Cretaceous bird with dinosaur skull sheds light on avian cranial evolution

Abstract

The transformation of the bird skull from an ancestral akinetic, heavy, and toothed dinosaurian morphology to a highly derived, lightweight, edentulous, and kinetic skull is an innovation as significant as powered flight and feathers. Our understanding of evolutionary assembly of the modern form and function of avian cranium has been impeded by the rarity of early bird fossils with well-preserved skulls. Here, we describe a new enantiornithine bird from the Early Cretaceous of China that preserves a nearly complete skull including the palatal elements, exposing the components of cranial kinesis. Our three-dimensional reconstruction of the entire enantiornithine skull demonstrates that this bird has an akinetic skull indicated by the unexpected retention of the plesiomorphic dinosaurian palate and diapsid temporal configurations, capped with a derived avialan rostrum and cranial roof, highlighting the highly modular and mosaic evolution of the avialan skull.

Fig. 1. Early Cretaceous enantiornithine IVPP V12707.

a Photograph. b digital reconstruction. at atlas, ca caudal vertebrae, ce cervical vertebrae, dt distal tarsals, lfe left femur, lil left ilium, lis left ischium, lpu left pubis, mt II–IV metatarsals II to IV, pd II–IV pedal digits II to IV, ph proximal phalanx of hallux, pt proximal tarsals, py pygostyle, rb rib, rfe right femur, rfi right fibula, ril right ilium, ris right ischium, rpu right pubis, rti right tibia, sk skull, sv sacral vertebra, tv thoracic vertebrae. Scale bars, 10 mm.

Fig. 2. Digital reconstruction of the skull of IVPP V12707.

a, b Skull and cranial cervicals. c Left lacrimal (arrowhead denotes the foramen). d Right jugal and quadratojugal (arrowhead denotes the corneal process). e Right squamosal. f Left quadrate (arrowhead denotes a fossa). g, h Facial reconstructions of IVPP V12707 (g), and Dromaeosaurus (h; modified from). c–e lateral view. f rostrolateral view. an angular, at atlas, atf antorbital fenestra, ax axis, bs basisphenoid-parasphenoid, ce cervical vertebra, co coronoid process, cr caudal ramus, de dentary, eb ethmoid bone, ec ectopterygoid, en external naris, fr frontal, hy hyoid, if infratemporal fenestra, is interorbital septum, jq jugal process, ju jugal, la lacrimal, lc lateral condyle, mf mandible fenestra, mx maxilla, na nasal, obp orbital process, oc occipital region, or orbit, otp otic process, pa palatine, pap paroccipital process, pm premaxilla, po postorbital, pop postorbital process, poz postzygapophysis, pp postorbital process, pr parietal, prp parietal processes, prz prezygapophysis, pt pterygoid, qf quadrate fenestra, qj quadratojugal, qjc quadratojugal cotyla, qjj quadratojugal process of jugal, qjs quadratojugal process of squamosal, rr rostral ramus, sa surangular, sf supratemporal fenestra, sp splenial, sq squamosal, sqp squamosal process, vr ventral ramus, vo vomer, l/r left/right side. Scale bars, 5 mm (a, b, g), 1 mm (c–f), 50 mm (h).

Fig. 3. Palatal complex comparison and primitive palate of IVPP V12707.

a–f Digital reconstruction of palatal elements of IVPP V12707: Basisphenoid-parasphenoid (ventral view); b Left pterygoid (lateral view); c Right vomer (dorsal view); and reconstructed palatal complex in ventral (d), lateral (e), and caudal view (f). g–j Digital reconstruction of Linheraptor (Dromaeosauridae) braincase in ventral view (h), palate complex in craniolateral (h) and caudomedial view (i), and left pterygoid in medial view (j). k, l Dromaius novaehollandiae (k; Casuariiformes), and Tragopan caboti (l; Galliformes) in ventral view, with their left quadrate and palatine in lateral view. bre basisphenoid recess, bsc basipterygoid process cotyla, bsp basipterygoid process, mc medial condyle, qur quadrate ramus, par palatine ramus, prr premaxillary ramus, psr parasphenoid rostrum, ptc pterygoid condyle, ptr pterygoid ramus, rfl rostral flange, sre subsellar recess. Scale bars, 5 mm (a–c), 2 mm, (d, e), 1 mm (f), 50 mm (k), 10 mm (l). The blue arrows denote the ball-socket articulation between the pterygoid and basisphenoid. The red arrows denote the condylar-based articulation between the quadrate and pterygoid, a derived feature absent in nonavialan dinosaurs and the enantiornithine IVPP V12707.

Fig. 4. Evolution of avian palatal complex and cranial kinesis.

The tree is simplified from the current phylogenetic analysis. The digitally reconstructed pterygoid exhibits almost identical morphology between enantiornithine IVPP V12707 and the dromaeosaurid Linheraptor. The modernization of modern avian palatal complex is signified by four stages, which collectively contribute to the avian cranial kinesis: a acquisition of the condylar-based contact between the quadrate and pterygoid; b–d loss/reduction of the quadrate ramus of the pterygoid (b), basipterygoid process (c), and ectopterygoid (d). The available fossils suggest all those modifications took place close to the origin of Ornithuromorpha. Drawings of palatal complex in ventral views except IVPP V12707 and tragopan are modified from literature^,, (shaded regions are not preserved, or reduced). The question marks denote the previous reconstructions of a quadrate-pterygoid articulation in Archaeopteryx and Sapeornis that should be treated with caution.