Triassic origin of scales, scutes, hair, etc. as biting fly barriers?

During the Middle to Late Triassic

  1. Mammals developed fur/hair.
  2. Aetosaurs developed plates and horns beyond the earlier paired dorsal scutes.
  3. Crocodylomorphs developed large scales beyond the earlier paired dorsal scutes.
  4. Dinosaurs lost those paired scutes and developed placodes and quills. Ultimately these became scales and feathers.
  5. Turtles developed hard scales over a carapace and plastron.
  6. Lepidosaurs developed small scales.
  7. Pterosaurs and their Late Triassic sisters developed pycnofibers

All of these developed on the soft, naked skin
(think of a plucked chicken) that was a universal covering for Carboniferous and Permian tetrapods (Early forms retained large ventral scales inherited from finned ancestors, but these were lost by the Permian).

All of these extradermal structures have one thing in common.
They separated and/or protected the animal’s naked skin from the environment, one way or another. They developed by convergence. Dhouailly 2009 and other workers discussed the chemical similarities of the keratin found in these dermal structures. 

The question is:
What was different about the Triassic environment that was not present in earlier Carboniferous and Permian environments? We can 
eliminate heat, cold, UV rays, rain, aridity, etc. as possible reasons for the development of insulator structures because those factors had always been present. So what was new in the Triassic that affected all terrestrial tetrapods?

Flies and their biting, piercing kin.
“The earliest definitive flies known from the mid-Triassic of France, approximately 230 Ma (Krzemiski and Krzeminska, 2003)” according to Blagoderov, Grimaldi and Fraser 2007. The order Diptera (flies, mosquitos and kin) tend to land on large tetrapods for food, blood, etc. Scales, scutes, hair, feathers, etc. all separate flying insects from the naked skin of Triassic terrestrial tetrapods. Williams et al. 2006 even found mosquito repellents in frog skin. It is notable that, except for armored placodonts and mosasaurus (derived varanid lepidosaurs), aquatic and marine tetrapods also had naked skin with the thalattosaur, Vancleavea, a notable sermi-terrestrial exception. Is that because they had aquatic antecedents in the Triassic that were never affected by flying insects?

It’s not just the insect bite that drives this evolution,
it’s the appearance of new vectors for the rapid spread of disease that drives this evolution.

Interesting coincidence.
If this is not the case, this will take further study.

Figure 1. Lacertulus, a basal squamate from the Late Permian

Figure 1. Lacertulus, a basal squamate from the Late Permian

Carroll and Thompson 1982 report
on the Late Permian lepidosaur, Lacertulus (Fig. 1), “No scales dermal or epidermal are evident in the specimen.”

From the Dhouailly 2009 abstract:
“I suggest that the alpha-keratinized hairs from living synapsids may have evolved from the hypothetical glandular integument of the first amniotes, which may have presented similarities with common day terrestrial amphibians.

Concerning feathers, they may have evolved independently of squamate scales, each originating from the hypothetical roughened beta-keratinized integument of the first sauropsids. The avian overlapping scales, which cover the feet in some bird species, may have developed later in evolution, being secondarily derived from feathers.” Not realized by Dhouailly, the purported clade ‘Sauropsida’ is paraphyletic and a junior synonym for Amniota and Reptilia in the LRT.

Earlier we looked at the first appearances
of hair, quills, pycnofibers and hard scales in a three-part series here, here and here

Exceptionally, humans are terrestrial tetrapods
that have lost most of their hair, more or less returning to the primitive naked state. And yes, flies and mosquitos do bother humans. It is the price we pay for the benefits of naked skin. Clothing helps provide a barrier.

Remember:
Just because an idea is proposed and a hypothesis is advanced doesn’t make it so. In science ideas have to be confirmed or refuted following their first appearance. If anyone has data concerning scales or other dermal structures in Carboniferous or Permian taxa, please make us aware of those.

