Paul Sereno— Dinosaurs: Phylogenetic reconstruction from Darwin to the present

Oops, missed the first part of this talk due to the distractions of Lunch. Walked in as he was talking about tree vs. ladder thinking (people have a hard time conceptualizing trees) and history as a chronicle — barebones description of events — or a narrative — events linked by causal explanations.

It took a century for biologists to use systematics to make testable hypotheses about evolution. Darwin himself talked at length about all kinds of evidence for evolution, but strangely neglected fossils and dinosaurs altogether. Sereno blames this on rivalry with Richard Owen, who was the big dinosaur man of the day. One fossil Darwin was pleased with was Archaeopteryx, and Huxley in particular made the link between Archy and birds. Sereno brought in fossil of Confuciusornis — very cool.

We have begun to separate out the chronology from the narrative; chronology is a limiting factor in our hypotheses. We are interested in the trajectory of change over time, and Sereno confesses to baldly exploiting that to get a publication in nature of Raptorex, but he carefully omitted any causal discussion in the paper, trusting readers to infer a narrative from the story, because that’s what we do.

Deplores the thinness of work in the philosophy of phylogeny.

History: Darwin crystallized many of the pieces of an existing chronology into an evolutionary narrative. The next big breakthrough was Hennig (1950) who atomized morphological transformations and branching patterns, defining specific terms to describe phenomena important for understanding trees. Quantitative cladistics (1969) put it on a solid empirical foundation. Character states were coded as mathematical variables.

Problem: everyone has a different matrix for the analysis of characters for each phylogeny examined. The matrix is a black box. We are searching for a methodology that will link everything together. A modern comparative cladistics would open up the black box for universal analysis. Need to figure out what the characters are, and need to be able to do comparative analysis. There is no global understanding of what a character or character state are. There is currently a movement to develop a universal character ontology.

He makes a strong case that we have a serious problem with different investigators studying the same phylogenies, but using different characters and even scoring them differently. We need to standardize to enable full comparisons of multiple data sets.

Darwinopterus and mosaic, modular evolution

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It’s yet another transitional fossil! Are you tired of them yet?

Darwinopterus modularis is a very pretty fossil of a Jurassic pterosaur, which also reveals some interesting modes of evolution; modes that I daresay are indicative of significant processes in development, although this work is not a developmental study (I wish…having some pterosaur embryos would be exciting). Here it is, one gorgeous animal.

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Figure 2. Holotype ZMNH M8782 (a,b,e) and referred specimen YH-2000 ( f ) of D. modularis gen. et sp. nov.: (a) cranium and mandibles in the right lateral view, cervicals 1-4 in the dorsal view, scale bar 5cm; (b) details of the dentition in the anterior tip of the rostrum, scale bar 2cm; (c) restoration of the skull, scale bar 5cm; (d) restoration of the right pes in the anterior view, scale bar 2 cm; (e) details of the seventh to ninth caudal vertebrae and bony rods that enclose them, scale bar 0.5 cm; ( f ) complete skeleton seen in the ventral aspect, except for skull which is in the right lateral view, scale bar 5 cm. Abbreviations: a, articular; cr, cranial crest; d, dentary; f, frontal; j, jugal; l, lacrimal; ldt, lateral distal tarsal; m, maxilla; mdt, medial distal tarsal; met, metatarsal; n, nasal; naof, nasoantorbital fenestra; p, parietal; pd, pedal digit; pf, prefrontal; pm, premaxilla; po, postorbital; q, quadrate; qj, quadratojugal; sq, squamosal; ti, tibia.

One important general fact you need to understand to grasp the significance of this specimen: Mesozoic flying reptiles are not all alike! There are two broad groups that can be distinguished by some consistent morphological characters.

The pterosaurs are the older of the two groups, appearing in the late Triassic. They tend to have relatively short skulls with several distinct openings, long cervical (neck) ribs, a short metacarpus (like the palm or sole of the foot), a long tail (with some exceptions), and an expanded flight membrane suspended between the hind limbs, called the cruropatagium. They tend to be small to medium-sized.

