Modern birds are typified by the presence of feathers, complex evolutionary innovations that were already widespread in the group of theropod dinosaurs (Maniraptoriformes) that include crown Aves. Squamous or scaly reptilian-like skin is, however, considered the plesiomorphic condition for theropods and dinosaurs more broadly. Here, we review the morphology and distribution of non-feathered integumentary structures in non-avialan theropods covering squamous skin and naked skin as well as dermal ossifications. The integumentary record of non-averostran theropods is limited to tracks, which ubiquitously show a covering of tiny reticulate scales on the plantar surface of the pes. This is consistent also with younger averostran body fossils, which confirm an arthral arrangement of the digital pads. Among averostrans, squamous skin is confirmed in Ceratosauria (Carnotaurus), Allosauroidea (Allosaurus, Concavenator, Lourinhanosaurus), Compsognathidae (Juravenator), and Tyrannosauroidea (Santanaraptor, Albertosaurus, Daspletosaurus, Gorgosaurus, Tarbosaurus, Tyrannosaurus), whereas dermal ossifications consisting of sagittate and mosaic osteoderms are restricted to Ceratosaurus. Naked, non-scale bearing skin is found in the contentious tetanuran Sciurumimus, possibly ornithomimosaurians (Pelecanimimus) and tyrannosauroids (Santanaraptor), and also on the patagia of scansoriopterygids (Ambopteryx, Yi). Scales are surprisingly conservative among non-avialan theropods compared to some dinosaurian groups (e.g., hadrosaurids); however, the limited preservation of tegument on most specimens hinders further interrogation. Scale patterns vary between and/or within body regions in Carnotaurus, Concavenator and Juravenator, and include polarised, snake-like ventral scales on the tail of the latter two genera. Unusual but more uniformly-distributed patterning also occurs in Tyrannosaurus, whereas feature scales are present only in Albertosaurus and Carnotaurus. Few theropods currently show compelling evidence for the cooccurrence of scales and feathers (e.g., Juravenator, Sinornithosaurus), although reticulate scales were probably retained on the mani and pedes of many theropods with a heavy plumage. Feathers and filamentous structures appear to have replaced widespread scaly integuments in maniraptorans. Theropod skin, and that of dinosaurs more broadly, remains a virtually untapped area of study and the appropriation of commonly-used techniques in other palaeontological fields to the study of skin holds great promise for future insights into the biology, taphonomy and relationships of these extinct animals.

To perform our review, we studied the non-feathered epidermal structures and dermal ossifications in 25 non-avialan theropod taxa bracketed phylogenetically between the early-diverging Theropoda Tawa alae (Nesbitt et al., 2009) and the early-diverging avialan Archaeopteryx lithographica (Elzanowski, 2001; Christiansen & Bonde, 2004; Mayr, Pohl, & Peters, 2005; Foth, Tischlinger, & Rauhut, 2014). Only postcranial osteoderms were considered in this study. With the possible exception of Tyrannosaurus (the epipostorbital; see Carr, 2020), the cranial dermal ossifications reported in some theropods such as abelisaurids (Carrano & Sampson, 2008) are more cornified tissues, armour-like dermis and other types of dermal ornamentations than true osteoderms (Carr et al., 2017; Delcourt, 2018). Specimens belonging to 22 taxa deposited in scientific collections of France, Germany, Portugal, Spain, Argentina, Brazil, USA, Canada, and China were examined first-hand and anatomical observations were assisted with the use of a digital camera and/or a digital microscope AM411T Dino-Lite Pro. The original integument was observed in the majority of theropod taxa, but high-resolution casts of skin were also used for specimens belonging to four non-maniraptoriform avetheropods (i.e., Allosaurus, Albertosaurus, Tarbosaurus and Tyrannosaurus). Descriptions and illustrations in the literature were relied upon for three additional taxa (i.e., Sciurumimus, Ornithomimus, and Epidendrosaurus), including high-resolution photographs provided by two colleagues for one of them (i.e., Sciurumimus). Three-dimensional (3D) models of skin were generated for Carnotaurus (MACN-CH 894) using photogrammetric data and the software Agisoft Photoscan 1.3.4, as well as for Allosaurus (UMNH VP C481) using a Creaform Go!SCAN 20 surface scanner at 0.2 mm resolution. The 3D models were exported, oriented, and scaled in Meshlab version 1.3.4BETA (Cignoni et al., 2008) and deposited in MorphoMuseuM (https://morphomuseum.com/) where they are freely downloadable (see Hendrickx & Bell 2021). Laser-Stimulated Fluorescence (LSF) imaging was used to describe preserved integument using standard protocols (Kaye et al., 2015; Wang et al., 2017). Morphology of the non-avialan theropod skin was compared to that of other dinosaurs and living amniotes based on personal examination and high-quality photographs of the skin of ornithischian and sauropodomorph dinosaurs, living birds, crocodiles, squamates and turtles.

