The origin of feathers and hair (part 3: feathers)

Yesterday, in part 2, we looked at the origin of mammal hair. The day before, in part 1, we looked at scales and skin. Today, in part 3, we’ll look at the origin of dinosaur scales and feathers with a concentration on their lumbar zones, as you’ll see.

Figure 1. The origin of dinosaurs to scale. Gray arrows show the direction of evolution. This image includes Decuriasuchus, Turfanosuchus, Gracilisuchus, Lewisuchus, Pseudhesperosuchus, Trialestes, Herrerasaurus, Tawa and Eoraptor.

Figure 1a. The origin of dinosaurs to scale. Gray arrows show more derived taxa. This image includes Decuriasuchus, Turfanosuchus, Gracilisuchus, Lewisuchus, Pseudhesperosuchus, Trialestes, Herrerasaurus, Tawa and Eoraptor. We don’t know if these taxa were scaly or naked, but basal taxa did have a line of dorsal scutes over the dorsal vertebrae, which is shorter in obligate bipeds.

Figure 1. Scales on the back of Scleromochlus, a basal bipedal croc and thus a distant sister to basal bipedal dinosaurs.

Figure 1. Scales on the back of Scleromochlus, a basal bipedal croc close to the base of all archosaurs and thus a distant sister to basal bipedal dinosaurs. No primordial feathers or scutes here.Was the rest of it naked? We don’t know…

First: phylogeny
Pseudhesperosuchus (Fig. 1a) is the last taxon in the lineage of Euparkeria to Herrerasaurus to retain dorsal scutes, the only dermal structures known for those fossils. ‘No scales’ might mean no scales were preserved. It could also mean the skin was naked. The latter is the scenario based on phylogenetic bracketing between pelycosaurs and chickens (get pdf of dermal tree here). But scales arise often within the Reptilia and a new origin cannot be discounted as it occurs in several marine clades, aetosaurs and Revueltosaurus.

No poposaurs have scutes. No basal dinosaurs have scutes — but Herrerasaurus had spine tables (perhaps vestiges of dorsal scutes fused to dorsal verts?).

When last we left dinosaurs,
they were just evolving from sisters to Gracilisuchus, Lewisuchus, Saltoposuchus, Pseudhesperosuchus, the PVL 4597 specimen (Lecuona and Desojo 2011) and Trialestes (in phylogenetic order Fig. 1a). All were bipeds or near bipeds. They ranged in size from something over a meter down to a half meter, so none were small or tiny, as in basal fenestrasaurs or basal mammals.

However, like basal fenestrasaurs, these croc and dino precursors elevated the forelimbs off the substrate, so they were free to do something else with them. Bipedal fenestrasaurs started flapping their forelimbs for several reasons, none related to flying…at first. Basal dinosaurs were just the opposite because dinosaur coracoids became more disc-like and less strut-like compared to their croc-like precursors (Fig. 1a).

With that said, let’s get back to skin, scales and feathers
At present the only clue to dermal appearance near the origin of dinosaurs is with Scleromochlus, a tiny bipedal croc close to Gracilisuchus (Fig. 1a). Scleromochlus has transverse bands of tiny scales (not large scutes) across its back (Figs. 1b, 2). Note this is exactly where feather primordials appear in embryo chicks (Fig. 3). Was the rest of Scleromochlus naked like a bird? Or scaled like…like I said, we have no examples of scales in fossil taxa near this node.

Were dorsal scales used to help stiffen the Scleromochlus lumbar area, like a girdle? That’s where the maximum stress would be felt on the long lever arm of the presacral area with a fulcrum at the acetabulum and sacral series.  A little support in the lower back would have been useful for these basal bipeds with long lumbar zones. But that’s not quite the situation in Herrerasaurus (Fig. 1a), which had a shorter torso and a bigger pelvis.

Scleromochlus, a basal crocodylomorph

Figure 2. Scleromochlus, a basal crocodylomorph not far from basal dinos, with tiny bands of scales. Gracilisuchus (not to scale) is in the upper right corner.

Now let’s put proto-dinosaurs into their environment 
Proto-dinosaur taxa were not denizens of the leaf litter. They were sprinting over it. And IF going bipedal suddenly makes you want to be glamorous and colorful, like a fenestrasaur, then dinosaurs might have gone down that same route starting with primordial feather bumps (Fig. 3) — IF ontogeny and embryology recapitulate phylogeny. Those primordials do make a pretty pattern, don’t they?

Figure 2. Primordial feathers on the back of a 10-day-old chick embryo.

Figure 3. Primordial feathers on the back of a 10-day-old chick embryo. From Dhouailly 2009., who reports: “In the chick embryo, the future feather first appears on the back as a round primordial. Then a weave of primordials develops across the back.” Note these primordial appear first on the back, as in Scleromochlus (Fig. 1).

