Balaur bondoc: flightless bird? or pre-bird?

This blogpost was modified June 22, 2015 with the addition of the red text and two cladograms pulled from Cau et al. 2015 along with a third from Brusatte et al. 2013.

Balaur bondoc (Figs. 1-6; EME PV.313, Csiki et al. 2010, Latest Cretaceous)is a mid-sized theropod dinosaur with not one, but two raised scythe claws on pedal digits 1 and 2 (Fig. 1). More typical forms of similar size, like Deinonychus and Velociraptor (Fig. 4), have only a single scythe claw.

Figure 1. The right foot of Balaur bondoc, a raptor-like theropod dinosaur known chiefly from its limbs and pelvis. Note the two scythe claws here. Yellow phalanges are raised off the substrate during terrestrial locomotion.

Figure 1. The right foot of Balaur bondoc, a raptor-like theropod dinosaur known chiefly from its limbs and pelvis. Note the two scythe claws here. Yellow phalanges are raised off the substrate during terrestrial locomotion. At left from Cau et al. 2015. Middle derived from that drawing. Right, traced from photo in Cau et al. 2015).

Originally
(Cziski et al. 2010) and later (Brusatte et al. 2013) Balaur nested with velociraptorine dromaeosaurids, based on the Theropod Working Group (TWiG) matrix. However, Cau et al (2015) noted that Balaur had a suite of autapomorphies not present in dromaeosaurids, nor in most other non-avialan theropods. These unique traits include a fused carpometacarpus, loss of a functional third manual digit, proximal fusion of the tarsometatarsus, and a relatively enlarged first pedal digit.

By contrast to the original nesting,
Cau et al. (2015) recovered Balaur more derived than Archaeopteryx among the birds. They used two prior theropod matrices in their study: Brusatte et al. (2014) and Lee et al. (2014). Cau et al. concluded, “Our reinterpretation of Balaur implies that a superficially dromaeosaurid-like taxon represents the enlarged, terrestrialised descendant of smaller and probably volant ancestors.” 

In other words,
Cau et al. nested Balaur after Archaeopteryx, which makes Balaur a flightless (= nonvolent) bird. Unfortunately Balaur was unlike the birds Cau et al. nested Balaur with, Sapeornis and Zhongjiaornis (Fig. 2). These two big-wing birds both have a pygostyle (reduced tail). Balaur does not. Details and other red flags follow.

Figure 2. Balaur compared to Zhongjiaornis and Sapeornis, sisters recovered by Cau et al. 2015. Unfortunagely both these taxa had a pygostyle and the former lacked teeth. Both also were likely volant based on the large size of their forelimbs.

Figure 2. Balaur compared to Zhongjiaornis and Sapeornis, sisters recovered by Cau et al. 2015. Unfortunagely both these taxa had a pygostyle and the former lacked teeth. Both also were likely volant based on the large size of their forelimbs.

Cau et al. 2015 
used the Brusatte et al. (2014) tree (860 characters vs. 152 taxa) to nest Balaur as a sister to Sapeornis (Fig. 1), a taxon with a pygostyle and very large forelimb/wings that was a more derived sister to Archaeopteryx. Cau et al. recovered more than a million MPTs in this test.

In addition, Cau et al. used the Lee et al. (2014) tree (1549 characters vs. 120 taxa) to nest Balaur close to Zhongjianopterus (Fig. 1) several nodes more derived than Archaeopteryx and slightly more derived than Sapeornis. Cau et al. recovered 1152 MPTs in this test.

Figure 3. Balaur nested in the large reptile tree between Aurornis and Archaeopteryx, two taxa with a long slender tail.

Figure 3. Balaur nested in the large reptile tree between Aurornis and Archaeopteryx, two taxa with a long slender tail.

Everyone acknowledges 
that Balaur is different than most other theropods. The goal here is to find out which theropods (birds included!) it is most like.

Added figure 3. Balaur sacral vertebrae colorized.

Added figure 4. Balaur sacral vertebrae colorized. Click to enlarge.

Unfortunately, or perhaps fortunately,
the matrix of the large reptile tree was not designed specifically for theropods. And worse yet, only about two dozen forelimb and hindlimb traits are preserved in Balaur that are listed in the large reptile tree character list. That’s a magnitude fewer than the competing tests (not sure how many of those characters are pectoral, pelvic and limb characters, though). Nevertheless the large reptile matrix recovered a fully resolved tree nesting Balaur between Aurornis and Archaeopteryx, two taxa that also have a long tail, though both are very much smaller and very much older. That nesting essentially makes Late Cretaceous Balaur a descendant of one of the last — still unknown — pre-birds AND gives Balaur plenty of time to get larger and develop some unique traits.

