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. 2020 Aug 18;18(8):e3000801.
doi: 10.1371/journal.pbio.3000801. eCollection 2020 Aug.

Decelerated dinosaur skull evolution with the origin of birds

Affiliations

Decelerated dinosaur skull evolution with the origin of birds

Ryan N Felice et al. PLoS Biol. .

Abstract

The evolutionary radiation of birds has produced incredible morphological variation, including a huge range of skull form and function. Investigating how this variation arose with respect to non-avian dinosaurs is key to understanding how birds achieved their remarkable success after the Cretaceous-Paleogene extinction event. Using a high-dimensional geometric morphometric approach, we quantified the shape of the skull in unprecedented detail across 354 extant and 37 extinct avian and non-avian dinosaurs. Comparative analyses reveal fundamental differences in how skull shape evolved in birds and non-avian dinosaurs. We find that the overall skull shape evolved faster in non-avian dinosaurs than in birds across all regions of the cranium. In birds, the anterior rostrum is the most rapidly evolving skull region, whereas more posterior regions-such as the parietal, squamosal, and quadrate-exhibited high rates in non-avian dinosaurs. These fast-evolving elements in dinosaurs are strongly associated with feeding biomechanics, forming the jaw joint and supporting the jaw adductor muscles. Rapid pulses of skull evolution coincide with changes to food acquisition strategies and diets, as well as the proliferation of bony skull ornaments. In contrast to the appendicular skeleton, which has been shown to evolve more rapidly in birds, avian cranial morphology is characterised by a striking deceleration in morphological evolution relative to non-avian dinosaurs. These results may be due to the reorganisation of skull structure in birds-including loss of a separate postorbital bone in adults and the emergence of new trade-offs with development and neurosensory demands. Taken together, the remarkable cranial shape diversity in birds was not a product of accelerated evolution from their non-avian relatives, despite their frequent portrayal as an icon of adaptive radiations.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Estimation of rates of cranial evolution on a time-calibrated phylogeny of Dinosauria using a variable-rates BM model of evolution.
(A) In the rostrum, ornithischians evolved faster than avian and non-avian theropods. (B) The cranial vault evolves fastest in non-avian dinosaurs with bony cranial ornaments. (C) Rates of evolution are generally conserved and low in the occipital region, with slightly elevated rates in Passeriformes and in pachycephalosaurs. Black triangle indicates the origin of Aves. See S2–S36 Figs for estimated rates for all cranial regions and phylogenetic hypotheses and detailed tip labels. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls. BM, Brownian Motion.
Fig 2
Fig 2. Comparison of per-group evolutionary rate scalars.
Birds do not have the highest rates of evolution in any cranial region. For each group, mean rate scalar is the mean of the rate scalars in the post-burn-in posterior distribution under the variable-rates evolutionary model estimated using BayesTraits under the traditional Dinosaur phylogenetic hypothesis (Saurischia and Ornithischia as sister clades). Mean rates were scaled to the sum of the branch lengths in the corresponding subtree. Mean rate scalars were compared between groups using non-parametric t tests; significantly different distributions are indicated with ****p < 0.00005. These results are robust to subsampling of taxa (S1 Fig 37), Procrustes superimposition (S1 Fig 38) and alternative methods for comparing evolutionary rates (S39–S42 Figs). Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls.
Fig 3
Fig 3. Per-landmark evolutionary rates (under single-rate BM model) and Procrustes variance.
Landmarks and sliding semi-landmarks represented in the 9-module dataset (A, B) and 11-module dataset (C, D), illustrated on the skull of Erlikosaurus andrewsi (IGM 100/111). Landmarks are coloured according to evolutionary rate (A, C) and Procrustes variance (B, D), where a warmer colour indicates greater value. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls. BM, Brownian Motion; IGM, Paleontological Center, Mongolian Academy of Sciences.
Fig 4
Fig 4. Phenotypic difference between each specimen for each landmark in the 11-module dataset and the mean skull shape.
For each specimen, the mean landmark configuration is plotted with points coloured relative to the Procrustes distance between the position of that point in the mean shape and in that specimen. Warmer colours denote landmarks having higher displacement from the mean, and cooler colours are more similar to the mean shape. Data and code archived at www.github.com/rnfelice/Dinosaur_Skulls.

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Grants and funding

This research was funded by European Research Council grant no. STG-2014-637171 (to A.G.) and SYNTHESYS grant no. FR-TAF-5635 (to R.N.F.). M.A.N.’s work was funded by the Macaulay family endowment to the AMNH, and NSF DEB-1457181. L.M.W.’s work was funded by NSF IOS-1050154 and IOS-1456503. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.