A skeleton from the Middle Jurassic of Scotland illuminates an earlier origin of large pterosaurs Author Jagielska, Natalia School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK n.jagielska@sms.ed.ac.uk Author O’Sullivan, Michael Gortroe Rathkeale, Co Limerick, Ireland Author Funston, Gregory F. School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK Author Butler, Ian B. School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK Author Challands, Thomas J. Author Clark, Neil D. L. The Hunterian, University of Glasgow, University Avenue, Glasgow, Scotland G 12 8 QQ, UK Author Fraser, Nicholas C. School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK & National Museums Scotland, Chambers Street, Edinburgh, Scotland EH 1 1 JF, UK Author Penny, Amelia School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK & School of Biology, University of St Andrews, Biomedical Sciences Research Complex, St. Andrews, Scotland KY 16 9 ST, UK Author Ross, Dugald A. Staffin Museum, 6 Ellishadder, Staffin, Isle of Skye, Scotland IV 51 9 JE, UK Author Wilkinson, Mark School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK Author Brusatte, Stephen L. School of GeoSciences, University of Edinburgh, Grant Institute, James Hutton Road, Edinburgh, Scotland EH 9 3 FE, UK & National Museums Scotland, Chambers Street, Edinburgh, Scotland EH 1 1 JF, UK stephen.brusatte@ed.ac.uk text Current Biology 2022 2022-02-28 32 1 8 http://dx.doi.org/10.1016/j.cub.2022.01.073 journal article 10.1016/j.cub.2022.01.073 93361143-cbf9-4a9e-a1c3-0271ebeea406 6251702 Dearc sgiathanach sp. nov. Etymology Scottish Gaelic, with the double meaning of ‘‘winged reptile’’and ‘‘reptile from Skye,’’ paying homage to pterosaurs (winged reptiles) and the Gaelic name for Skye (An t-Eilean Sgitheanach, the ‘‘winged isle’’). Phonetic pronunciation: jark ski-an-ach. Holotype NMS (National Museums Scotland, Edinburgh) G.2021.6.1-4 ( Figures 1, 2 , 3 , S 2 , and S3), a three-dimensionally preserved articulated skeleton, lacking anterior and dorsal portions of the cranium, left manus, portions of the wings, hindlimb elements, and the distal tail. The fossil was separated into four slabs during preparation: the main slab contains the majority of bones, exposed in dorsal view ( NMS G.2021.6.1 ), and the main counter slab contains bones exposed ventrally ( NMS G.2021.6.3 ). An additional block contains a wing phalanx ( NMS G.2021.6.4 ). The skull and anterior cervical vertebrae (NMS G. 2021.6.2 ) were separated from the main slab for X-ray computed microtomography ( M CT) ( Figure 2 ). Measurements in Data S1A. Figure 1. The new Middle Jurassic pterosaur Dearc sgiathanach (A–C) Photographs of main slab (NMS G.2021.6.1– 2), bones in dorsal view (A); wing phalanges 2–3 (NMS G.2021.6.3–4), in dorsal view (B); and main counterslab (NMS G.2021.6.3), bones in ventral view (C). (D–F) Schematic drawings of (A)–(C). (G–H) Reconstruction of skull in dorsal (G) and ventral (I) views and skeleton in lateral view (H). ar, articular region; cd, caudal vertebrae; cor, coracoid; cv, cervical vertebrae; d, digit; den, dentary;dors,dorsal vertebrae;dpc,deltopectoral crest; ep, extensor process; fm, femur; gas, gastralia; hdc, humeral distal condyle; hmt, humeral tubercle; isc, ischium; ju, jugal; max, maxilla; mc, metacarpal; mt,metatarsal;po,postorbital;r, ribs; sac, sacral plate; sca, scapula; scv, sacral (?) vertebrae; sm, sesamoid; sq, squamosal; st, sternum; symp, symphysis; uc, ulnar crest; ul, ulna; wp, wing phalanx; r/l, right/left. Blue on reconstructions are missing regions; red line in (E) is location of histological sectioning. Scale bars, 30 mm. See Figures S2 and S 3 . Locality and horizon The specimen was discovered by A.P. in 2017 at Rubha nam Brathairean ( Brothers’ Point ), Trotternish , Isle of Skye , Scotland , in the Lonfearn Member of the Lealt Shale Formation (Bathonian, Middle Jurassic) 9 , 10 ( Figure S1 ). The skeleton was embedded in a well-sorted lagoonal bioclastic limestone (rich in Neomiodon , ostracods, and conchostracans), which overlies and infills dinosaur trackways impressed in subaerially exposed mudstones. 