In the evolution and origin of birds
Aurornis represents a clade that was getting smaller and more gracile that ultimately led to all birds — and all birds have a reduced scythe claw. On the other hand/branch, Balaur represents a just discovered clade that became larger and more robust — and developed a second scythe claw. Even metatarsal 5 is more robust. Balaur was built like a tank. Balaur fuses a long list of bones that otherwise do not fuse in sister taxa, but do occasionally do fuse by convergence in more distantly related theropods.

Figure 2. How T-rex fits within the current taxon list, within the Theropoda. Many other tyrannosauroids are known, but not shown here.

Figure 4. How Baluar fits within the current taxon list, within the Theropoda. Here it nests between Aurornis and Archaeopteryx, flights and pre-bird, nevertheless it did flap its wings based on coracoid length.

Interestingly
when taxa go their own way it is often at the base of an innovative clade.  We’ve seen this before with Atopodentatus, Catorhynchus, Longisquama and Homo.

Figure 5. Balaur (in vertical and horizontal configurations) compared to Haplocheirus and Velociraptor, Aurornis, Archaeopteryx and Gallus.

Figure 5. Balaur (in vertical and horizontal configurations) compared to Haplocheirus and Velociraptor, Aurornis, Archaeopteryx and Gallus.

Cau et al. considered
the sole phalanx of vestigial manual digit 3 to be the fusion of phalanges 1-3. That may be so… OR the distal phalanges might not have been preserved. Either way it makes no difference to the large reptile tree.

Convergent with living birds,
the Balaur anterior sacrum is wide and the pubis of Balaur bows laterally, producing a wide area for the guts between them. This could also be the result of a switch to herbivory (as Cau et al. speculates) and, if so, the twin scythe claws may have been used only for climbing trees. A second scythe-like ungual was not necessary to open the guts of a dinosaur with more efficiency, but a second large claw might have helped a heavier, perhaps less mobile herbivorous Balaur hang more easily on a tree trunk with both medial and lateral digits opposing one another.

Unfortunately,
despite the fact that the manus is larger than the pes in Balaur, alone among all theropod taxa tested in the large reptile tree, Cau et al. considered its forelimbs ‘reduced’  by comparison to the flying birds, Sapeornis and Zhongjiaornis (Fig.1), perhaps due to insularism (living on an island). They suggest that Balaur may have had a proportionally shorter-tail and a less raptorial-looking foot than previously depicted. This suggestion ignores the fact that the tail was not pygostylic and the pes was trenchant, if not raptorial. We’ve seen co-author D. Naish make such hopeful suggestions before, based on a lack of attention to such red flags as that long tail on Balaur. Naish also prefers to shoehorn taxa into existing clades (like pterosaurs into the Ornithodira), rather than allow the tree to recover new clades (like the Tritosauria and Fenestrasauria).

Figure 3. Aurornis pes. Note the relatively large ungual 1, as in Balaur. This taxon represents the smaller,  more gracile lineage leading more directly to birds.

Figure 6. Aurornis pes. Note the relatively large ungual 1, as in Balaur. This taxon represents the smaller, more gracile lineage leading more directly to birds. Although metatarsal 1 is short and placed on the shaft of metatarsal 2, metatarsal 1-3 are aligned, as in Balaur.

No doubt
Balaur was feathered and, with those long, but small, coracoids, it flapped feebly. No doubt it was too large and bulky to fly. It was also a living fossil found in the Latest Cretaceous, representing a node split prior to the Late Jurassic appearances of Archaeopteryx and perhaps Aurornis.

Red Flag
Cau et al. (2015) report, “The sister taxon relationship recovered between Balaur and the short-tailed Sapeornis is quite unexpected. According to that topology, the short pygostyle-bearing tail of Sapeornis evolved independently of the same condition in more crownward birds.” 

I’ll print this addition in red: Cau et al. also report, “The topology that results from our use of the dataset modified from Lee et al. (2014) agrees with most analyses of avialan relationships (e.g., Cau & Arduini, 2008; O’Connor, Chiappe & Bell, 2011; O’Connor et al., 2013;Wang et al., 2014) in depicting a single origin of the pygostylian tail among birds. Here we should note that topological discrepancies and alternative placements of problematic taxa may be influenced by artefacts in coding practice, or by the logical basis of character statement definition followed by different authors (Brazeau, 2011).We therefore consider it likely that some discrepancies between the updated analyses of Brusatte et al. (2014) and Lee et al. (2014)—including the alternative placements of Balaur and Sapeornis among basal avialans—reflect artefacts of coding rather than actual conflict in the data. In conclusion, we consider the consensus among the results of these alternative tests (i.e., Balaur as a non-pygostylian basal avian) as the phylogenetic framework for the discussion on its evolution and palaeoecology.” 

