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New Tyrannosaur from the Mid-Cretaceous of Uzbekistan Clarifies Evolution of Giant Body Sizes and Advanced Senses in Tyrant Dinosaurs

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New Tyrannosaur from the Mid-Cretaceous of Uzbekistan Clarifies Evolution of Giant Body Sizes and Advanced Senses in Tyrant Dinosaurs New tyrannosaur from the mid-Cretaceous of Uzbekistan clarifies evolution of giant body sizes and advanced senses in tyrant dinosaurs Stephen L. Brusattea,1, Alexander Averianovb,c, Hans-Dieter Suesd, Amy Muira, and Ian B. Butlera aSchool of GeoSciences, University of Edinburgh, Edinburgh EH9 3FE, United Kingdom; bZoological Institute, Russian Academy of Sciences, St. Petersburg 199034, Russia; cDepartment of Sedimentary Geology, Saint Petersburg State University, St. Petersburg 199178, Russia; and dDepartment of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20560 Edited by Neil H. Shubin, The University of Chicago, Chicago, IL, and approved January 29, 2016 (received for review January 5, 2016) Tyrannosaurids—the familiar group of carnivorous dinosaurs in- We here report the first diagnostic tyrannosauroid from the mid- cluding Tyrannosaurus and Albertosaurus—were the apex predators Cretaceous, a new species from the Turonian (ca. 90–92 million in continental ecosystems in Asia and North America during the years ago) Bissekty Formation of Uzbekistan. This formation has latest Cretaceous (ca. 80–66 million years ago). Their colossal sizes recently emerged as one of the most important records of mid- and keen senses are considered key to their evolutionary and eco- Cretaceous dinosaurs globally (9–11). Possible tyrannosauroid logical success, but little is known about how these features devel- specimens from the Bissekty Formation were reported more than oped as tyrannosaurids evolved from smaller basal tyrannosauroids a half century ago (12), and, more recently, several isolated fossils that first appeared in the fossil record in the Middle Jurassic (ca. 170 were assigned to the group (9, 13), but none of these has been million years ago). This is largely because of a frustrating 20+ million- particularly complete or diagnostic at the species level, and their year gap in the mid-Cretaceous fossil record, when tyrannosauroids phylogenetic relationships have been difficult to assess. We de- transitioned from small-bodied hunters to gigantic apex predators scribe a remarkably preserved and highly diagnostic braincase that but from which no diagnostic specimens are known. We describe the links together these specimens and reveals the existence of a mid- first distinct tyrannosauroid species from this gap, based on a highly sized species phylogenetically intermediate between the oldest, derived braincase and a variety of other skeletal elements from the smallest tyrannosauroids and the largest, last-surviving tyran- ca. – Turonian ( 90 92 million years ago) of Uzbekistan. This taxon is phy- nosaurids, which had already developed many of the apomorphic logenetically intermediate between the oldest basal tyrannosauroids features of the tyrannosaurid brain and ear but not the cranial and the latest Cretaceous forms. It had yet to develop the giant size sinus system. and extensive cranial pneumaticity of T. rex and kin but does possess the highly derived brain and inner ear characteristic of the latest Systematic Paleontology Cretaceous species. Tyrannosauroids apparently developed huge Dinosauria Owen, 1842; Theropoda Marsh, 1881; Coelurosauria size rapidly during the latest Cretaceous, and their success in the Huene, 1914; Tyrannosauroidea Osborn, 1905; Timurlengia euotica top predator role may have been enabled by their brain and keen EARTH, ATMOSPHERIC, gen. et sp. nov. AND PLANETARY SCIENCES senses that first evolved at smaller body size. Holotype dinosaur | Tyrannosauroidea | Uzbekistan | phylogenetics | evolution ZIN PH (Paleoherpetological Collection, Zoological Institute, Russian Academy of Sciences, Saint Petersburg, Russia) 1146/16, yrannosaurs were at their heyday during the final ∼20 million a well-preserved braincase missing only the paroccipital processes years of the Age of Dinosaurs. Iconic taxa like Tyrannosau- T and much of the parabasisphenoid (Figs. 1 and 2 and Figs. S1−S3). EVOLUTION rus, Tarbosaurus, and Albertosaurus reigned at the top of the food chain in Asia and North America, endowed with colossal size Significance and sophisticated senses that set them apart from other carniv- orous dinosaurs (1, 2). These multiton, ecologically dominant Tyrannosaurs—the iconic group of dinosaurian carnivores that latest Cretaceous species (tyrannosaurids) evolved from an an- Tyrannosaurus rex— cestral lineage of basal tyrannosauroids, which originated more includes dominated latest Cretaceous than 100 million years before T. rex but for most of their history ecosystems with their colossal sizes and sophisticated senses. A gap in the mid-Cretaceous fossil record between these giant remained second-tier predators, rarely with a mass exceeding apex predators and their older, smaller relatives makes it dif- that of a horse (2–4). The ascent of tyrannosaurs from these early ficult to understand how the characteristic body size and eco- species to the latest