11 These units formed in a marginal marine/nearshore environment that fluctuated between submerged and exposed. Diagnosis Dearc sgiathanach is a rhamphorhynchine pterosaur with the following autapomorphies: tri-tubular vomers with ‘‘trident-shaped’’ precapillary contact, pre-choana depression on the palatal surface of the maxilla, enlarged optic lobes expanded anteroposteriorly, and fourth metatarsal more robust (diameter 2.5 × ) than mt1-3. For additional information, see STAR Methods. Bone histology and maturity Using Bennett’s 12 osteologically based ontogenetic stages for the closely related Rhamphorhynchus , NMS G. 2021.6.1–4 has features of terminal-stage adults, such as large and recurved premaxillary teeth, fused scapula-coracoid, well-developed humeral crests, smooth bone texture, and fused long bone epiphyses. However, some osteological features are indicative of immaturity according to Bennett: 12 portions of the skull are unfused, such as the jugal with the lacrimal, and there appears to be limited fusion in the sacral vertebrae. Immaturity is corroborated by bone histology (STAR Methods; Data S2). The cortex of a sampled wing phalanx is composed entirely of primary fibrolamellar bone 13 and preserves two prominent lines of arrested growth (LAGs), which indicate that the individual was at least 2 years old at death. 14 The position of the second LAG close to the external bone surface suggests that the individual died shortly after emerging from an annual growth hiatus. The cortex is densely vascularized and has a high proportion of woven bone, indicating a rapid rate of growth throughout life. 15 The presence of vasculature extending to the external bone surface and the absence of an external fundamental system indicate that the individual was actively growing when it died. In many respects, the bone microstructure is similar to small, young individuals (<30% adult wingspan; size class I 12 ) of Rhamphorhynchus 16 and other actively growing juvenile pterosaurs, 17 , 18 indicating that it is best interpreted as a juvenile or subadult 19 that had not reached adult body size when it perished. Figure 2. Skull of the new Middle Jurassic pterosaur Dearc sgiathanach and comparisons of pterosaur brain and ear endocasts (A–L) Photographs (A–D), segmented M CT scan renderings (E–H), and schematic drawings (I–L) of the skull (NMS G.2021.6.2) in, from top to bottom, left lateral (reversed), dorsal, right lateral, and ventral views. (M–U) Brain and inner ear endocasts of Rhamphorhynchus (based on Witmer et al. 7 ) (M, P, and Q), Dearc (N, R, and S), and Tapejara (based on Eck et al. 8 ) (O, T, and U), shown in the skull in left lateral view and isolated in left lateral and dorsal views, respectively. asc, anterior semi-circular canal; bp, basisphenoid; cbl, cerebellum; cer, cerebrum; ch, choana; chl, channels; cv, third cervical; d, dentary; den, dentition; e, endocast; ec, ectopterygoid; et, edentulous anterior tip; f, frontal (?); hy, hyoid; ipv, interpterygoid vacuity; itf, inferior temporal fenestra; j, jugal; la, lacrimal; md, matrix infilled dent; mx, maxilla; n, nasal; olf, olfactory bulb; opl, optic lobe; p, parietal; pm, premaxilla; po, postorbital; ppd, post-palatal depression; psc, posterior semi-circular canal; ptf, pneumatic foramen; q, quadrate; qj, quadrojugal; rapr, retroarticular process; rh, probable placement of rhamphotheca; sof, suborbital fenestra; sq,squamosal;sbtf,subtemporal fenestra;stf, superior temporal fenestra.In (E)–(L), bones that cannot be distinguished in the M CT scan due to fusion or insufficient resolution are conservatively rendered together in one color. Scale bars, 30 mm. See Figure S2 . Wingspan and body size Wingspan—defined as double the summed lengths of the bones of a single wing 5 —is tightly correlated to body mass and wing area in pterosaurs and thus a robust body size proxy. 