References
Blagoderov V, Grimaldi D and Fraser NC 2007. How Time Flies for Flies: Diverse Diptera from the Triassic of Virginia and Early Radiation of the Order. American Museum Novitates 3572:1-39. DOI: 10.1206/0003-0082(2007)509[1:HTFFFD]2.0.CO;2
Carroll RL and Thompson P 1982.
A bipedal lizardlike reptile from the Karroo. Journal of Palaeontology 56:1-10.
Dhouailly D 2009.
A new scenario for the evolutionary origin of hair, feather, and avian scales Journal of Anatomy 214(4): 587–606. doi: 10.1111/j.1469-7580.2008.01041.x
Krzeminnski, W., and E. Krzeminska. 2003. Triassic Diptera: descriptions, revisions and phylogenetic relations. Acta Zoologica Cracoviensia (suppl.) 46: 153–184.
Maderson PFA and Alibardi L 2000.
The Development of the Sauropsid Integument: A Contribution to the Problem of the Origin and Evolution of Feathers. American Zoologist 40:513–529.
Rohdendorf BB, Oldroyd H and Ball GE 1974. The Historical Development of Diptera. The University of Alberta Press, Edmonton, Canada. ISBN 0-88864-003-X.
Williams CR, Smith BPC, Best SM and Tyler MJ 2006.
Mosquito repellents in frog skin. Biol Lett. 2006 Jun 22; 2(2): 242–245. doi: 10.1098/rsbl.2006.0448

Patterns in T-rex scales

The big news last night
was all about the scale patches found on a T-rex skeleton (Bell et a. 2017). This one (Fig. 1) is from the dorsal neck. It may or may not be from the midline.

Figure 1. GIF animation, 3 rounds, about 24 frames adding possible pattern overlays to the patch.

Figure 1. GIF animation, 3 rounds, about 24 frames adding possible pattern overlays to the patch. Photo from Bell et al. 2017. If this scale patch evolved from feathers only the visible branching pattern is similar. Distinct from feathers, each scale has its own base in the epidermis. The largest of these scales are each slightly longer than a centimeter in length.

The paper focused on
various aspects of theropod integument, chronicling taxa with feathers and others with scales along with the origin of scales from feathers in certain theropods. The paper also nested feathered Yutyrannus basal to tyrannosaurs. In contrast, the large reptile tree (LRT) nests feathered and winged Zhenyuanlong  basal to tyrannosaurs, Yutyrannus closer to Allosaurus.

Here
(Fig. 1) I applied colors to apparent patterns in the scale patch. Not sure what they mean. Overall this patch reminds me of a town with one main street, several side streets and dozens of single resident plots, each a little more than 1 cm on a side. Each scale has its own base in the epidermis. Were they derived from feathers? The scales provide no clue to that origin. The medial symmetry shown here may be a result of this patch lying on the midline (sagittal plane).

References
Bell et al. (6 other authors) 2017. Tyrannosaurid integument reveals conflicting patterns of gigantism and feather evolution. Biology Letters 13: 20170092. http://dx.doi.org/10.1098/rsbl.2017.0092

Saltopus preserves early archosaur skin and scales

Basal Crocodylomorpha

Figure 1. Basal Crocodylomorpha, including Gracilisuchus, Saltopus, Scleromochlus and Terrestrisuchus

The basal archosaur
(crocs + dinos) Saltopus (von Huene 1910; Late Triassic; ~210 mya, ±60 cm long; Figs. 1–3) poorly preserves bones, but also preserves some scaly skin.

Figure 2. Saltopus skin and scales surrounding the right pelvis.

Figure 2. Saltopus skin and scales surrounding the right pelvis. Not all bones nor all scales are traced here. Benton and Walker 2011 reported no evidence for osteoderms. The bones are hard to delineate and segregate from scales because here they are covered with fossilized desiccated skin. Photo from Benton and Walker 2011 who trace the femoral head extending beneath the pelvis. 

Saltopus nests well within
the Crocodylomorpha and, along with Scleromochlus (Fig. 1), present examples of basal archosaur skin and scales. Even more basal, Gracilisuchus (Fig. 1) had dorsal scutes derived from ancestors going back to the Early Triassic Euparkeria.

Figure 2. Saltopus pelvis latex peel from Benton and Walker 2011. They found two large sacrals. Using DGS I found four sacrals, the same length as the dorsals and causals. Sister taxa have four sacrals.

Figure 2. Saltopus pelvis latex peel from Benton and Walker 2011. They found two large sacrals. Using DGS I found four sacrals, the same length as the dorsals and causals. Sister taxa have four sacrals.

Gracilisuchus and basal dinosaurs
had only two sacral vertebrae, but basal bipedal crocs, like Scleromochlus, double that number. Benton and Walker 2011 traced two sacrals in a latex cast of the sacral area, but each sacral was twice as long as proximal dorsals and causals. Here four sacrals are tentatively identified in the latex peel, all about as long as proximal non-sacral vertebrae.

Dinosaur skin
can be scaly, or naked with feathers, or a combination of the two. Dinosaur scales may be different than croc or lizard scales in that at least some dinosaur scales, like those on the metatarsus of theropods appear to be derived from former feathers.