Or maybe not…
Persons and Currie (2015) report 
“It is now recognized that early feathers had a simple form comparable in general structure to the hairs of mammals. This has led to the generally accepted opinion that the early feather coats of dinosaurs functioned as thermo insulation. Like mammalian hair, simple feathers could serve as insulation only when present in sufficiently high concentrations. We advocate for a novel origin theory of feathers as bristles. Bristles are facial feathers common among modern birds that function like mammalian tactile whiskers, and are frequently simple and hair-like in form. Bristles serve their role in low concentrations, and therefore offer a feasible first stage in feather evolution.”

They go on… “It is not difficult to imagine the first simple feather, or sparse arrangement of simple feathers, appearing on the face of a dinosaur, or more basal archosaurs, and providing an immediate slight selective benefit in the form of increased tactile sensitivity. Evolutionary pressures could then gradually favor more and longer bristles for the same function. Concentrations of bristles around the eyes and other key facial regions would begin to offer hygienic benefits as dust shields, and, once a high enough concentration of bristles was reached, they would begin to provide a small degree of insulation. As facial feathers, bristles would have been optimally positioned to insulate the relatively intense heat that is generally emitted from an animal’s head. In the final step, a high concentration of simple facial feathers with the primary function of thermal insulation would develop and eventually spread to encompass the rest of the body.”

Essentially this is the same as the whisker (vibrissae) hypothesis
for mammals. The problem is: dinosaurs did not go through a burrowing phase, or even a nocturnal leaf litter phase where tactile input would have been more important. No, they were primarily visual, aural and olfactory hunters.

Persons and Currie also mistakenly report
that pterosaurs were dinosaur relatives when they report, “Outside the Dinosauria, but on an adjacent branch of the archosaur family tree, are the hair-like pycnofibres found pervasively throughout pterosaurs.” This is an outdated paradigm as shown in the large reptile tree. So they’re not off to a good start here. To make matters worse for the Persons and Currie hypothesis, Dhouailly 2009 reports: “In the chick embryo, the future feather first appears on the back as a round primordial. Then a weave of primordials develops across the back.” (See fig. 3). So these primordia do not appear first on the face or neck, as Persons and Currie postulate — again IF ontogeny and embryology recapitulate phylogeny.

The bird/theropod connection
has been reinforced several dozen times with wonderful transitional examples from China and Germany, so there’s no need to hash through that again. The question has become: how far back do feathers go in dinosaurs now that we know ornithischians, like Kulidadromaeus (Fig. 6), likewise had protofeathers? So far, no one has found anything resembling feathers on sauropods and they probably never will…

Figure 2. In situ anterior causals of Eoraptor. A tracing (left) appears to indicate fibers (f not cracks, chisel marks or plant debris).

Figure 4. In situ anterior causals of Eoraptor. A tracing (left) appears to indicate fibers (f not cracks, chisel marks or plant debris).Click to enlarge.

But wait…
there may be some fibers arising from around the spines in Eoraptor (Fig. 2), which nests between sauropods and ornithischians. If basal dinosaurs had proto-feathers and ornithichians had proto-feathers, then intervening taxa, like Eoraptor, should also have had proto-feathers. In Eoraptor these lines were not described, and perhaps for good reason. Perhaps they are the flotsam and jetsam that sometimes attend fossils still in the matrix. Perhaps someday they will be looked at under a microscope with an eye to determine what they are.

Scales originated several times within the Reptilia
and feathers do not arise from scales as shown below (Fig. 5).

Figure x. From Dhouailly 2009, the various pathways to scales, hair and feathers, first in traditional phylogenies, and below according to the large reptile tree.

Figure 5. From Dhouailly 2009, the various pathways to scales, hair and feathers, above in traditional phylogenies, and below according to the large reptile tree. Click to enlarge. Note that mammals and archosaurs share a dermal condensation. Remember this could be analogous rather than homologous considering the phylogenetic distance.

However, some scales arose from feathers
Dhouailly (2009) proposed that “overlapping scales in some birds may be secondarily derived from feathers. Owl feet are covered with feathers, not scales.” This puts a whole new light on the scaly feet of birds — and beyond, perhaps, in dinosaurs. Workers have shown that feathers are not elaborate scales. But Dhouailly’s work (also see references therein) indicates that the only scales on birds (discounting the ventral pedal pads) are the foot scales and they were derived from feathers.

Many samples of dinosaur skin 
consist of granulated scales, not overlapping scales. The question is, are these former proto-feather primordia, too? Or just scales? Scales could be new structures in dinosaurs or evolved primordial. As carnivorous bipeds, basal birds were closer to the bauplan of basal dinosaurs than were the other large herbivorous dinosaur clades. And under their feathers, birds are naked.

Dhouailly 2009 reports: “Birds may have been entirely covered by feathers, except for the plantar face of their feet, of which the feather formation program is blocked at its initiation step by genetic limb regulation. The early morphogenesis of avian and mammalian integument implicates the formation of a dense dermis, followed by that of placodes overlying dermal condensations, in contrast to squamate skin.”