Cretaceous giants was one of the seminal logical habits of T. rex and kin developed. A new species from events in dinosaur evolution, establishing the final dinosaur- Uzbekistan fills this gap. This horse-sized animal shows that dominated faunas that flourished before the end-Cretaceous tyrannosaurs had yet to achieve huge size at this time but had mass extinction (5). already evolved key brain and sensory features of the gigantic Little is known, however, about how tyrannosaurids developed latest Cretaceous species. Tyrannosaurs apparently developed many of their signature features, such as their gigantic sizes, giant body size rapidly, late in the Cretaceous, and their success highly unusual brains, ears attuned to low-frequency sounds, and may have been enabled by their early-evolving keen senses. extensively pneumatized skulls. This is due to a vexing gap in the fossil record that has long frustrated attempts to understand ty- Author contributions: S.L.B., A.A., and H.-D.S. designed research; S.L.B., A.A., H.-D.S., A.M., rannosaur evolution. There are hundreds of specimens of large- and I.B.B. performed research; S.L.B. contributed new reagents/analytic tools; S.L.B., A.M., bodied latest Cretaceous tyrannosaurids (1), and now a growing and I.B.B. analyzed data; and S.L.B., A.A., and H.-D.S. wrote the paper. record of smaller and more primitive Middle Jurassic−Early Cre- The authors declare no conflict of interest. taceous tyrannosauroids (2, 6–8). However, there are no diagnostic This article is a PNAS Direct Submission. fossils from the intervening 20+ million years of the mid-Cretaceous, 1To whom correspondence should be addressed. Email: [email protected]. the time when tyrannosauroids transitioned from marginal hunters This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. to apex predators (1, 2). 1073/pnas.1600140113/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1600140113 PNAS | March 29, 2016 | vol. 113 | no. 13 | 3447–3452 Downloaded by guest on October 1, 2021 Fig. 1. Skeletal reconstruction of T. euotica, with known bones colored in red. Individual bones come from different individuals, as they were surface- collected as isolated specimens in the Bissekty Formation of Uzbekistan. The proportions of the skeleton are based on an intermediate body type between Xiongguanlong and Tyrannosaurus but should be considered provisional until associated material is found. Bones are as follows: A, left frontal, ZIN PH 2330/ 16; B, holotypic braincase, ZIN PH 1146/16; C, cervical vertebra, ZIN PH 671/16; D, cervical vertebra, USNM (National Museum of Natural History) 538131; E, dorsal neural arch, USNM 538132; F, dorsal vertebra, CCMGE (Chernyshev’s Central Museum of Geological Exploration) 432/12457; G, anterior caudal ver- tebra, ZIN PH 951/16; H, middle caudal vertebra, ZIN PH 120/16; I, distal caudal vertebra, ZIN PH 507/16; J, pedal ungual, USNM 538167; K, manual ungual,ZINPH 619/16; L, right articular and surangular (reversed), ZIN PH 1239/16; M, left quadrate, ZIN PH 2296/16; N, right dentary, ZIN PH 15/16; and O, right maxilla (reversed), ZIN PH 676/16. (Individual scale bars, 2 cm.) Skeletal drawing courtesy of Todd Marshall. Etymology Body Size Timurlengia, in reference to the fourteenth-century Central Asian The holotypic braincase of T. euotica is nearly identical in size to ruler Timurleng (English: Tamerlane), and euotica, meaning “well- that of the holotype of Xiongguanlong baimoensis (based on eared” in reference to the large inner ear of the holotype. nearly equal widths of the occipital condyle and supraoccipital above the foramen magnum, and depth of the proximal end of Referred Specimens the paroccipital process). Along with the phylogenetic proximity ZIN PH 854/16 is the right side of a partial braincase that shares of the two taxa, this suggests that the holotypic individual of unique apomorphies with, and is otherwise identical to, the ho- T. euotica was roughly the same body size as Xiongguanlong, lotype (Fig. S4). We also refer to T. euotica a series of isolated whose mass has been estimated at 170–270 kg (14, 15). Al- cranial and postcranial bones described by Averianov and Sues though most sutures on the holotype of T. euotica are fused, part (9) and identified as belonging to indeterminate tyrannosauroids of the broken parabasisphenoid was not fused to the remainder (Fig. 1). These bones possess tyrannosauroid characters, are of the braincase, perhaps suggesting that the individual was not from the same horizon as the holotype of T. euotica, and belong yet osteologically mature and adults of the species may have to individuals of approximately the same body size. Furthermore, been somewhat larger. However, almost all other tyrannosau- separate phylogenetic analyses place the braincase and the series roid specimens from the Bissekty Formation are of the same of additional bones in the same position as an “intermediate”- size, or smaller, than corresponding bones in the holotype of grade tyrannosauroid (see Systematics). We therefore consider it X. baimoensis (9). The one possible exception is a fragment of most parsimonious that all of these specimens belong to the the posterior end of the lower jaw that was described as be- same taxon.
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