Cretaceous bird from Brazil informs the evolution of the avian skull and brain

Abstract

A dearth of Mesozoic-aged, three-dimensional fossils hinders understanding of the origin of the distinctive skull and brain of modern (crown) birds¹. Here we report Navaornis hestiae gen. et sp. nov., an exquisitely preserved fossil species from the Late Cretaceous of Brazil. The skull of Navaornis is toothless and large-eyed, with a vaulted cranium closely resembling the condition in crown birds; however, phylogenetic analyses recover Navaornis in Enantiornithes, a highly diverse clade of Mesozoic stem birds. Despite an overall geometry quantitatively indistinguishable from crown birds, the skull of Navaornis retains numerous plesiomorphies including a maxilla-dominated rostrum, an akinetic palate, a diapsid temporal configuration, a small cerebellum and a weakly expanded telencephalon. These archaic neurocranial traits are combined with a crown bird-like degree of brain flexion and a bony labyrinth comparable in shape to those of many crown birds but substantially larger. Altogether, the emergent cranial geometry of Navaornis shows an unprecedented degree of similarity between crown birds and enantiornithines, groups last sharing a common ancestor more than 130 million years ago². Navaornis provides long-sought insight into the detailed cranial and endocranial morphology of stem birds phylogenetically crownward of Archaeopteryx, clarifying the pattern and timing by which the distinctive neuroanatomy of living birds was assembled.

Fig. 1. The holotype of the enantiornithine N. hestiae gen. et sp. nov. from the Late Cretaceous of Brazil.

a,b, Photograph (a) and interpretive drawing (b) of the exposed side of the holotype of N. hestiae (MPM-200-1) in left lateral view. c, Micro-computed tomography rendering of MPM-200-1 in right ventral–lateral view. Scale bar, 10 mm.

Fig. 2. Three-dimensional cranial reconstruction of N. hestiae.

Composite three-dimensional reconstruction of the skull of N. hestiae from MPM-200-1 and referred braincase MPM-334-1. Scale bar, 10 mm.

Fig. 3. Endocranial anatomy of N. hestiae and brain evolution in stem birds.

a, Three-dimensional reconstruction of the endocranial morphology of N. hestiae from MPM-200-1 and MPM-334-1. Portions deriving from MPM-200-1 and MPM-334-1, as well as the reconstruction process, are explained in the Methods and Extended Data Fig. 7. b, Evolution of endocranial morphology across Pennaraptora. Numbers in the coloured boxes refer to the degree of expansion of each of the main neuroanatomical and sensorial regions for each taxon. Brown arrows in b depict the orientation of the foramen magnum.

Fig. 4. Navaornis combines a geometrically crown bird-like skull with a central nervous system morphologically intermediate between Archaeopteryx and crown birds.

a, Three-dimensional principal component morphospace of neornithine skulls (PC1 versus PC2). Warped models illustrate extremes along PC1 and PC2. b, Three-dimensional principal component morphospace (PC1 versus PC3) of endocrania from Aves and relevant non-avian taxa. Navaornis falls in crown bird morphospace along PC3 but not along PC2 (Extended Data Fig. 10). Landmarks are colour-coded for high (warm colours) to low (cold colours) per-landmark variances. Brown arrows in b depict the foramen magnum orientation.

Extended Data Fig. 1. The holotype of the enantiornithine Navaornis hestiae gen. et sp. nov. and associated postcranial elements.

a,b, Photograph (a) and interpretative drawing (b) of the holotype (cranium, white colour in b, MPM-200-1), referred postcranial elements hypothesized to belong to the same individual (light grey in b, MPM-200), and additional associated bones interpreted as belonging to other individual enantiornithine birds (dark grey in b, MPM-200). The fossils were mechanically prepared, but their original connection and association is illustrated as they were found in the quarry.

Extended Data Fig. 2. The phylogenetic position of Navaornis hestiae.

Consensus tree based on implied weights (K = 12) using only the scorings derived from the holotype (cranium, MPM-200-1). Navaornis hestiae clusters with Gobipteryx minuta and Yuornis junchangi within Enantiornithes. Bootstrap values over 50% are listed on branches. Inset shows 2D line drawings based on our three-dimensional reconstruction of N. hestiae in dorsal, ventral and left lateral views.

Extended Data Fig. 3. In-situ cranial anatomy of Navaornis hestiae (exposed side).

a, Digital render from the reconstructed three-dimensional volumes of the in-situ micro-CT scanned cranial elements of the holotype (MPM-200-1). b,c, Three-dimensional renders of the same region and view are shown with different cranial elements sequentially removed in order to expose key anatomical details of underlying bones. Cranial elements are colour-coded as in Fig. 1.

Extended Data Fig. 4. In-situ cranial anatomy of Navaornis hestiae (matrix side).

a, Digital render from the reconstructed three-dimensional volumes of the in-situ micro-CT scanned cranial elements of the holotype specimen (MPM-200-1). b,c, Three-dimensional renders of the same region and view are shown with different cranial elements sequentially removed in order to expose key anatomical details of underlying bones. Cranial elements are colour-coded as in Fig. 1.

Extended Data Fig. 5. The three-dimensional cranial reconstruction of Navaornis hestiae (all main views).

Composite three-dimensional reconstruction of the skull of Navaornis from (MPM-200-1) and referred braincase (MPM-334-1) in six different views. Cranial elements are colour-coded as in Fig. 1.

Extended Data Fig. 6. Detailed cranial anatomy of Navaornis hestiae.

Plate showing all the main cranial elements from the holotype specimen of N. hestiae. (MPM-200-1) in different views and annotated anatomical details commented on in the main text.

Extended Data Fig. 7. The 3D reconstruction process of the brain and inner ear endocast of Navaornis hestiae.

Green arrow in b indicates the approximate outline of the dorsal rim of the parietal used to guide the retrodeformation process of the frontal.

Extended Data Fig. 8. Isolated braincase (MPM-334-1) is morphologically indistinguishable from the holotype of Navaornis hestiae.

Comparison of the basicranium and the endosseous labyrinth of the inner ear between the holotype MPM-200-1 and the referred specimen MPM-334-1 of Navaornis hestiae.

Extended Data Fig. 9. Cranial shape similarity between individual crown-bird species and Navaornis hestiae.

Shape differences are quantified as Procrustes distances between landmark configurations after Generalized Procrustes Superimposition (Procrustes residuals, see Methods). Species-values in the histogram plot are ordered from the most similar, to the least similar. Inset depicts the individual taxa that are closest in cranial shape to Navaornis. Note that the values of Procrustes distances to Navaornis are very similar among a wide range of species belonging to disparate lineages and that individual species do not necessarily resemble Navaornis in the same aspects of cranial geometry.

Extended Data Fig. 10. Additional information from the comparative geometric morphometrics analyses of exocranial and endocranial geometry.

a,b, Exocranial (a) and endocranial (b) landmarking scheme followed in this study. a, Some of the annotated changes in the exocranium landmarking scheme (see Methods for full list of changes). c,d, PCA bivariate plots of the morphospaces resulting from the three main axes (PC1-3) of exocranial (c) and endocranial (d) shape variation for Navaornis and the comparative datasets used in this study.