References
Benton MJ and Walker AD 2011. Saltopus, a dinosauriform from the Upper Triassic of Scotland. Earth and Environmental Science Transactions of the Royal Society of Edinburgh: 101 (Special Issue 3-4):285-299. DOI:10.1017/S1755691011020081
von Huene FR 1910. Ein primitiver Dinosaurier aus der mittleren Trias von Elgin. Geol. Pal. Abh. n. s., 8:315-322.

wiki/Saltopus

When fish scales evolved into reptile scales

Figure 1. Tulerpeton parts from Lebedev and Coates 1995 here colorized and newly reconstructed. Note the well-preserved scales, studied in detail by Mondéjar-Fernandez et al. 2014.

Figure 1. Tulerpeton parts from Lebedev and Coates 1995 here colorized and newly reconstructed. Note the well-preserved scales, studied in detail by Mondéjar-Fernandez et al. 2014.

The scales of Tulerpeton
were made of compact bone lacking enamel, dentine and isopedine layers found in more basal sarcopterygians (Mondéjar-Fernandez et al. 2014). This was the first step in a process that ultimately also removed bone from scales leaving only keratin scales arising from the epidermis.

Several times later
bone reappeared in the dermis producing osteoderms.

Earlier the Devonian tetrapod Tulerpeton heretically nested as the oldest known of the basalmost amniotes, the last common ancestors of all living reptiles, birds and mammals.

References
Mondéjar-Fernandez J, Clément G and Sanchez S 2014. New insights into the scales of the Devonian tetrapods Tulerpeton curtum Lebedeve, 1984. Journal of Vertebrate Paleontology 34:1454-1459.

wiki/Tulerpeton

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

 

 

 

 

 

 

 

The origin of feathers and hair (part 1: skin and scales)

Three clades
developed extra dermal hair-like structures: mammals, dinosaurs (reaching an acme in birds) and pterosaurs. Traditional thinking holds that reptile scales evolved early, along with the origin of the amniotic membrane. Both of these were viewed as adaptations to a non-aquatic, (i.e. ‘dry’) environment. Unfortunately there’s very little evidence for scales in the earliest reptiles (see below). They appear to have lived in a moist coal forest leaf litter environment throughout the Carboniferous.

Basal amniotes
Dhouailly 2009 reports: “The common ancestor of amniotes may have presented both a glandular and a ‘granulated integument’, i.e. an epidermis adorned with a variety of alpha-keratinized bumps, and thus may have presented similarities with the integument of common day terrestrial amphibians. Whereas the glandular quality of the integument was retained and diversified in the mammalian lineage, it was almost completely lost in the sauropsid lineage (non-mammalian amniotes). When the amniote ancestors started to live exclusively on land in the late Carboniferous, they derived from a group of basal
amphibiotic tetrapods, and it is plausible that they evolved a skin barrier similar to that of modern toads to prevent desiccation”

Two dermal proteins
are key to discussions on reptile skin: alpa-keratins and beta-keratins.

Alpha-keratins
Dhouailly 2009 reports: “In all living vertebrates, at least from trout to human, specific types of alpha-keratins characterize the epidermis and corneal epithelium showing a strong homology in the different lineages.In all amniotes, the last supra-basal layers of the epidermis are cornified, meaning they are formed of dead cells filled entirely with alpha-keratin filaments coated with specific amorphous proteins and lipids, providing a barrier to water loss.”

Beta-keratins
Dhouailly 2009 reports: “Only the sauropsids (birds and reptiles) possess an additional capacity for beta-keratin synthesis, an entirely different type of intermediate filament, which appears to result from a phylogenetic innovation that occurred after that of the alpha-keratins.”

Perhaps a correction here: In the large reptile tree there is no clade “Sauropsida.” Rather synapsids are more derived than the basal reptiles that ultimately evolved into the other amniotes. So, if beta-keratins had a single origin, mammals and perhaps their closest ancestors lost the capacity to produce beta-keratins. Phylogenetic bracketing indicates this could have happened at any node between Protorothyris and Megazostrodon.

Scales
When did scales arise? And are lizard scales homologous with those of turtles, crocs, birds, pangolins and opossum tails? Unfortunately fossils of skin and scales are rare.