The pterodactyls are a more derived group that appear in the late Jurassic. Their skulls are long and low, and have a single large opening in front of the eyes, instead of two. Those neck ribs are gone or reduced, they have a long metacarpus and short tails, and they’ve greatly reduced the cruropatagium. Some of the pterodactyls grew to a huge size.

Here’s a snapshot of their distribution in time and phylogenetic relationships. The pterosaurs are in red, and the pterodactyls are in blue.

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Time-calibrated phylogeny showing the temporal range of the main pterosaur clades; basal clades in red, pterodactyloids in blue; known ranges of clades indicated by solid bar, inferred ‘ghost’ range by coloured line; footprint symbols indicate approximate age of principal pterosaur track sites based on Lockley et al. (2008); stratigraphic units and age in millions of years based on Gradstein et al. (2005). 1, Preondactylus; 2, Dimorphodontidae; 3, Anurognathidae; 4, Campylognathoididae; 5, Scaphognathinae; 6, Rham- phorhynchinae; 7, Darwinopterus; 8, Boreopterus; 9, Istiodactylidae; 10, Ornithocheiridae; 11, Pteranodon; 12, Nyctosauridae; 13, Pterodactylus; 14, Cycnorhamphus; 15, Ctenochasmatinae; 16, Gnathosaurinae; 17, Germanodactylus; 18, Dsungaripteridae; 19, Lonchodectes; 20, Tapejaridae; 21, Chaoyangopteridae; 22, Thalassodromidae; 23, Azhdarchidae. Abbreviations: M, Mono- fenestrata; P, Pterodactyloidea; T, Pterosauria; ca, caudal vertebral series; cv, cervical vertebral series; mc, metacarpus; na, nasoantorbital fenestra; r, rib; sk, skull; v, fifth pedal digit.

Darwinopterus is in there, too—it’s the small purple box numbered “7”. You can see from this diagram that it is a pterosaur in a very interesting position, just off the branch that gave rise to the pterodactyls. How it got there is interesting, too: it’s basically a pterosaur body with the head of a pterodactyl. Literally. The authors of this work carried out multiple phylogenetic analyses, and if they left the head out of the data, the computer would spit out the conclusion that this was a pterosaur; if they left the body out and just analyzed the skull, the computer would declare it a pterodactyl.

What does this tell us about evolution in general? That it can be modular. The transitional form between two species isn’t necessarily a simple intermediate between the two in all characters, but may be a mosaic: the anatomy may be a mix of pieces that resemble one species more than the other. In this case, what happened in the evolution of the pterodactyls was that first a pterodactyl-like skull evolved in a pterosaur lineage, and that was successful; later, the proto-pterodactyls added the post-cranial specializations. Not everything happened all at once, but stepwise.

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Schematic restorations of a basal pterosaur (above), Darwinopterus (middle) and a pterodactyloid (below) standardized to the length of the DSV, the arrow indicates direction of evolutionary transformations; modules: skull (red), neck (yellow), body and limbs (monochrome), tail (blue); I, transition phase one; II, transition phase two.

This should be a familiar concept. In pterodactyls, skulls evolved a specialized morphology first, and the body was shaped by evolutionary processes later. We can see a similar principle in operation in the hominid lineage, too, but switched around. We evolved bipedalism first, in species like Ardipithecus and Australopithecus, and the specializations of our skull (to contain that big brain of which we are so proud) came along later.

As I mentioned at the beginning, this is an example of development and evolution in congruence. We do find modularity in developmental process — we have genetic circuits that are expressed in tissue- and region-specific ways in development. We can talk about patterns of gene expression that follow independent programs to build regions of the body, under the control of regional patterning genes like the Hox complex. In that sense, what we see in Darwinopterus is completely unsurprising.

What is interesting, though, is that these modules, which we’re used to seeing within the finer-grained process of development, also retain enough coherence and autonomy to be visible at the level of macroevolutionary change. It caters to my biases that we shouldn’t just pretend that all the details of development are plastic enough to be averaged out, or that the underlying ontogenetic processes will be overwhelmed by the exigencies of environmental factors, like selection. Development matters — it shapes the direction evolution can take.