Naish’s note is correct.
I glazed over their conclusion, and now I see why. But that’s not the end of this nesting problem. 

Added Figure 1. The Cau et al tree based on the Brusatte et al. tree. Note the nesting of Balaur among long-tailed post-Archaeopteryx birds, but a sister to Sapeornis, which has a pygostyle. This tree is distinct from added figure 2. Click to enlarge. 

Added Figure 1. The Cau et al tree based on the Brusatte et al. tree. Note the nesting of Balaur among long-tailed (pink) post-Archaeopteryx birds, but a sister to Sapeornis, which has a pygostyle (yellow). This tree is distinct from added figure 2. Click to enlarge.

Added figure 2. The Cau et al. tree based on the Lee et al. tree. Note the nesting of Balaur exactly between the long-tailed theropods and pygostylic, perching (retroverted hallux) birds, distinct from added figure 1.

Added figure 2. The Cau et al. tree based on the Lee et al. tree. Note the nesting of Balaur exactly between the long-tailed (pink) theropods and pygostylic, perching (retroverted hallux, yellow) birds, distinct from added figure 1. An odd nesting, especially considering that Jeholornis and Jixiangornis had an proto-retroverted hallux.

That brings up a whole new topic I also glazed over earlier, the retroverted hallux, which originates with Zhongianornis and Sapeornis in the Cau/Lee cladogram. Shenzhourapator (= Jeholornis) and Jixiangornis demonstrate the expected intermediate morphology for perching.  Balaur, on the other hand, shows no sign of an intermediate or reversed hallux. More basal taxa (Rahonavis, Archaeopteryx, etc.) likewise do not have a reversed hallux, the perching toe.

Cau et al. listed the following traits supporting the placement of Balaur among Avialae. With relatively few traits (none listed below), the large reptile tree nested Balaur just outside of the Avialae (Archaeopteryx). Perhaps the solution to the Balaur problem lies somewhere around this node. Traits that could have arisen as a result of a tree-clinging behavior and the strain on the joints that that produces as size increases are marked with a bullet (•). But a size increase may not have occurred until after the bird split. 

  1. the hypertrophied and proximally placed coracoid tubercle •
  2. the anterior placement of the condyles of the humerus •
  3. the proximally fused carpometacarpus with a laterally shifted semilunate carpal •
  4. the closed intermetacarpal space •
  5. the reduced condyles on metacarpals I–II •
  6. the slender metacarpal III – (vestige)
  7. the reduced phalangeal formula of the third digit – (vestige)
  8. the extensively fused tibiotarsus •
  9. the extensively fused tarsometatarsus •
  10. the distal placement of the articular end of first metatarsal  •
  11. the large size of the hallux • (but it is oriented anteriorly, not reversed)
  12. and the elongation of the penultimate phalanges of the pes  • 
Added figure 3. From Brusatte et al. 2013, the nesting of Balaur far from the birds, within the dromaeosaurs.

Added figure 3. From Brusatte et al. 2013, the nesting of Balaur far from the birds, within the dromaeosaurs.Aurornis is missing here. A later paper by Brusatte et al. 2014, (Fig. 1) changed much of this topology and included Aurornis.

Bottom line:
ArchaeopteryxAurornis, and Balaur were all derived from dromaeosaurids. Balaur appears to represent a hitherto unknown robust clade, distinct from the smaller, more gracile bird line represented by Aurornis and Archaeopteryx. Balaur had a long tail, not a pygostyle. It had forelimbs similar in size relative to the torso, as those of pre-birds, not post-Archaeopteryx birds. The laterally expanded gut indicates a likely switch to herbivory. The second scythe-like claw likely aided tree-clinging. It did not have a perching toe.

In any case, Balaur first appears at the latest Cretaceous with a ghost lineage rolling back to the early Late Jurassic. It certainly could have had much smaller ancestors with a similar list of traits, traits that were retained among later Avialae (birds). That it has several unique traits is only to be expected after so many tens of millions of years of evolution. 

