. That's it. No metatherians, no eutherians except maybe one tooth.

Another is the fossil record of Madagascar. South America and Madagascar had almost the same dinosaurs in the Late Cretaceous because they were connected for much or maybe all of that time via Antarctica, India, and the Seychelles. There are fossil mammals known from the Late Cretaceous of Madagascar: a gondwanathere, an unpublished weirdo known from a complete skeleton or something, and one tooth that was initially interpreted as a metatherian but has been reinterpreted as a probably non-placental eutherian.

This brings us to India. One gondwanathere; a few teeth and ankle bones of what seem to be non-placental eutherians.

Now for the fourth. Metatheria did not originate in Gondwana but in Laurasia. There's a plethora of Mesozoic metatherians in Asia and North America, from the very base of their tree (Sinodelphys) to the end-Cretaceous "pediomyids" (shrew-like) and stagodontids (Tassie-devil-like). Indeed, superficially opossum-like metatherians survived the K-Pg boundary, temporarily even spread into Africa, and died out in the northern continents pretty late in the Miocene. In South America and Australia, Marsupialia (and the slightly larger group Notometatheria as a whole) appears in the Paleocene. Clearly, the ancestors of Notometatheria came from North to South America sometime around the K-Pg boundary (perhaps shortly before, as for example the hadrosaurid dinosaurs did), then had their initial radiation there and entered Australia via Antarctica in the early or middle Paleocene.

Note that the authors of this paper do not "show" that placentals were diversifying in the mid Cretaceous, they have *extrapolated* this conclusion from their data, which is not quite the same thing.

This extrapolation would be pretty robust if the calibration points were reliable and if the effect of maximal ages had been explored...

I'll try to get your paper, thanks for alerting me. :-)

I should have mentioned that the only certain fossil ornithorhynchids are Miocene and younger. There are no known fossil tachyglossids (apparently the group evolved in the underexplored New Guinea). There are no known fossil monotremes from the Eo- or Oligocene (or for that matter the Late Cretaceous... there are several from the Early Cretaceous, however). Thus, Bininda-Emonds et al. have obviously used Monotrematum to calibrate the divergence between Ornithorhynchidae and Tachyglossidae.

Oops, there are known fossil tachyglossids, but only from the Pleistocene and (I forgot) maybe the Pliocene, which doesn't change my point.

Oops... I didn't quite answer the question. Complete separation of Australia and Antarctica, eastern Antarctica icing over: apparently 45 Ma ago (mid-late Eocene). Separation of South America and Antarctica, western Antarctica icing over: some 37 Ma ago (late Eocene). Earliest marsupials in Australia: over 55 Ma ago (late Paleocene). Earliest marsupials in South America: up to 65 Ma ago (early Paleocene).

The Hunter & Janis paper is here; even if you don't have full access, you should be able to read the abstract. (I have read the paper a couple of months ago. It's very good. Of course, it inevitably suffers from the continuing lack of a morphological analysis of placental phylogeny of reasonable size.)

This HAS been done --- see Foote et al. Science 1999.

Yes, but it should probably be updated. (I don't think the conclusion would change, though.)

I agree with post 46, Repenomamus giganticus from the middle Early Cretaceous being the exception that proves the rule.

Is it possible that the meteor strike killed the large plants.

This seems to be what happened, but keep in mind that trees are "large plants", and that you can't grow when you've starved to death... or what do you mean? ~:-|

As far as I am aware, zalambelestids and zhelestids are probably the closest outgroups to placentalia we currently know of

Things like Cimolesta and Leptictida are probably much closer, and present in the last stage of the Cretaceous but AFAIK not earlier. (They are seemingly still not inside the crown-group, but there's no good phylogenetic analysis of that part of the tree...)

If this is so, then one could take the view that the _initial_ inerordinal divergences (i.e. between afrotheria and xenarthra) among placentalians could have occurred anytime between 65 million years ago and 90 million years ago, and maybe even a little further back.

Fine -- but 42 such divergences is clearly too much.

Also, aside from this, I suspect the role of giant birds as the primary predator in many systems during the Paleocene results in some of the patterns we see.

The latest word on the gastornithids -- Diatryma is a junior synonym of Gastornis -- is that they were herbivores, eating e. g. palm hearts.

it appears from the comments that the relationships shown in the tree are fairly accurate, just the dates in question.

Yep. Part of the reason is that most of the tree is simply not new -- that's why it's called a supertree: it's a combination of trees that have already been published elsewhere.

I find it very curious that the bovines and cervines are closer to the cetaceans than to the equids, and that all of those are closer to the carnivora and chiroptera that to the rodentia!

That's normal. Every molecular analysis that doesn't suffer from obvious problems has found these relationships (using different combinations of different genes and different methods). Morphological analyses have since confirmed the sister-group relationship of hippos and whales (leaving the position of the ruminants as the only difference between morphology and molecules in the cetartiodactyl tree) and are so far inconclusive on the rest, though AFAIK monophyly of all herbivorous placentals has never been suggested.

What do elephants and whales have in common? Did you confuse the whales with the sea cows?

On the phylogenetic position of the bats, I'll try to dig up the link to the Pegasoferae paper (which is free-access). Pegasoferae is what the clade composed of Perissodactyla, Chiroptera and Carnivora (and by implication Pholidota) has been named. It is the sister-group of Cetartiodactyla. :-)