Lü J, Unwin DM, Jin X, Liu Y, Ji Q (2009) Evidence for modular evolution in a long-tailed pterosaur with a pterodactyloid skull. Proc. R. Soc. B published online 14 October 2009 doi: 10.1098/rspb.2009.1603

I should have mentioned that Darren Naish has a very thorough write-up on Darwinopterus!

Ardipithecus ramidus

What a day to be stuck in airplanes for hours on end; I had to slurp in a bunch of files on my iPhone and then look at them on that itty-bitty screen, just to catch up on the story of Ardipithecus. Fortunately, you can just read Carl Zimmer’s excellent summary to find out what’s cool about it.

For a summary of a summary: it’s another transitional fossil in our lineage. Ardipithecus ramidus is old, 4.4 million years or so — so it’s well before Lucy and the australopithecines. The latest result is a thorough analysis of a large number of collected specimens that shows it is an interesting mosaic of traits: it was bipedal, but not quite so well adapted to terrestrial locomotion as we are, and it had feet with an opposable big toe. And of course it had a small brain, only a little larger than a chimpanzee’s.

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Digital representations of the Ar. ramidus cranium and mandible. (A to D) The ARA-VP-6/500 and downscaled ARA-VP-1/500 composite reconstruction in inferior, superior, lateral, and anterior views (in Frankfurt horizontal orientation). (E) Individual pieces of the digital reconstruction in different colors. Note the steep clivus plane intersecting the cranial vault on the frontal squama (as in Sts 5 and not apes). (F and G) Lateral and superior views of the ARA-VP-1/401 mandible (cast). (H and I) Lateral and superior views of the ARA-VP-6/500 left mandibular corpus with dentition.

Ardipithecus is clearly different from (but related!) to us, and it’s also very different from a chimpanzee. One thing I’m finding baffling in all the commentary is the argument that this somehow shows that the last common ancestor of humans and chimpanzees would have been very unchimpanzee-like, and perhaps closer in morphology to us than to modern chimps. I’m not buying it. Has anybody actually ever suggested that chimpanzees have been in a state of relative stasis for 6 million years? Chimps have evolved in parallel with us for all of that time, so that argument is addressing a non-controversy, or at least, an argument that should have been recognized as silly all along.

We’re also going to have to push the fossil record back another couple of million years to get to that last common ancestor, and there’s no reason to presume that Ardi’s ancestors weren’t also rather different from Ardi. We also need to know more about the breadth of the primate family tree at that time; was Ardi a weirdly specialized sub-branch, or actually representative of a wider trend in the ape species that would lead to us? I think this image is a nice way to illustrate Ardipithecus‘s place in the family tree.

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Evolution of hominids and African apes since the gorilla/chimp+human (GLCA) and chimp/human (CLCA) last common ancestors. Pedestals on the left show separate lineages leading to the extant apes (gorilla, and chimp and bonobo); text indicates key differences among adaptive plateaus occupied by the three hominid genera.

Don’t get me wrong: Ardipithecus is a magnificent addition to our family album, and the author’s of the multiple papers that have come out have done a very impressive job of analysis and documentation. We can all jump up and down with joy at these new data, and we can rightly point to this species and say, “Transitional form! Boo-ya, creationists!”

Unfortunately, I’m also seeing the press mangling the story already. National Geographic says, Oldest “Human” Skeleton Found—Disproves “Missing Link”, which is annoying. The article itself isn’t bad, but can we just kill the “missing link” nonsense altogether? It’s as if the only way some science journalists can grasp a new discovery is by relating it to a misbegotten misconception.

The prize for the very worst coverage has to go to Metro News and the Torstar News Service (is that from the Toronto Star?). They put up an article titled New theory may answer missing link question, which opens with the bizarre assertion, Man didn’t descend from apes. There is no new theory here. There is new evidence and further data documenting the details of one lineage’s descent. And if you put the phrase “missing link” in your headline any more, we’re going to have to put a silly hat on your editors and make them sit in a corner.

But the very worst part is this misinterpretation of the suggestion that the LCA of humans and chimps would have had characters we consider human-like. I guarantee you that this will be the core of the creationist response to Ardi in the near future.