References
Brusatte, et al. 2013. The osteology of Balaur bondoc, an island-dwelling dromaeosaurid (Dinosauria: Theropod) from the Late Cretaceous of Romania. Bulletin of the American Museum of Natural History, 374:1-100.
Brusatte S, Lloyd G,Wang S, Norell M. 2014. Gradual assembly of avian body plan culminated in rapid rates of evolution across the dinosaur–bird transition. Current Biology 24:2386–2392 DOI 10.1016/j.cub.2014.08.034.
Csiki Z, Vremir M, Brusatte SL, Norell MA 2010. An aberrant island-dwelling theropod dinosaur from the Late Cretaceous of Romania. Proceedings of the National Academy of Sciences of the United States of America 107 (35): 15357–15361.
Cau​ A, Brougham​ T and Naish​ D. 2015. The Phylogenetic Affinities of the Bizarre Late Cretaceous Romanian Theropod Balaur bondoc (Dinosauria, Maniraptora): Dromaeosaurid or Flightless Bird? PeerJ3: E1032. DOI: dx.doi.org/10.7717/peerj.1032
Lee MSY, Cau A, Naish D, Dyke GJ. 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds. Science 345(6196):562–566 DOI 10.1126/science.1252243.

EME = (TransylvanianMuseum Society, Dept. of Natural Sciences, Cluj-Napoca, Romania)

Tyrannosaurus rex joins the large reptile tree

Minor bone change made June 16, 2015 on a note sent minutes ago (see below) and June 19, 2015 with the addition of taxa to the Theropoda (Fig. 2).

The most iconic dinosaur,
the hero of Jurassic World, and everyone’s favorite is Tyrannosaurus rex (Fig. 1).

Figure 1. The skull of Tyrannosaurus rex in several views, bones colorized to aid identification and extent. The dorsally expanded parietal shield anchored large neck muscles to hold the giant skull in place and handle the high stresses involved with every skull slam on its dinosaurian prey. It would be great if all paleontologists started illustrating skulls and skeletons with colors as it is so much easier to understand. Many do already.

Figure 1. The skull of Tyrannosaurus rex in several views, bones colorized to aid identification and extent. The dorsally expanded parietal shield anchored large neck muscles to hold the giant skull in place and handle the high stresses involved with every skull slam on its dinosaurian prey. It would be great if all paleontologists started illustrating skulls and skeletons with colors as it is so much easier to understand. Many do already.

As readers know, I have avoided
doing the large well-known dinosaurs in favor of the lesser-known basal dinosauroids like PVL 4597, Trialestes and Herrerasaurus. I wanted to know the evolutionary relationships dinosaurs had with other prehistoric reptiles while others concentrate their efforts on the more popular dinosaurs.

But now and then
you have to add some more popular forms, like T-rex, Gallus the chicken and, on another branch of the large reptile tree, humans (Homo sapiens). Whenever any taxon is added to the large reptile tree, its complete ancestry back to Devonian basal tetrapods can be traced. With that list of intervening taxa, you can see, more or less, the direct lineage of any included taxon (up to 556 at last count). You can see where traits were enlarged or added while others were reduced or eliminated.

Figure 2. How T-rex fits within the current taxon list, within the Theropoda. Many other tyrannosauroids are known, but not shown here.

Figure 2. How T-rex fits within the current taxon list, within the Theropoda. Many other tyrannosauroids are known, but not shown here.

Paleontologists know quite a bit
about the lineage of T-rex. Many of its closest relations are known. The majority of these are not included in the large reptile tree taxon list. So, with this in mind, the closest known sister on the present taxon list is Sinocalliopteryx and both nest on the branch leading to birds.

Did T-rex have feathers?
Earlier I suggested that the evolution of feathers in basal naked dinosaurs was associated with their adoption of a bipedal gait among basal archosaurs. Later larger dinos often developed scales, which quite possibly were derived from primitive feathers, just as chicken leg scales are derived from feathers. The fossil and extant evidence for feathers has its advent with Sinocalliopteryx in the taxon list of the large reptile tree and most taxa that follow also preserve feathers.

The Origin and Evolution of Bird Wings

Earlier we looked at
the evolution of the wing in pterosaurs and in bats. Today we’ll look at the evolution of wings in birds. Other than falsifying/modifying the ‘phase shift’ hypothesis (Wagner and Gauthier 1999), there’s nothing heretical about what you’re going to see and read here. Everyone agrees on the taxon list, phylogenic order and bone identification.

Figure 1. The ancestry of birds illustrated by Haplocheirus, Velociraptor, Aurornis, Archaeopteryx and Gallus.

Figure 1. The ancestry of birds illustrated by Haplocheirus, Velociraptor, Aurornis, Archaeopteryx and Gallus to scale. Click to enlarge. Thanks to Scott Hartman for his Velociraptor, manus flesh outline oddly omitted.

The origin of feathers and wings
in birds has been well documented in hundreds of publications. Here (Figs. 1, 2) all those accounts have been simplified into just two graphics and a little text.

Figure 2. A selection of pre-bird and bird hands/wings including Haplocheirus, Limusaurus, Velociraptor, Archaeopteryx, Anser, Passer and two versions of the Hoatzin , Opisthocomus, adult and juvenile.

