Neil Shubin—“Major Transitions” in Evolution: Fossils, Genes, and Embryos

Shubin had a tough act to follow, coming after Kingsley’s great talk. I’m sure it will be good, though — last night I got a tour of his lab, saw the original Tiktaalik specimens and some new ones, and some of his work in progress (which I won’t tell you about until it’s published), so I’m confident I’m going to have a happy hour.

Darwin pulled together diverse lines of evidence to document his ideas. The different lines all reinforce each other making the argument even stronger, and what we’re seeing now is new syntheses, which is the theme of this talk: how do we use different lines of evidence to make a case that is more the sum of its parts.

The questions is the origin of limbs, fins to legs. Fins and legs look very different, with fins having rays and many bones, while legs have few bones in a fixed pattern. Intermediate taxa show us the changes, with transitions with bony core of the limb pattern and fish-like rays. He uses geology and extant fossils to make predictions about where to find intermediates, and paleontology also informs his understanding of developmental processes that build the limb.

Began his work in Pennsylvania, which was like the Amazon delta 360 million years ago. They followed the PA dept. of transportation around looking at road cuts that exposed the rocks of that age. They found many fossils, but one that changed his thinking was a fin of sauripterus, with fin rays and a core of tetrapod-like limbs. Definitely fishy, but contained precursors to the pattern.

They searched in Ellesmere Island for Devonian age rocks and fossils that would reveal the history of the limb. The logistics were very difficult, since the area is inaccessible. First started working in 1999, in rocks that were from marine sources and didn’t yield much. Moved east to freshwater sources. Found a layer of rock that was rich in bone, and found a snout of a flat-headed fish poking out. Eventually exposed about 20 specimens of this animal. Took months to fully expose the details of the specimen.

He showed off a cast of Tiktaalik — physical objects are really good at capturing people’s imagination.

It took a year and a half to prepare out the fins; the bones show articular surfaces, so you can actually see how the structure bent in life. What does this tell us about extant fins?

A tetrapod limb has 3 components: 1 bone, then 2 bones, then multiple bones in wrist and fingers. The limb forms in phases, with an early phase of hox expression that sets up the proximal bone, then phase II in which hox genes switch on in a patterned way to form digits. Are there elements of phase 2 in fish fins?

Looked in Polyodon, and embryos do have a distal phase of hox expression, not identical to tetrapod pattern, but definitely a phase 2.

What is a limb and how did it develop? The AER sets up the proximo-distal axis, ZPA sets up anteriorposterior axis. Cutting off the AER at different stages produces progressive deletions of portions of the limb. ZPA is a source of Sonic Hedgehog and sets up a gradient of positional information.

Does the common ancestor of all fish have these same two-axis signals? Chondrichthyans do, with patterns that can be manipulated in the same way as we do in chickens. The appendage patterning system is general to all vertebrate appendages.

How do fins differ from other outgrowths? Branchial arches have the same patterning, with an AER and ZPA. Seems to be a universal way for vertebrates to set up the patterning of outgrowths. Gill, fin, and limb have similar toolkits of patterning genes.

The patterning mechanisms may have originated in a general outgrowth and been coopted for limbs and gills. Shubin proposes to do targeted collecting of Ordovician vertebrates, expecting to find novel non-limb outgrowths that may be precursors to the patterning mechanism. Paleontology guided by developmental biology!

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


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.

(Click for larger image)

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.

(Click for larger image)

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.

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.

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!


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


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.


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.

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.