20 A complete wingspan cannot be measured directly from NMS G.2021.6.1–4 because some wing phalanges are missing. To estimate wingspan, we compiled measurements of complete wingspans of two non-monofenestratans represented by large sample sizes— Rhamphorhynchus and Dorygnathus —and regressed these against the lengths of individual bones to create predictor formulas (STAR Methods; Data S1C–S1Q). Using Rhamphorhynchus scaling, the humerus length (112 mm) and skull length (222 mm) of NMS G.2021.6.1–4 indicate wingspans of 3.8 and 2.2 m, respectively. The largest known Rhamphorhynchus (Natural History Museum UK 37002) is considerably smaller, with a wingspan of 1.8 m, humeral length of 79 mm, and skull length of 202 mm. Using Dorygnathus scaling, the humeral length of NMS G.2021.6.1–4 indicates a wingspan of 1.9 m, approximately 10% larger than the largest Dorygnathus (1.69 m wingspan, 84 mm humerus). These results demonstrate that Dearc is the largest Jurassic pterosaur yet known, consistent with the fact that its humerus and skull are the longest of any Jurassic specimens. Furthermore, we interpret these results as evidence that Dearc likely achieved wingspans over 2.5 m, and perhaps larger (>3 m). This is based on two lines of reasoning. First, we consider the Rhamphorhynchus equations, which give larger wingspan estimates, as the most valid predictors: Rhamphorhynchus is a closer relative of Dearc than is Dorygnathus , is known from a larger sample size (and thus generates a regression with tighter error bars and a higher r 2 value), and has a well-established and nearly isometric growth trajectory that makes predicting wingspan from isolated skeletal elements more justifiable. 21 Second, the holotype of Dearc (NMS G.2021.6.1–4) was an actively growing juvenile-subadult at death and would have been larger as an adult (STAR Methods). Description A detailed description is provided in Data S2, with salient features summarized here. Dearc generally conforms to the classic non-monofenestratan body plan, as it has an elongate mandibular symphysis (>20% mandible length), cervical ribs (visible in M CT data of anterior cervicals), a neck shorter than the combined dorsal and sacral series, a short metacarpus (<80% humerus length), and an elongate tail comprised of elongate caudal vertebrae supported by interlocking zygapophyses ( Figures 1, 2 , and 3). It does, however, possess some features typical of pterodactyloids and often considered part of a ‘‘module’’ unique to their bauplan, 6 including a skull that is longer than the combined dorsal and sacral series and a highly inclined quadrate ( Figure 2 ). Furthermore, although the cervical vertebrae are short and squat as in non-monofenestratans, they are proportionally more elongate than most members of that grade, beginning to approach the proportions of more derived pterosaurs like Wukongopterus lii and Douzhanopterus zhengi 22 , 23 (STAR Methods). There is a continuum between two distinct types of dentition: elongate fangs at the snout tip and conical pegs along much of the jaw length ( Figures 2 and 3 ). Figure 3. Postcranial skeleton and dentition of the new Middle Jurassic pterosaur Dearc sgiathanach Photographs of the right manus (A), cervical series (B), pubic region (C), right humerus (D), left humerus (E), left metacarpal-phalanx articular region (F), right maxilla (G), and left pes (H) of NMS G.2021.6.1–4. ac, anterior caudal vertebrae; ar, articular region; c, condyle; cdv, caudal vertebrae; cor, coracoid; cv, cervical vertebrae; d, dentary; dc, distal condyle; dpc, deltopectoral crest;dvrt, dorsal vertebrae; en,enamel;exp,extensor process; fem,femur; ft, flexor tubercle; gas,gastralia; h, humerus;ic, intercondylar groove; isc,ischium; max,maxilla; mcp,metacarpal; md, maxillary dentition; mg, medial groove; mt, metatarsal; nss,neural spine scar; pa, preacetabular process; poz, postzygapophysis ppb,prepubis; prez,prezygapophysis; rad,radius;rb,rib; sac,sacrum;sm,sesamoid;uc,ulnar crest; ul,ulna;un, ungual;vert, vertebra;wp1, wing phalanx one. Scale, 10 mm per bar. See Figures S2 and S 3 . Figure 4. Phylogenetic relationships of the Middle Jurassic pterosaur Dearc sgiathanach and wingspan estimates for Jurassic pterosaurs Strict consensus of most parsimonious trees from phylogenetic analysis,with silhouettes scaled to wingspan ( Dearc = ca.2.0 m) (1), and skull reconstructions of key taxa: (A) Scaphognathus crassirostris (based on GPIB 1304), (B) Dorygnathus banthensis (based on SMNS 55886), (C) Rhamphorhynchus muensteri (based on NHMUK R 37002), (D) Angustinaripterus longicephalus (based on ZDM T8001), and (E) Dearc sgiathanach . Wingspan plot (2): estimated wingspan range for isolated pterosaur remains from the Taynton Limestone collection. See Data S1D for complete element list. (A) NHMUK PV R 36634, (B) GSM 113726, (C) OUM J28352,(D) NHMUK PV R 38016, (E) NHMUK PV R1362, (F) LL12158, (G) NHMUK PV R 40126,(H) NMS G.2021.6.1-4 ( Dearc ), (I) OUM J23046, (J) OUM J28273, (K) NHM UK PV R 40126 B, (L) OUM J28319, (M) OUM J28307, (N) OUM J28271, (O) OUM J28354, (P) LL12160, (Q) OUM J23047, and (R) MJM L K1995. See Figure S4 and Data S1 and S2. M CT data provide a stellar view of a complete, articulated palate and hyoid of a non-monofenestratan pterosaur in dorsal and ventral view ( Figure 2 ). The heart-shaped choana is cut medially by forking vomers, comprised of three cylindrical rods that converge anteriorly in a trident-shaped contact. There is a thin extension of the ectopterygoid, which rotates around its own axis, forming an elevated ventral border of the postpalatine fenestra, joining the vomers at a perpendicular angle. This ‘‘contorted’’ morphology has not been described in other pterosaurs. M CT data also provide one of the few brain and inner ear endocasts of a basal pterosaur ( Figure 2 ). Like Rhamphorhynchus , 7 Dearc had a large cerebrum with optic lobes positioned at the same level as the forebrain and a large flocculus, around which thin and arched semicircular canals looped, that nonetheless did not project to the same lateral level as the cerebrum. In pterodactyloids, however, the brain is highly flexed so that the cerebrum is elevated relative to the optic lobes, and the flocculus is expanded beyond the cerebrum laterally. 7 , 8 , 24 In Dearc , the optic lobes are larger, anteroposteriorly longer, and more widely exposed dorsally than in any known basal pterosaur or pterodactyloid ( Rhamphorhynchus , 7 Allkauren , 24 and Tapejara 8 ). Phylogenetic analysis Our phylogenetic analysis focuses on non-monofenestratan pterosaurs and combines data from several independent published analyses 22 , 25 – 35 with new characters, while excluding taxa known only from highly immature specimens and characters that exhibit strong ontogenetic variation, resulting in a dataset of 58 taxa scored for 155 characters (Data S1B and S2). Dearc sgiathanach is recovered within a large grade of nonmonofenestratans, including subclades centered on Rhamphorhynchus and Scaphognathus ( Figure 4 ). Dearc is in the former subclade, where it groups with the Chinese Angustinaripterus and Sericipterus , in the clade Angustinaripterini, diagnosed here for the first time by several features including a large antorbital fenestra, reclined quadrate, and proportionally elongate anterior cervicals (see above). Remarks The holotype of Dearc sgiathanach is a rare three-dimensionally preserved pterosaur from the Jurassic, which gives unique insight into the osteology, size, growth, and neuroanatomy of a basal non-monofenestratan. Its most remarkable attribute is its size: its wingspan was ca. 1.9–3.8 m, roughly the size of the largest flying birds today (e.g., wandering albatross), and it was not fully grown at death. Triassic and Jurassic pterosaurs have long been stereotyped as relatively small animals, constrained to wingspans of approximately 1.6–1.8 m or less over the first ca. 70 million years of their evolutionary history, 5 before becoming larger in the latest Jurassic or Early Cretaceous, culminating in airplane-sized giants like Quetzalcoatlus with 10-m wingspans. 5 A few tantalizing specimens have hinted at larger Jurassic pterosaurs, 36 – 38 but these are often limited to one or a few bones, which make body size estimations difficult. Dearc is the first Jurassic pterosaur whose wingspan can confidently be estimated at ca. 2.5 m or greater, based on a well-preserved, articulated skeleton. 5 Its closest relatives, Angustinaripterus and Sericipterus , are also sizeable for Jurassic species, with wingspans previously estimated at 1.6 1 –1.7 38 m extrapolated from patchy fossils. Our regression equations indicate larger wingspans for these taxa: ca. 2–3 m, which is still approximately 10% smaller than Dearc . Dearc , therefore, anchors a clade of large, long-snouted Jurassic non-monofenestratans: Angustinaripterini. 