The four-foot, 110-pound female’s skeleton and physiological characteristics bear a closer resemblance to modern-day humans than to contemporary apes, meaning they evolved from humanlike creatures — not the other way around.

Brace yourself, gang. The creationists are going to be claiming that this shows humans were created first, and all of these other hairy beasts the paleontologists are digging up are just degenerate spawn of the Fall.

Arthrodires got penises!

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This is the skull of an arthrodire, an armored placoderm from the Devonian.

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Somehow, 20 foot long predatory fish with a mouth lined with razor-edged bony shears has never made me think of sexy time…until I ran across this comparison image.

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Oh, schwiiing. It really doesn’t take much to get a mammal to associate just about anything with sex. And then, what do you know, the latest Nature has a short article on an interesting fossil: it’s the pelvic region of an arthrodire, Incisoscutum ritchiei, and look what it’s got: an ossified clasper, comparable to the erectile organ of modern sharks. This is a bony rod that would have been the core of an intromittent organ in the living animal, so what we have here is a small relic of the sex life of a big fish from a few hundred million years ago.

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a, Pelvic girdle in dorsal view; b, pelvic girdle restored.

Think about this, you over-sexed apes: what will be left of your manhood 300 million years from now?

Ahlberg P, Trinajstic K, Johanson Z, Long J (2009) Pelvic claspers confirm chondrichthyan-like internal fertilization in arthrodires. Nature 460:888-889.

Big love among the ostracods

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How can anyone resist an article titled “Sexual Intercourse Involving Giant Sperm in Cretaceous Ostracode”? You can’t, I tell you. It’s like a giant brain magnet, you open the journal to the index, and there’s that title, and you must read it before you can even consider continuing on to anything else.

Some organisms have evolved immensely long sperm tails — Drosophila bifurca, for instance, has sperm cells that are about 60mm long, or 20 times longer than the length of the entire adult body. The excessively long sperm tail is obviously not a structure that has evolved for better swimming; instead, it is thought to act as a tangled barrier in the female reproductive tract to prevent other males from fertilizing the female, and there is also some very interesting evidence that sperm coevolves with the female reproductive tract, so some sexual selection at the level of the gametes is going on.

At the same time, sperm morphology is extremely diverse, and seems to evolve very rapidly. Perhaps these mega-sperm are a transient fad? Not all species of Drosophila exhibit the phenomenon, and those that do vary considerably from species to species. What we’d like to know is if there are any lineages that maintain these patterns of giant sperm over long periods of evolutionary time…so what do we need to do? We need to go spelunking for sperm in fossils!

That’s what this short letter in Science is about: the authors looked at ostracodes, a class of tiny crustacea that invests heavily in reproduction. About a third of their volume is their reproductive system, with males building giant (relative to their size) sperm pumps, and females having large seminal receptacles for sperm storage. The individual sperm are also large, often longer than the body length of the adult, and are also aflagellate — no flagellar tail at all, just a long, threadlike cell body. You can tell if a female ostracod is a virgin just by looking at those seminal receptacles, since they inflate hugely with all the giant sperm tucked inside.

So, if you look at the large orange blobs, the seminal receptacles, in this 3-D scan of a fossil female ostracod (bottom right of this image), you can tell that she was inseminated before she died, and that her mate had very large sperm. Her condition was also very similar to that of modern ostracodes (bottom left).

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Partial reconstruction of E. virens (extant) and H. micropapillosa (fossil). Anterior is to the left. Orange structures indicate central tubes of Zenker organs in males or seminal receptacles in females; brown, esophagus; turquoise, mandible; purple, upper lip; pink, lower lip; green, valves; and gray scales, whole-body reconstruction. All scale bars indicate 100 µm. (A) Lateral view of male E. virens with several organs included for comparison. (B) Male H. micropapillosa in lateral view with several organs in context of whole-body reconstruction. (C and D) Ventral views of several organs including tubes of Zenker organs of male H. micropapillosa. (E) Lateral view of female E. virens with several organs included for comparison. (F) Female H. micropapillosa in lateral view with several organs in context of whole-body reconstruction, including seminal receptacles.