The origin of feathers
If feather primordials appeared on basal dinosaurs in the same pattern and shape they do in chick embryos (Fig. 3) then decoration for secondary sexual selection appears to be reason for the origin of dinosaur proto-feather primordial starting on the back. Evidently those patterned bumps were attractive but would only have made a visual impression at close range. As evolution progressed, evidently primordials became less interesting as crests and gigantism became the fashion — both in theropods and phytodinosaurs. Perhaps those more obvious secondary sexual traits were easier to see at a distance. So basal dino primordials could have become scales in later giants. They became feathers in smaller theropods and more obvious feathers as primordials elongated posterior to the now flapping forelimbs. Does that make sense?

(Godefroit et al. 2014) conclude that “protofeather-like structures were probably widespread in Dinosauria, possibly even in the earliest members of the clade.” That appears to be supported by phylogenetic bracketing.

Unfortunately Godefroit et al. go too far afield
when they report, “the ability to form simple monofilaments and more complex compound structures is potentially nested within the archosauromorph clade, as exemplified by Longisquama, pterosaurs, ornithischians, and theropods (including birds). As noted earlier, Longisquama and pterosaurs developed their monofilaments independently according to the large reptile tree.

 Figure 1. Kulindadromeus, a sister to Heterodontosaurus with proto-feathers. Images from and traced from Godefroit et al. 2014. Since theropods and heterodontosaurs both had something like feathers, if they were the same kind of feathers, their last common ancestor had feathers. That last common ancestor was a herrerasaur or its proximal predecessor. Note the Godefroit et al. skull does not match their description but has a standard maxilla ascending process. See color overlays for correct ed interpretation.


Figure 6. Kulindadromeus, a sister to Heterodontosaurus with proto-feathers. Images from and traced from Godefroit et al. 2014. Since theropods and heterodontosaurs both had something like feathers, if they were the same kind of feathers, their last common ancestor had feathers. That last common ancestor was a herrerasaur or its proximal predecessor. Note the Godefroit et al. skull does not match their description but has a standard maxilla ascending process. See color examples for correct ed interpretation. Click to enlarge.

Kulindadromeus
Godefroit et al 2014 described three types of scales and three types of feather-like structures on the heterodontosaur, Kulindadromeus (Fig. 6).

  1. Small (<3.5 mm long) imbricated and hexagonal scales, resembling the scutella in modern birds are associated with the distal parts of the tibiae
  2. Smaller (<1 mm) rounded and non overlapping scales occur around the manus, tarsus (metatarsus, and pes resembling the reticula along the plantar face of the pes in modern birds
  3. The tail is covered by at least five longitudinal rows of slightly arched scales. The largest scales (~20 mm long and 10 mm wide) occur along the proximal part. Each scale forms a triangular anterior spur that covers the preceding one, so that adjacent elements are interconnected by a clip-like system. Proximally, at the level of the base of the tail the scales become progressively smaller and more rounded and do not overlap.
  4. Monofilaments are widely distributed around the thorax, on the back, and around the head.
  5. Compound, non-shafted integumentary structures are along the humerus and femur. These occur as groups of six or seven filaments that converge proximally and arise from the central regions of a basal plate.
  6. On the proximal tibia clusters of six or seven ribbon-shaped elements appear more or less bundled together proximally, close to the bone surface. Thin internal parallel filaments are within each ribbon-shaped element.

Godefroit et al. report, “In Kulindadromeus the distal hindlimb is extensively covered by scales and devoid of featherlike structures. This condition might thus be primitive in  dinosaurs… [but] paleontological and genetic evidence suggests that the pedal scales of ornithuromorph birds are secondarily derived from feathers” as earlier described by Dhouailly (2009). And if so, are all dinosaur scales secondarily derived from primordials?That’s the big question at this point. 

Naked skin
was primitive for reptiles. Until evidence indicates otherwise, scales may have appeared independently in turtles, lepidosaurs, crocs, birds and non-bird dinosaurs. Currently there is no phylogenetic connection, and thus no homology between scale appearances in these several clades. That could be the fault of the fossil record. Or it could be that certain clades remained naked, as already demonstrated for pelycosaurs, therapsids, enaliosaurs and birds. Feathers arise from naked skin in chick embryos. Everyone know that. Even so, it’s still a potential paradigm buster when it comes to thinking about basal dinosaurs and their scales or lack thereof.

Scales come and go.
Scales may be less widely distributed in the reptile tree than mot of us thought before. Some scales become scutes, but none become feathers. And in meter-long basal dinos feathers probably originated in the middle of the back as primordials for decoration, not as face bristles.

Like you,
I’m learning as I go (just finished this the day it was published) and looking forward to the next discoveries and hypotheses that come out on this subject. If I’ve missed anything, please send me the data and corrections will be made.

References
Bennett AF and Ruben JA 1986. The metabolic thermoregulartory 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.
Godefroit P et al. 2014. A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science 345:451-455.
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

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