38 The large size of Dearc prompted us to re-examine fragmentary specimens from the Taynton Limestone, 39 an English unit that formed at the same general time as the Scottish Middle Jurassic deposits, in or along the margins of the same seaway. We identified 17 specimens—all single bones—that yield wingspan estimates of over 1.7 m based on our predictor formulas (above), including several that may have had wingspans of over 3.0 m. The discovery of Dearc , and our survey of Taynton specimens, reveals that Jurassic pterosaurs were capable of achieving considerably larger sizes than previously thought. Jurassic pterosaurs may still have been constrained in size— and certainly there is no evidence they approached the grandeur of giant Cretaceous pterodactyloids—but if so, that constraint was at a substantially greater wingspan than 1.6–1.8 m. 5 Trends in pterosaur size evolution, particularly the shift to increasingly larger species in the Cretaceous, have been interpreted in terms of two main hypotheses, which are not mutually exclusive: (1) advances in the pterodactyloid body plan allowed them to become larger and more efficient fliers than non-pterodactyloids, and (2) the diversification of birds (Avialae) may have driven latest Jurassic/Cretaceous pterosaurs into ever-larger size niches. 5 Our identification of Dearc demonstrates that non-pterodactyloids were able to grow to larger sizes by the Middle Jurassic, with some evidence for large pterosaurs back to the Early Jurassic, 37 tens of millions of years before birds underwent their adaptive Cretaceous radiation. 40 , 41 These size increases seemingly occurred too early for avialans, which are first definitively known from the Late Jurassic, to have been a direct cause. Alternatively, if there was pressure on pterosaurs to become larger, it may have started deep in the Jurassic and involved competition with unrecognized early avialans or other animals, 40 like non-avialan feathered dinosaurs or other pterosaurs. Not only is Dearc large, but it and its closest angustinaripterin relatives possess derived characters considered keystones of the pterodactyloid skull ‘‘module,’’ notably an elongate skull and inclined quadrate. Previous work has argued that the transition between non-pterodactyloids and pterodactyloids involved a nearly perfect modular shift, in which features of the skull changed together in a tightly integrated unit, followed by the body, limbs, and tail. 6 While we do not dispute the overarching modularity of the pterosaur skeleton, Dearc hints that some of the trademark ‘‘pterodactyloid’’ features convergently evolved in other groups, 42 perhaps due to feeding ecology or other factors. Yet the endocranial anatomy of Dearc is distinctly primitive, as it has the unflexed brain and smaller flocculus of basal pterosaurs 7 , 24 and not the transformed brain of pterodactyloids. Thus, it seems, non-pterodactyloids had a similar neuroanatomy regardless of body size. Our recognition of large Middle Jurassic pterosaurs exposes a taphonomic bias, to add to the already notoriously problematic record of pterosaurs. 43 , 44 There were fairly large pterosaurs in the Jurassic (wingspans> 1.8 m), but reasonably complete adult or near-mature skeletons are mostly lacking, for reasons unclear and worthy of further study. The Middle Jurassic age of Dearc adds to increasing evidence that this interval—once a frustrating gap in the pterosaur record—was in fact a dynamic time of diversification, in which a variety of basal taxa and early monofenestratan lineages 6 , 39 coexisted and occupied a range of environments, from open marine to lagoonal, nearshore to desert, around the world. We can now add larger taxa, with derived pterodactyloid-type skull characters, to that roster. As with dinosaurs 45 and mammals, 46 the Middle Jurassic was likely a vibrant time in pterosaur history, not a static and archaic prelude to a Cretaceous explosion of larger, 5 more disparate, 47 more efficient fliers. 20 With the dawn of the Cretaceous, however, the diverse non-monofenestratans disappeared, including larger ones with pterodactyloid convergences. This mystery remains to be solved.