Figure 2. A selection of pre-bird and bird hands/wings including Haplocheirus, Limusaurus, Velociraptor, Archaeopteryx, Anser, Passer and two versions of the Hoatzin , Opisthocomus, adult and juvenile. Click to enlarge. Not to scale. Note the medial digit of the outlier, Limusaurus, which is a product of neotony, retained from embryonic tissue recapitulating the seven-finger manus of basal tetrapods (figure 3). Note the return of digit 0 fused to the anterior rim of Anser, Passer and the adult Opisthocomus.

Haplocheirus
had grasping hands and trenchant unguals. The fingers were relatively short. Digit 1 was the most robust. Unlike the more basal theropods, Tawa and Herrerasaurus (Fig. 4, 5), manual digits 4 and 5 were absent in Haplocheirus and kin. Digit 3 was also reduced compared to those basal theropods.

Limusaurus
is very much an outlier, not a transitional taxon, different than other related taxa due to its vestigial size and embryonic development. As noted earlier, the Limusaurus manus retains a vestigial embryonic bud of digit ‘0’ which appears in basalmost tetrapods and many embryos, but not otherwise — unless you accept the hypothesis that the anterior process of metacarpal 1 in many extant birds (Fig. 2) is the return of this digit.

Velociraptor
was smaller overall and had longer fingers and longer metacarpals. Note metacarpal 3 is now subequal to metacarpal 2, but metacarpal 1 remains the most robust. One gets the impression that the fingers in Velociraptor had to be stiffer when they supported feathers. At some point they lost or were losing their ability to flex. At the same time the wrist better able to fold the manus in the plane of the forearm, as birds do.

Aurornis
was smaller overall and also had longer more gracile fingers. There is no bow to metacarpal 3 in Aurornis. This manus can be called a wing here.

Archaeopteryx
was overall smaller, but otherwise quite similar to Aurornis. This manus/wing of Archaeopteryx bore large primary feathers.

Anser
is an extant goose. Metacarpal 1 develops an anterior process where digit ‘0’ appeared on Limusaurus. Metacarpal 3 was bowed. The unguals are much smaller. The proximal metacarpals are fused.

Passer
is an extant sparrow. The phalanges are fused to one another.

Opisthocomus
is the extant hoatzin, which goes through a metamorphosis during growth. Juveniles have claws and adults absorb those while fusing the fingers together.

Wagner and Gauthier (1999)
noted the primitive phalangeal formula for tetrapods goes back to Tulerpeton, (Fig. 3) which they considered, “a synapomorphy that arose in the late Devonian, before the origin of Tetrapoda.” Now paleontologists consider Tulerpeton a tetrapod. The phalangeal formula, of course, has roots in Acanthostega, which has three extra digits, one medially and two laterally. Note: it is the reappearance of the medial digit, digit ‘0’, that is key to the present controversy. Note that Tulerpeton has lost one medial and one lateral digit.

Figure 3. Manus of a bird embryo, and two basal tetrapods, Acanthostega and Tulerpeton, the latter with digits 1-3 colorized like the birds in figure 2. Note the extra medial digit in Acanthostega.

Figure 3. Manus of a bird embryo, and two basal tetrapods, Acanthostega and Tulerpeton, the latter with digits 1-3 colorized like the birds in figure 2. Note the extra medial digit in Acanthostega. This is key to the present controversy. The metapterygial axis runs through the longset finger in basal tetrapods.

Embryology
Wagner and Gauthier (1999) report, “There has long been a dissenting view from the hypothesis that the bird hand is composed of digits DI, DII, and DIII. This position is held chiefly by embryologists who argue that the remaining fingers actually represent DII, DIII, and DIV because the DI and DV were thought to have been lost. Morse (19) observed that, when digital reduction occurs in mammals and lizards, the first digit (DI) is invariably the first to be lost in ontogeny, followed by the fifth (DV), and that a modified version of this pattern applies to the foot of birds as well. Thus, the proposition that ultimately became known as Morse’s Law holds that the three functional fingers remaining in adult birds must be DII, DIII, and DIV.”

That hypothesis assumes that the metapterygial axis continued to produce digit 4. The other option is this:  Evidently there WAS a phase shift, shifting the metapterygial axis from 4 in basal archosaurs to 3 in basal theropods and birds. This is a possibility that was not considered in prior studies. And it makes sense because theropods lose manual digits 3 and 4.

Sometimes paleontology does not occur out in the field,
or in the lab, but between the ears, as a new way of thinking becomes the solution to a vexing problem. (Note: no DGS was involved in this heretical appraisal.)