So, the conclusion is that boinking with giant sperm is an enduring property of at least some lineages: they’ve been going at it for a hundred million years. The authors also suggest that this kind of technique could be useful for measuring sexual selection by assessing pre-mating parental investment in fossil invertebrates.

Matzke-Karasz R, Smith RJ, Symonova R, Miller CG, Tafforeau P (2009) Sexual Intercourse Involving Giant Sperm in Cretaceous Ostracode. Science 324(5934):1535.

Miller GT, Pitnick S (2002) Sperm-Female Coevolution in Drosophila. Science 298(5596):1230-1233.

Limusaurus inextricabilis

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My previous repost was made to give the background on a recent discovery of Jurassic ceratosaur, Limusaurus inextricabilis, and what it tells us about digit evolution. Here’s Limusaurus—beautiful little beastie, isn’t it?

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Photograph (a) and line drawing (b) of IVPP V 15923. Arrows in a point to a nearly complete and fully articulated basal crocodyliform skeleton preserved next to IVPP V 15923 (scale bar, 5 cm). c, Histological section from the fibular shaft of Limusaurus inextricabilis (IVPP V 15924) under polarized light. Arrows denote growth lines used to age the specimen; HC refers to round haversian canals and EB to layers of endosteal bone. The specimen is inferred to represent a five-year-old individual and to be at a young adult ontogenetic stage, based on a combination of histological features including narrower outermost zones, dense haversian bone, extensive and multiple endosteal bone depositional events and absence of an external fundamental system. d, Close up of the gastroliths (scale bar, 2 cm). Abbreviations: cav, caudal vertebrae; cv, cervical vertebrae; dr, dorsal ribs; ga, gastroliths; lf, left femur; lfl, left forelimb; li, left ilium; lis, left ischium; lp, left pes; lpu, left pubis; lsc, left scapulocoracoid; lt, left tibiotarsus; md, mandible; rfl, right forelimb; ri, right ilium; rp, right pes; sk, skull.

What’s especially interesting about it is that it catches an evolutionary hypothesis in the act, and is another genuine transitional fossil. The hypothesis is about how fingers were modified over time to produce the patterns we see in dinosaurs and birds.

Birds have greatly reduced digits, but when we examine them embryologically, we can see precisely what has happened: they’ve lost the outermost digits, the thumb (I) and pinky (V), and retain the forefinger, middle finger, and ring finger (II-IV), which have been reduced and fused together. This is called Bilateral Digit Reduction, BDR, because they’ve lost digits from the medial and lateral sides, leaving the middle set intact.

Dinosaurs, when examined anatomically, seem to have a different pattern: they have a thumb (I), forefinger (II) and middle finger (III), and have lost the lateral two digits, the ring and pinky finger (IV-V). This arrangement has been advanced as evidence that birds did not evolve from dinosaurs, since they have different bones in their hands, and getting from one pattern to the other is complicated and difficult and very unlikely.

The alternative hypothesis is that there is no conflict, and that dinosaurs actually underwent BDR and their digits are II-III-IV…but that what has also happened is a frame shift in digit identities. So dinosaurs actually have three digits, which are the index, middle, and ring finger, but they’ve undergone a subtle shift in morphology so that their forefinger develops as a thumb, and so forth.

Now we could resolve all this easily if only the physicists would get to work and build that time machine so we could go back to the Mesozoic and study dinosaur embryology, but they’re too busy playing with strings and quanta and dark matter to do the important experiments, so we’ve got to settle for another plan: find intermediate forms in the fossil record. That’s where Limusaurus steps in.

Limusaurus has a thumb, a tiny vestigial nubbin, and has lost its pinky completely. This is a (I)-II-III-IV pattern, and is evidence of bilateral digit reduction in a basal ceratosaur. In addition, the forefinger has become very robust, and while still distinctly a digit II, has been caught in the early stages of a transformation into a saurian first digit. It’s evidence in support of the dinosaurian II-III-IV hypothesis and the frameshift in digit identity! It’s almost as good as having a time machine.

