Multiple pathways to herbivory underpinned deep divergences in ornithischian evolution

Abstract

The extent to which evolution is deterministic is a key question in biology, 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9 with intensive debate on how adaptation 6 , 10 , 11 , 12 , 13 and constraints 14 , 15 , 16 might canalize solutions to ecological challenges. 4 , 5 , 6 Alternatively, unique adaptations 1 , 9 , 17 and phylogenetic contingency 1 , 3 , 18 may render evolution fundamentally unpredictable. 3 Information from the fossil record is critical to this debate, 1 , 2 , 11 but performance data for extinct taxa are limited. 7 This knowledge gap is significant, as general morphology may be a poor predictor of biomechanical performance. 17 , 19 , 20 High-fiber herbivory originated multiple times within ornithischian dinosaurs, 21 making them an ideal clade for investigating evolutionary responses to similar ecological pressures. 22 However, previous biomechanical modeling studies on ornithischian crania 17 , 23 , 24 , 25 have not compared early-diverging taxa spanning independent acquisitions of herbivory. Here, we perform finite-element analysis on the skull of five early-diverging members of the major ornithischian clades to characterize morphofunctional pathways to herbivory. Results reveal limited functional convergence among ornithischian clades, with each instead achieving comparable performance, in terms of reconstructed patterns and magnitudes of functionally induced stress, through different adaptations of the feeding apparatus. Thyreophorans compensated for plesiomorphic low performance through increased absolute size, heterodontosaurids expanded jaw adductor muscle volume, ornithopods increased jaw system efficiency, and ceratopsians combined these approaches. These distinct solutions to the challenges of herbivory within Ornithischia underpinned the success of this diverse clade. Furthermore, the resolution of multiple solutions to equivalent problems within a single clade through macroevolutionary time demonstrates that phenotypic evolution is not necessarily predictable, instead arising from the interplay of adaptation, innovation, contingency, and constraints. 1 , 2 , 3 , 7 , 8 , 9 , 18

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