Figure 3. The source of the phase shift hypothesis, assuming the homology of manual digit 4 as the first digit to appear on the manus of Alligator (above) and Struthio (below).

Figure 3. The source of the phase shift hypothesis, assuming the homology of manual digit 4 as the first digit to appear on the manus of Alligator (above) and Struthio (the Ostrich, below). Clic to enlarge. It is easy to see how the mistake was made. Evidently there WAS a phase shift, shifting the metapterygial axis from 4 in basal archosaurs to 3 in basal theropods and birds. This is a possibility that was not considered in prior studies.

Which manual digit is the longest in in basal theropods?
Distinct from most other theropods, manual digit 3 is the longest in Herrerasaurus (Fig. 4) and Tawa (Fig. 5). So, digit 3 is where the new metapterygial axis is located on theropods and birds. Digits 4 and 5 are tiny and tinier vestiges, completely lost in later theropods and birds. It doesn’t make sense that the metapterygial axis should produce a vestige – or no digit at all! Rather, it is the metapterygial axis that has shifted one digit medially. That’s the new heretical phase shift promoted here.

A new nose for Herrerasaurus

Figure 4. Herrerasaurus. The manus has three functional fingers. The two lateral fingers are vestiges.

 

Figure x. The basal theropod, Tawa, with its long manual digit 3. This is where the metapterygial axis has shifted.

Figure 5. The basal theropod, Tawa, with its long manual digit 3. This is where the metapterygial axis has shifted.

Wagner and Gauthier (1999)
also point to the example of the Kiwi manus, some of which have only one finger and two metacarpals. One of these examples had one less phalanx than the other. IMHO you should use fully functioning examples, real wings and real hands, not tiny useless vestiges that are taking various fast tracks toward reduction and disappearance. Wagner and Gauthier also placed the phase shift between Torvosaurus and Allosaurus on their cladogram. That’s an odd place to put a major transition: between two giants. I put the new phase shift at the very base of the Dinosauria, just prior to Herrerasaurus and the basal phytodinosaur, Eoraptor, which also has vestigial lateral fingers.

Wagner and Gauthier (1999) also report,
“We are not aware of any other case in which such a conflict between a developmental and a functional constraint in digit reduction existed.” That’s true. And there is no such conflict in birds if one accepts the novel hypothesis that the metapterygial axis shifted medially as the lateral digits became useless vestiges.

The deeper you get into evolution, the more it all comes together…

References
Müller GB and Alberch P 1990. Journal of Morphology 203, 151–164.
Wagner GP and Gauthier JA 1999. 1,2,3 = 2,3,4: A solution to the problem of the homology of the digits in the avian hand. Proceedings of the National Academy of Science 96:5111-5116.

Evolution of dinosaur epidermal structures

Barrett, Evans and Campione (2015)
“find no compelling evidence for the appearance of protofeathers in the dinosaur common ancestor and scales are usually recovered as the plesiomorphic state, but results are sensitive to the outgroup condition in pterosaurs. Rare occurrences of ornithischian filamentous integument might represent independent acquisitions of novel epidermal structures that are not homologous with theropod feathers.”

Unfortunately
the Barrett team followed two false traditions with regard to pterosaurs, which gained their epidermal structures independent from dinos. The two clades are not related according to the large reptile tree which nests pterosaurs in a new clade of lepidosaurs.

Based on their false assumption of scaly pterosaurs
as an outgroup, their analysis recovered primitively scaled Dinosauria and Ornithischia. So we’re off to a bad start based on taxon exclusion and false inclusion. Scales have never been found on pterosaurs. Why didn’t they assume filamented pterosaurs? We have evidence for that. So there is a lack of logic here that would have changed their conclusion.

The actual outgroup
for dinosaurs is the Crocodylomorpha for which tiny back scales first appear on the lower back of tiny Scleromochlus and ultimately cover the entire dermal surface on large extinct and extant taxa. Tiny scales may have been present on basal dinos, but more likely they had naked skin, like birds without their feathers. Scales on bird feet are transformed feathers.

The Barrett team database
included 24 ornithischians, 6 sauropods and 40 theropods (including Mesozoic birds). All taxa were scored for the presence/absence of epidermal scales, unbranched filaments (protofeathers)/quills and more complex branched filaments (including feathers).

The Barrett team report,
“Additional examples of protofeathers would be required from early dinosaur lineages or non-dinosaurian dinosauromorphs to optimize this feature to the base of Dinosauria. In particular, the ancestral condition in pterosaurs is pivotal in this regard, but currently unknown.” Longtime readers know this is false based on a cladogram, the large reptile tree) that includes several hundred more taxa.