To review the distribution and evolution of epidermal structures and dermal ossifications in dinosaurs, we mapped 71 tegument-based characters coded for 67 archosauriform taxa, among which 40 taxa were examined first hand (See Excel file "Dataset_theropod_integument_Aug_2021.xlsx"; Mesquite files "Mapping_Integument_characters_Aug_2021.nex" and "Mapping_Integument_characters_Aug_2021_no_DIP.nex"; TNT files "Mapping_Integument_characters_Aug_2021.tnt"and "Mapping_Integument_characters_Aug_2021_no_DIP.tnt"). Although characters on epidermal structures (i.e., smooth skin, scales, osteoderms and feathers) are incorporated in some data matrices, the majority of the integument-based characters we propose are new (See Excel file "Dataset_theropod_integument_Aug_2021.xlsx"). Taxa were bracketed phylogenetically between early-diverging archosauriforms (Campione et al. (2020) and references therein) and the early-diverging avialan Archaeopteryx lithographica (e.g., Foth, Tischlinger, & Rauhut, 2014). Non-ornithodiran archosauriforms were chosen as the outgroup over pterosaurs because the latter already show particularly derived integuments such as a non-scaly skin forming an airfoil and complex filamentous structures (Bakhurina & Unwin, 1995; Frey et al., 2003; Kellner et al., 2010; Barrett et al., 2015; Yang et al., 2019) whereas basalmost archosauriforms show the plesiomorphic condition of having body scales (Reisz & Sues, 2000; Campione et al., 2020). Sauropodomorphs and ornithischians were also excluded as the outgroups because their phylogenetic distribution among dinosaurs is unsettled (see Baron, Norman, & Barrett, 2017; Langer et al., 2017; Müller et al., 2018; Baron, 2021) and their most-basal members preserving integument (monofilaments in the heterodontosaurid Tianyulong, polygonal basement scales in the sauropod Mamenchisaurus; (Ouyang & Ye, 2002; Zheng et al., 2009) have very different epidermal structures.

The distribution of integument-based characters was visualized on six topological trees representative of alternative phylogenetic hypotheses for non-avian theropod evolution (See Mesquite file "Mapping_Integument_characters_Aug_2021_no_DIP.nex"). These informal supertrees were built using Mesquite 3.2 (Maddison & Maddison, 2017) following the results obtained by Godefroit et al. (2014) and Boyd (2015) for ornithischians, Müller et al. (2018) for non-tetanuran saurischians, Rauhut et al. (2012) for non-coelurosaur tetanurans, Delcourt and Grillo (2018) for tyrannosauroids, and Pei et al. (2020) for maniraptoriforms (see Pittman et al., 2020). Variations in the topology result from the differing placement of: 1) Juravenator as a non-avetheropod tetanuran (Tree1; Rauhut et al., 2012; Foth et al., 2020) or a compsognathid coelurosaur (Tree2; Pei et al., 2020); 2) sauropodomorphs within the clade of Saurischia (Tree1; e.g., Langer et al., 2017; Müller et al., 2018) or as a sister-clade of Ornithoscelida (Tree3; i.e., Theropoda + Ornithischia; Baron, Norman, & Barrett, 2017); 3) anchiornithines as early-branching avialans (Tree1; Pei et al., 2020) or troodontids (Tree4; Brusatte et al., 2014); and 4) troodontids among Deinonychosauria (Tree1; Turner, Makovicky, & Norell, 2012; Pei et al., 2020), as the sister clade of Dromaeosauridae + Averaptora (Tree5; Motta et al., 2020), or as the sister clade of Avialae (Tree6; Avialae = Anchiornithinae + Archaeopteryx; Cau et al., 2017; Foth & Rauhut, 2017). Our preferred topology (Tree1) follows a phylogenetic tree in which Sauropodomorpha and Theropoda form the clade Saurischia, Juravenator and Sciurumimus are classified as early-branching non-avetheropod Tetanurae (n.b., the integument of Juravenator is, however, described in the section on Compsognathidae), anchiornithines are placed as the earliest birds, and Deinonychosauria is resolved. Although included in the data matrix for comparative purposes, a large unnamed tyrannosauroid STM 1-5 (Xu et al., 2010) and the contentious maniraptoran Yixianosaurus longimanus (Xu & Wang, 2003) were excluded in the analyses because their phylogenetic distribution among coelurosaurians are unsettled (Dececchi, Larsson, & Hone, 2012; Xu, Sullivan, & Wang, 2013; Lambertz, 2017). Conversely, because of its importance in our understanding of feather evolution (Xing et al., 2016; Lambertz, 2017) and while its position among coelurosaurs is unsettled, the specimen DIP-V-15103 was included in the analysis following the topology of our preferred tree topology and classified as a basally branching non-neocoelurosaur coelurosaur (Tree0). Character distributions for integument-based features were visualized on each tree WinClada 1.00.08 (Nixon, 2002) based on the Nexus file created with Mesquite 3.6.1 (See Mesquite files "Mapping_Integument_characters_Aug_2021.nex" and "Mapping_Integument_characters_Aug_2021_no_DIP.nex").

An ancestral state reconstruction analysis was additionally performed in Mesquite v. 3.6.1 using the parsimony criterion with the integument based data matrix and the six aforementioned tree topologies (See Mesquite File "Ancestral_state_reconstruction_analysis_Aug_2021.nex"). The ParsimonyUnordered model was used as it is the software's standard parsimony mapping for categorical data. This calculates the most parsimonious ancestral states at the nodes of the tree assuming one step per state change (unordered or Fitch parsimony). In this analysis, the ichnotaxa Grallator and Eubrontes (e.g., Gatesy, 2001; Demathieu et al., 2002; Milner et al., 2006a) as well as the non-avialan coelurosaur DIP-V-15103 (Xing et al., 2016), the oviraptorosaur Ningyuansaurus (Ji et al., 2012) and the microraptorine IVPP V13476 (Xu & Li, 2016) were excluded as their phylogenetic affinities are insufficiently resolved.

 

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Each file is self-explanatory.