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.
Highlights
Among tetrapods, extant birds exhibit incredible taxonomic and ecomorphological diversity, comprising over 10,000 extant species that occupy myriad niches on 7 continents [1,2,3]
Extant birds exhibit incredible taxonomic and ecomorphological diversity, comprising over 10,000 extant species that occupy myriad niches on 7 continents [1,2,3]. They possess a number of specialised traits that have been proposed as key innovations that facilitated their radiation, including the keeled pectoral girdle and flight stroke [4,5]; a hindlimb capable of perching [6]; a short, fused caudal axial skeleton [7]; an air-sac–based respiratory system [8]; an edentulous beak [9]; and highly encephalised brains [10,11] among other traits. Did this broad suite of phenotypic changes result in enhanced disparity and rates of phenotypic evolution in birds compared to their non-avian relatives? The rich fossil record shows that the stem group of birds, the non-avian dinosaurs, exhibit remarkable variation in body plan, body size, and trophic ecology [12,13]
The patterns of cranial shape evolution exhibited by birds do not reflect those of the other dinosaur groups
Summary
Extant birds exhibit incredible taxonomic and ecomorphological diversity, comprising over 10,000 extant species that occupy myriad niches on 7 continents [1,2,3] They possess a number of specialised traits that have been proposed as key innovations that facilitated their radiation, including the keeled pectoral girdle and flight stroke [4,5]; a hindlimb capable of perching [6]; a short, fused caudal axial skeleton [7]; an air-sac–based respiratory system [8]; an edentulous beak [9]; and highly encephalised brains [10,11] among other traits. Despite this uncertainty about the timing of rate shifts in dinosaur macroevolution, there is an emerging consensus that there is heterogeneity in the tempo and mode of evolution across body regions [15,20] and across lineages [16,17,18,22]
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