As noted above, scales are unknown in pterosaurs.
However, their known outgroup taxa, Longisquama, SharovipteryxCosesaurus and Macrocnemus all have scales. The former three also have ptero-hairs (pycnofibers) and are the only Triassic fenestrasaurs (including pterosaurs) known to have these epidermal structures.

Based on their appearance and location,
dinoaurian ‘quills’ appear to be hyper elongated primordia without branching.

The Barrett team concluded,
“It seems most likely that scaly skin, unadorned by feathers or their precursors, was primitive for Dinosauria and retained in the majority of ornithischians, all sauropodomorphs and some early-diverging theropods (filaments are thus far unknown in ceratosaurians, abelisaurids and allosauroids.” In Science “it seems most likely” is a very weak argument, further weakened by the fact that birds don’t have scales, except on their legs, and those are transformed feathers.

The Barrett team provided a cladogram
that depicted the extent to which scales, filaments and feathers were present. Notably they did not also include the extent of naked skin, which is a fourth possibility not covered by the text or graphic. The possibility exists that all dinosaur scales are transformed primordia (filaments) or transformed feathers. Dinosaur scales could also be novel epidermal structures that appear only on large dinosaurs just as croc scales are novel epidermal structures. Based on their appearance and location, dinoaurian ‘quills’ appear to be hyper elongated primordia.

Embryo birds
first develop primordial feathers in the middle of their backs, replaying phylogeny during ontogeny. With current data, that trait may go all the way back to basal archosaurs, like Scleromochlus.

Bottom line:
When you play with phylogenetic bracketing, you have to have a valid cladogram.

References
Barrett PM, Evans DC, Campione NE 2015. Evolution of dinosaur epidermal structures. Biol. Lett. 11: 20150229. online

 

 

 

 

 

 

 

Paleo Irony: Rhetoric vs. Reality on Birds (+ Pterosaurs, while we’re at it)

A new paper
by Smith et al. (2015) cements the relationship of birds with mairaptoran theropod dinosaurs (a nesting confirmed by the large reptile tree.) It was inspired by recent papers attempting to distance birds from theropod dinosaurs by Alan Feduccia and the late Stephen Czerkas (links below).

From the Smith et al. abstract: “Birds are maniraptoran theropod dinosaurs. The evidence supporting the systematic position of Avialae as a derived clade within Dinosauria is  voluminous and derived from multiple independent lines of evidence. In contrast, a paucity of selectively chosen data weakly support, at best, alternative proposals regarding the origin of birds and feathers. Opponents of the theory that birds are dinosaurs have frequently based their criticisms on unorthodox interpretations of paleontological data and misrepresentation of phylogenetic systematic methods. Moreover, arguments against the nested position of Avialae in Dinosauria have often conflated the logically distinct questions of avian origins, the evolution of flight, and the phylogenetic distribution of feathers. Motivated by a Perspectives article with numerous factual inaccuracies that recently appeared in The Auk, we provide a review of the full complement of facts pertaining to the avian origins debate and address the misplaced criticisms raised in that opinion paper.”

All you have to do is substitute
‘pterosaurs’ for ‘birds’ in the abstract and the rest follows in perfect irony:

Pterosaurs are fenestrasaur tritosaur lepidosaurs. The evidence supporting the systematic position of Pterosauria as a derived clade within Fenestrasauria is  voluminous and derived from multiple independent lines of evidence (fenestrasaurs are not necessary to nest pterosaurs within tritosaur lepidosaurs). In contrast, a paucity of selectively chosen data weakly support, at best, alternative proposals regarding the origin of pterosaurs as archosaurs. Opponents of the theory that pterosaurs are fenestrasaurs have frequently based their cladograms on taxon exclusion and misrepresentation of scoring data. Moreover, arguments against the nested position of Pterosauria in Fenestrasauria/Tritosauria/Lepidosauria have often conflated the logically distinct questions of pterosaur origins, the evolution of flight, and the phylogenetic distribution of patagial and other membranes. Motivated by a Sues and Nesbitt (2013) paper based on a Nesbitt (2011) cladogram with numerous scoring inaccuracies and taxon exclusion that has been a traditional fault, I provide a review of the full complement of facts pertaining to the pterosaur origins debate and address the misplaced criticisms raised in a Hone and Benton (2007, 2008) paper.

See ReptileEvolution.com and various topics within PterosaurHeresies.Wordpress.com for text and figures.

See here and here for Nesbitt 2011 issues and here for Hone and Benton issues.

And while you’re at it
you can look up alternative nestings for Vancleavea, Casea, Mesosaurus, turtles, synapsids, tiny pterosaurs, Eudibamus, Cartorhynchus, Gephyrostegus, etc. etc.