Want to learn more? Carl Zimmer has a summary of the digit changes, while one of the authors of the paper, David Hone, also discusses the digits (the story is a little more complicated than I’ve laid out), and also has more on the rest of the animal—it’s a herbivorous ceratosaur, which is interesting in itself.

Xu X, Clark JM, Mo J, Choiniere J, Forster CA, Erickson GM, Hone DWE, Sullivan C, Eberth DA, Nesbitt S, Zhao Q, Hernandez R, Jia C-k, Han F-l, Guo Y (2009) A Jurassic ceratosaur from China helps clarify avian digit homologies. Nature 459(18):940-944.

Darwinius masillae

This is an important new fossil, a 47 million year old primate nicknamed Ida. She’s a female juvenile who was probably caught in a toxic gas cloud from a volcanic lake, and her body settled into the soft sediments of the lake, where she was buried undisturbed.

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What’s so cool about it?

Age. It’s 47 million years old. That’s interestingly old…it puts us deep into the primate family tree.

Preservation. This is an awesome fossil: it’s almost perfectly complete, with all the bones in place, preserved in its death posture. There is a halo of darkly stained material around it; this is a remnant of the flesh and fur that rotted in place, and allows us to see a rough outline of the body and make estimates of muscle size. Furthermore, the guts and stomach contents are preserved. Ida’s last meal was fruit and leaves, in case you wanted to know.

Life stage. Ida is a young juvenile, estimate to be right on the transition from requiring parental care to independent living. That means she has a mix of baby teeth and adult teeth — she’s a two-fer, giving us information about both.

Phylogeny. A cladistic analysis of the fossil revealed another interesting point. There are two broad groups of primates: the strepsirrhines, which includes the lemurs and lorises, and the haplorhines, which includes monkeys and apes…and us, of course. Ida’s anatomy places her in the haplorhines with us, but at the same time she’s primitive. This is an animal caught shortly after a major branch point in primate evolutionary history.

She’s beautiful and interesting and important, but I do have to take exception to the surprisingly frantic news coverage I’m seeing. She’s being called the “missing link in human evolution”, which is annoying. The whole “missing link” category is a bit of journalistic trumpery: almost every fossil could be called a link, and it feeds the simplistic notion that there could be a single definitive bridge between ancient and modern species. There isn’t: there is the slow shift of whole populations which can branch and diverge. It’s also inappropriate to tag this discovery to human evolution. She’s 47 million years old; she’s also a missing link in chimp evolution, or rhesus monkey evolution. She’s got wider significance than just her relationship to our narrow line.

People have been using remarkable hyperbole when discussing Darwinius. She’s going to affect paleontology “like an asteroid falling down to earth”; she’s the “Mona Lisa” of fossils; she answers all of Darwin’s questions about transitional fossils; she’s “something that the world has never seen before”; “a revolutionary scientific find that will change everything”. Well, OK. I was impressed enough that I immediately made Ida my desktop wallpaper, so I’m not trying to diminish the importance of the find. But let’s not forget that there are lots of transitional forms found all the time. She’s unique as a representative of a new species, but she isn’t at all unique as a representative of the complex history of life on earth.

When Laelaps says, “I have the feeling that this fossil, while spectacular, is being oversold,” I think he’s being spectacularly understated. Wilkins also knocks down the whole “missing link” label. The hype is bad news, not because Ida is unimportant, but because it detracts from the larger body of the fossil record — I doubt that the media will be able to muster as much excitement from whatever new fossil gets published in Nature or Science next week, no matter how significant it may be.

Go ahead and be excited by this find, I know I am. Just remember to be excited tomorrow and the day after and the day after that, because this is perfectly normal science, and it will go on.

Laelaps has some serious reservations about the analysis — the authors may not have done as solid a cladistic analysis as they should, and its position in the family tree may not be as clear as it has been made out to be.

Franzen JL, Gingerich PD, Habersetzer J, Hurum JH, von Koenigswald W, Smith BH (2009) Complete Primate Skeleton from the Middle Eocene of Messel in Germany: Morphology and Paleobiology. PLoS ONE 4(5): e5723. doi:10.1371/journal.pone.0005723.