Herbivorous ecomorphology and specialization patterns in theropod dinosaur evolution

Abstract

Interpreting key ecological parameters, such as diet, of extinct organisms without the benefit of direct observation or explicit fossil evidence poses a formidable challenge for paleobiological studies. To date, dietary categorizations of extinct taxa are largely generated by means of modern analogs; however, for many species the method is subject to considerable ambiguity. Here we present a refined approach for assessing trophic habits in fossil taxa and apply the method to coelurosaurian dinosaurs--a clade for which diet is particularly controversial. Our findings detect 21 morphological features that exhibit statistically significant correlations with extrinsic fossil evidence of coelurosaurian herbivory, such as stomach contents and a gastric mill. These traits represent quantitative, extrinsically founded proxies for identifying herbivorous ecomorphology in fossils and are robust despite uncertainty in phylogenetic relationships among major coelurosaurian subclades. The distribution of these features suggests that herbivory was widespread among coelurosaurians, with six major subclades displaying morphological evidence of the diet, and that contrary to previous thought, hypercarnivory was relatively rare and potentially secondarily derived. Given the potential for repeated, independent evolution of herbivory in Coelurosauria, we also test for repetitive patterns in the appearance of herbivorous traits within sublineages using rank concordance analysis. We find evidence for a common succession of increasing specialization to herbivory in the subclades Ornithomimosauria and Oviraptorosauria, perhaps underlain by intrinsic functional and/or developmental constraints, as well as evidence indicating that the early evolution of a beak in coelurosaurians correlates with an herbivorous diet.

Fig. 1.

Select cranial traits appearing in multiple lineages of coelurosaurian theropod dinosaurs tested herein as PHTs. Ecomorphological indicators statistically correlated with extrinsic evidence of herbivory (first- and second-order CHTs) are marked with an asterisk. Traits featured on six species representing four coelurosaurian theropod subclades, including the only predominantly folivorous modern bird. (A) Opisthocomus hoazin skull, left lateral view (extant Aves), adapted from http://digimorph.org/. Extinct theropods: (B) Ornithomimus edmontonicus (RTMP 95.110.1) skull, left lateral view (derived Ornithomimosauria); (C) Shenzhousaurus orientalis (NGMC 977–4-002) skull, left oblique dorsolateral view (primitive Ornithomimosauria), adapted from ref. ; (D) Incisivosaurus gauthieri (IVPP V13326) skull left lateral view (primitive Oviraptorosauria); and (E) Caenagnathus collinsi (CMN 8776) fused lower mandibles, dorsal view (derived Oviraptorosauria; Table S7, and see SI Appendix, Section A3 for trait descriptions.

Fig. 2.

Phylogeny of coelurosaurian theropods used in correlation and correspondence analyses showing: (A) Distribution of EEH and EEC (Left; for explanation, see Table S1); (B) Ancestral state reconstruction optimizations using maximum parsimony (ASR-MP) of the 11 CHTs detected as evolving in a statistically significant order in the clades Ornithomimosauria and Oviraptorosauria (Left); and (C and D) Quantitative dietary interpretations at the species level based on the total number of actual CHTs (C Right) and interpretations estimated using ASR-MP (D Right), respectively (Table S3). Black bars on phylogeny at right represent taxa with intermediate numbers of CHTs for which diet is ambiguous. Only ancestral (not autapomorphic) optimizations were used for rank correspondence analysis although both are shown here. For alternate tree topologies used in analyses, see Fig. S1. Species collapsed into higher-level OTUs for Dromaeosauridae, Compsognathidae, and Tyrannosauroidea. Black/red stripe indicates that some species in higher-level OTUs possess evidence of diet. Actual CHT number ≤1 for all dromaeosaurs except Microraptor. Reconstructed CHT number ≤3 for all dromaeosaurs except Rahonavis, Buitreraptor, and Unenlagia. For specific data on CHT number per species, see Table S3. See SI Appendix, Section A3 for genus abbreviations.