Isn’t it ironic
that the paleontologists who support an archosaur relationship won’t even look at a lepidosaur relationship? And they reject papers that do present a lepidosaur relationship because such a nesting is heterodox (= different). AND they continue to promote the hypothesis that pterosaurs evolved “without obvious antecedent” with purported sisters that don’t look anything like pterosaurs.

We need
a generally accepted large scale umbrella study of the Reptilia (= Amniota) in order to proceed with smaller more focused studies with greater confidence and to repair old issues. In fact, such a study should also quiet the opposition from Dr. Feduccia on the bird/theropod issue.

References
Smith NA, Chiappe LM, Clarke JA, Edwards SV, Nesbitt SJ, Norell MA, Stidham TA, Turner A, van Tuinen M,  Vinther J and Xu X 2015. Rhetoric vs. reality: A commentary on “Bird Origins Anew” by A. Feduccia. The Auk 132(2): 467-480

doi: http://dx.doi.org/10.1642/AUK-14-203.1
http://www.bioone.org/doi/abs/10.1642/AUK-14-203.1

Secondary sexual behavior in Longisquama (and Cosesaurus)

Sure Longisquama had giant plumes
that likely entranced the lay-dees… and/or the gents…

But as the proximal outgroup to the Pterosauria,
and provided with a similar pectoral girdle (sternal complex, strap-like scapulae, quadrant-shaped coracoids, it was a likely flapper, as we talked about earlier here with similar traits in Cosesaurus (Fig. 1)

Figure 1. Cosesaurus flapping - fast. There should be a difference in the two speeds. If not, apologies. Also, there should be some bounce in the tail and neck, but that would involve more effort and physics.

Figure 1. Click to enlarge and animate. Cosesaurus flapping.

Here (Fig. 2) is an animated Longisquama, flapping and with tail wags, which we talked about earlier here.

Figure 2. Click to animate. Longisquama flapping and wagging its tail.

Figure 2. Click to animate. Longisquama flapping and wagging its tail.

With these traits and behaviors basal fenestrasaurs converged with theropods ancestral to birds. In these ways flapping preceded powered flight, in both cases co-opted from secondary sexual behaviors in these highly visual reptiles.

Bird stem evolved faster than other theropods

Figure 1. The evolution of birds as a consequence of miniaturization. Artist: Davide-Bonnadonna

Figure 1. The evolution of birds as a consequence of miniaturization. Artist: Davide-Bonnadonna. I think the last taxon on the right has been enlarged somewhat for clarity. See Figure 2. 

A new paper by Lee et al. (2014)
reported on their phylogenetic analysis of theropods employing 1549 characters. They found two drivers underlying the dinosaur-bird transition: 1) sustained miniaturization; and 2) the evolution of skeletal adaptations 4x faster than other dinosaurs.

They found that miniaturization facilitated the evolution of morphological novelties associated with small size: reorientation of the body mass; 2) increased aerial ability; and 3) paedomorphic skulls with enlarged eyes and brains along with a reduced snout and smaller teeth without serrations.

I heartily endorse this work.
It supports a paradigm that miniaturization that produces new clades. Cope’s Rule generally does not. We see similar miniaturization at the genesis of reptiles, amphibians, therapsids, mammals, dinosaurs, crocodylomorphs (together the archosaurs), pterosaurs, diapsids and several clades within each of these, like bats and pterodactyloid-grade pterosaurs. We knew for a long time that sustained miniaturization also produced birds. So that’s not news. It just has never been so well laid out before.

Figure 2. Sinocalliopteryx along with Aurornis and Archaeopteryx to scale. This illustration produced over a year ago, tells the same tale as the new Lee et al. paper, but without the great supporting details.

Figure 2. Sinocalliopteryx along with Aurornis and Archaeopteryx to scale. This illustration produced over a year ago, tells the same tale as the new Lee et al. paper, but without the great supporting details.

Lee et al. conclude: 
“Because size reduction, feather elaboration, paedomorphism, and other anatomical novelties permitted by small size all evolved in concert along the bird stem, identifying the primary driver of this sustained trend is probably impossible. It is likely that all traits influenced and provided the context for the evolution of others.” 

Actually not so impossible.
The authors make no mention of the fact that smaller taxa generally mature more quickly, breed more often and die sooner. In other words, generational turnover happens more quickly in smaller taxa, as everyone know. The rate of evolution over time is accelerated by the rate of reproduction over time (all other things being equal). That’s the primary driver. 

In the family tree of amniotes,
you see this all the time, not just in bird origins. Good to see this get the press it deserves.

References
Lee MSY, Cau A, Naish D and Dyke GJ 2014. Sustained miniaturization and anatomical innovation in the dinosaurian ancestors of birds.