Ultramicrostructural reductions in teeth: implications for dietary transition from non-avian dinosaurs to birds

Abstract

Background: Tooth morphology within theropod dinosaurs has been extensively investigated and shows high disparity throughout the Cretaceous. Changes or diversification in feeding ecology, i.e., adoption of an herbivorous diet (e.g., granivorous), is proposed as a major driver of tooth evolution in Paraves (e.g., Microraptor, troodontids and avialans). Here, we studied the microscopic features of paravian non-avian theropod and avialan teeth using high-spatial-resolution synchrotron transmission X-ray microscopy and scanning electron microscopy. Results: We show that avialan teeth are characterized by the presence of simple enamel structures and a lack of porous mantle dentin between the enamel and orthodentin. Reduced internal structures of teeth took place independently in Early Cretaceous birds and a Microraptor specimen, implying that shifts in diet in avialans from that of closely related dinosaurs may correlate with a shift in feeding ecology during the transition from non-avian dinosaurs to birds. Conclusion: Different lines of evidence all suggest a large reduction in biting force affecting the evolution of teeth in the dinosaur-bird transition. Changes in teeth microstructure and associated dietary shift may have contributed to the early evolutionary success of stemward birds in the shadow of other non-avian theropods.

Molecular phyloecology suggests a trophic shift concurrent with the evolution of the first birds

“…The herbivory of the CALB is also consistent with the occurrence of ceca observed in the majority of living birds, including the basal lineages (e.g., ratites), which is generally considered to be helpful for cellulose digestion and fermentation linked to herbivory 18,78 . The dietary shift of the CALB to herbivory is also consistent with the observation of reductions in both the teeth 3,8 and biting force 79,80 across the theropod-bird transition, which is considered to have resulted from the dietary shift from carnivorous to herbivorous diets 15,79 . The similar transition from carnivory to herbivory occurs multiple times in theropods 15,81,82 .…”

“…The similar transition from carnivory to herbivory occurs multiple times in theropods 15,81,82 . The causes underlying the evolutionary shift to the herbivory of the CALB are not clear, but the possible competition from carnivorous theropods and pterosaurs is proposed as a possible candidate 14,79 . The finding of the herbivory of the CALB ingesting fruits, seeds, and/or nuts, which characterize seed plants adapted to dry land environments 83 , may strongly suggest that the CALB mainly occurred in terrestrial habitats rather than an aquatic environment, as hypothesized previously 84 .…”

Trophic shift and the origin of birds

“…The herbivory of the CALB is also consistent with the occurrence of ceca observed in the majority of living birds, including the basal lineages (e.g., ratites), which is generally considered to be helpful for cellulose digestion and fermentation linked to herbivory (Clench and Mathias 1995;Miller and Harley 2016). The dietary shift of the CALB to herbivory is also consistent with the observation of reductions in both teeth and biting force across the theropod-bird transition, which is considered to have resulted from the dietary shift from carnivorous to herbivorous diets (Zanno and Makovicky 2011;Li et al 2020). The similar transition from carnivory to herbivory occurs multiple times in theropods (Zanno et al 2009; Zanno and Makovicky 2011; Barrett 2014).…”

“…The causes underlying the evolutionary shift to the herbivory of the CALB are not clear, but the possible competition from carnivorous theropods and pterosaurs is proposed as a possible candidate (Wang et al 2016a;Li et al 2020). The finding of the herbivory of the CALB ingesting fruits, seeds, and/or nuts, which characterize seed plants adapted to dry land environments (Cowen 2013), may strongly suggest that the CALB mainly occurred in terrestrial habitats rather than an aquatic environment, as hypothesized previously (You et al 2006).…”

“…This may be particularly true for early birds that would necessarily demand frequent foraging (O'Connor 2019) and much time for the oral processing of their food (e.g., hard seeds) (O'Connor and Zhou 2020) if no gizzard were available under relatively high predation risk (including both aerial, arboreal, and ground predators), while the evolution of the bird-like digestive system may help to maximize foraging efficiency and minimize their exposure to predators. Indeed, direct fossil evidence, for instance, the preservation of intact seeds or whole fish in the alimentary canal of ancestral birds, demonstrates that ancestral birds seem not to have used their teeth to process food; rather, their teeth, if any, were mainly used for the acquisition of food (Zhou and Zhang 2002;Zheng et al 2011;Zheng et al 2014;O'Connor and Zhou 2015;Li et al 2020).…”