Carroll and Baird 1972
traced long interwoven ventral ‘scales’ for the basal lepidsosauromorph, Cephalerpeton,  similar to those found in basal amniotes like Gephyrostregus watsoni. Carroll and Baird also report, “The skin impressions along the forelimb [of Cephalerpepton] have a slightly pebbly texture—rougher than the limb bones but smoother than the broken surface of the matrix. There is no evidence of discrete scales. An indication of epidermal scales would be expected in this type of preservation, if they were present in the animal.epidermal scales can only be recorded as impressions and this type of preservation is rare and apparently not reported in other Paleozoic reptiles.”

As you’ll recall, reptiles divide at the start into two lineages, the Lepidosauromorpha and the Archosauromorpha.

Lepidosauromorphs 
The most primitive appearance of dermal tissue in the lepidosaurorph line occurs with the scutes of pareiasaurs, Sclerosaurus and basal turtles. These include a bony base. At some point turtles developed scales that covered the face and limbs, but when is not known. My guess is as far back as Stephanospondylus because it was a large and tasty herbivore.

Otherwise nothing on scales appears until  Xianglong, a gliding basal lepidosaurifom (not a squamate). Li et al. 2007 report, “The entire body including the skull is covered with small granular scales, which show little size variation.” Perhaps noteworthy, this is the node at which some short-legged, ground-dwelling flattened owenettids evolved to became large-limbed and arboreal, exposed to the dry air above the damp leaf litter.

Perhaps more misunderstood, those wing spars are actually ossified dermal extensions, as in a sister taxon, Coelurosauravus, not extended ribs, as we carefully considered earlier here and here.

Figure 1. Xianglong, a basal lepidosauriform with dermal extensions, not ribs, with which it used to glide.

Figure 1. Xianglong, a basal lepidosauriform with dermal extensions, not ribs, with which it used to glide.

Then there’s Sphenodon, an extant basal lepidosaur with a variety of large and small scales, some were overlapping and others were not. Basalmost sphenodontids, like Pleurosaurus, were trending toward an aquatic niche. Sphenodon is a burrowing and foraging reptile. the best clue to basal sphenodontid squamation comes from a tritosaur sister, Tijubina (see below).

Of course, all living lizards (squamates) have scales.
and they shed their skin in whole or in patches during ontogeny.

The tritosaur lepidosaurs are a special case,
The basal tritosaur, Tijubina, preserves rhomboid scales on the neck, large rhomboid scales on the trunk and annulated ones on the ventral side of the entire caudal region. Not far removed from Sphenodon with regard to squamation.

By contrast, a more derived tritosaur, Huehuecuetzpalli preserves tiny disassociated calcified granular scales over its dorsal neural arches. A more derived tritosaur, Macrocnemus (Renesto and Avanzini 2002), had a scale covering in the sacral and proximal caudal region.

Now things get more than interesting…
The scales of Cosesaurus (Ellenberger and DeVillalta 1974, Fig. 2) were about the size of the matrix particles in its mold, so they have not been described. However, Cosesaurus had extra dermal tissues in the form of a gular sac, a dorsal frill, fibers streaming from the posterior arm, uropatagia trailing the hind limbs and long hairs emanating from the tail. A larger sister, Kyrgyzsaurus had scales and similar extra dermal ornaments. Sharovipteryx shares these traits and accentuates the uropatagia. Longisquama shares these also but accentuates the dorsal plumes. The latter two taxa also have pycnofibers (hairs) at least surrounding the cervical series. Their sisters, the pterosaurs, accentuate the trailing arm fibers, which become fiber-embedded foldable wings. Pterosaur ‘hair’ reaches its acme in Jeholopterus, which may have used its ‘hair ball’ as a barrier to insects likewise attracted bloody patches of dinosaur skin. In certain basal pterosaurs the tail hairs coalesce to become tail vanes.

Figure 1. Click to enlarge. The origin and evolution of Longisquama's "feathers" - actually just an elaboration of the same dorsal frill found in Sphenodon, Iguana and Basiliscus. Here the origin can be found in the basal tritosaur squamate, Huehuecuetzpalli and becomes more elaborate in Cosesaurus and Longisquama.

Figure 2. Click to enlarge. The origin and evolution of Longisquama’s “feathers” – actually just an elaboration of the same dorsal frill found in Sphenodon, Iguana and Basiliscus. Here the origin can be found in the basal tritosaur squamate, Huehuecuetzpalli and becomes more elaborate in Cosesaurus and Longisquama.

It is clear in fenestrasaurs that extra dermal membranes were secondary sexual traits, decorations that enhanced their chances for mating. Hairs ultimately became barriers or acted as insulation. Arm fibers ultimately became wings.

Archosauromorphs
Like the basal lepidosauromorph, Cephalerpeton, basal archosauromorphs like Eldeceeon  had ossified belly scales in V-shaped patterns, but not coalesced to form gastralia.

According to Carroll and Baird (1972) in Brouffia, “many ventral scales are present in the blocks. They are quite broad, rather than being narrowly wheat-shaped, as has been considered typical in early reptiles. A faint impression of dorsal scales is evident also, but these are too insubstantial to illustrate.”

Pelycosaurs lacked scales. They were naked. So were basal therapsids as far as the fossil record goes. Estemmenosuchus (Chudinov 1970), an herbivorous therapsid, preserves no scales, hair or hair follicles. However, the preserved skin was well supplied with glands.

Since all living basal mammals (Fig. 3) are richly endowed with fur, that trait probably extends to the first tiny egg-laying mammals, denizens of the leaf litter. In tiny animals, so in contact with the substrate, the leaf litter and water, hair appears to have developed not only to insulate its little warm-blooded body, but also to act as a barrier to all dermal contact with the environment. Insects, like fleas, had to lose their wings to burrow past the hair to get to the skin.

Figure 2. This is Amphitherium a basal mammal.

Figure 3. This is Amphitherium a basal mammal.

In basal diapsids, the sisters of basal synapsids no dermal material has been found.

Plesiosaurs and ichthyosaurs were naked, so pachylpleurosaurs, thalattosaurs and mesosaurs were likely naked as well. A rare exceptions, the thalattosaur Vancleavea, was covered with large bony scales. Hupehsuchids had short bony plates over the neural spine tips.

For protorosaurs or proterosuchids no dermal scales have been reported.  Dorsal armor developed as large plates in the likely piscivore Doswellia, and to a less degree in Champsosaurus, Diandongosuchus, and then again to a greater degree in parasuchids, proterochampsids and chanaresuchids.

For euarchosauriformes a line of dorsal scutes also appeared on the dorsal midline of Euparkeria and many descendant taxa (except finbacks and poposaurs). The herbivorous Aeotosaurs,  Revueltosaurus and Simosuchus independently expanded their armor in similar ways. So did the carnivorous extant alligators and crocodiles and their ancestors. However basal bipedal and near-bipedal croc taxa, like Gracilisuchus do not preserve scales, other than their dorsal scutes. These may have enhanced the strength of the backbone. Otherwise, basal bipedal crocs were likely not heavily scaled, and neither were the oceanic swimmers, like Metriorhynchus.

That brings us to dinosaurs.
Kaplan (2013) reports “the overwhelming majority had scales or armor.” We’ll cover dinosaur scales and dinosaur feathers in more detail in part 3: feathers.

References
Kaplan M 2013. Feathers were the exemption rather than the rule for dinosaurs. Nature News. doi:10.1038/nature.2013.14379
Renesto S and Avanzini M 2002. Skin remains in a juvenile Macrocnemus bassanii Nopsca (Reptilia, Prolacertiformes) from the Middle Triassic of Northern Italy. Jahrbuch Geologie und Paläontologie, Abhandlung 224(1):31-48.
Carroll RL and Baird D 1972. Carboniferous Stem-Reptiles of the Family Romeriidae. Bulletin of the Museum of Comparative Zoology 143(5):321-363. online pdf
Bennett AF and Ruben JA 1986. The metabolic thermoregulatory status of therapsids. In The Ecology and Biology of Mammal-like reptiles (Hottom, Roth and Roth eds) 207-218. Smithsonian Institution Press, Washington DC
Chudinov PK 1970. Skin covering of therapsids [in Russian] In: Data on the evolution of terrestrial vertebrates (Flerov ed.) pp.45-50 Moscow: Nauka.
Dhouailly D 2009. A new scenario for the evolutionary origin of hair, feather, and avian scales. Journal of Anatomy 214:587-606.
Lecuona A and Desojo, JB 2011. Hind limb osteology of Gracilisuchus stipanicicorum(Archosauria: Pseudosuchia). Earth and Environmental Science Transactions of the Royal Society of Edinburgh 102 (2): 105–128.
Persons WC4 and Currie PF 2015. Bristles before down: A new perspective on the functional origin of feathers.Evolution (advance online publication)
DOI: 10.1111/evo.12634
http://onlinelibrary.wiley.com/doi/10.1111/evo.12634/abstract

* too bad I did not know this when I painted Estemmenosuchus with scales for the cover of a book.