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Science Journals — AAAS RESEARCH ◥ Such adaptations enable distinctive foraging REPORT strategies such as the use of precise sound localization and low-light (scotopic) vision in PALEONTOLOGY the barn owl (Tyto alba), which can hunt in complete darkness (5). These sensory adap- Evolution of vision and hearing modalities in tations leave clear skeletal signatures that should be evident in fossils. Nevertheless, theropod dinosaurs sensory evolution in birds and their theropod stem lineage is poorly understood [but see, Jonah N. Choiniere1†, James M. Neenan1,2†, Lars Schmitz3,4, David P. Ford1, e.g., (6–9)].Thisisasubstantialshortcom- Kimberley E. J. Chapelle1,5, Amy M. Balanoff5,6, Justin S. Sipla7, Justin A. Georgi8, Stig A. Walsh9,10, ing in our understanding of dinosaurian Mark A. Norell5, Xing Xu11,12, James M. Clark13, Roger B. J. Benson1,14* biology and of the structure of Mesozoic ecosystems. Owls and nightbirds are nocturnal hunters of active prey that combine visual and hearing adaptations to To evaluate the evolution of vison and hear- overcome limits on sensory performance in low light. Such sensory innovations are unknown in nonavialan ing in extinct theropods, we studied skeletal theropod dinosaurs and are poorly characterized on the line that leads to birds. We investigate proxies for two sensory systems: the scleral morphofunctional proxies of vision and hearing in living and extinct theropods and demonstrate deep ossicle ring (hereafter “scleral ring”)oftheeye evolutionary divergences of sensory modalities. Nocturnal predation evolved early in the nonavialan lineage for vision and the endosseous cochlear duct Alvarezsauroidea, signaled by extreme low-light vision and increases in hearing sensitivity. The Late Cretaceous of the bony labyrinth for hearing. The scleral alvarezsauroid Shuvuuia deserti had even further specialized hearing acuity, rivaling that of today’s barn ring is embedded in the eyeball surface in owl. This combination of sensory adaptations evolved independently in dinosaurs long before the numerous living and extinct amniotes. Noc- Downloaded from modern bird radiation and provides a notable example of convergence between dinosaurs and mammals. turnal species typically have wider ring aper- tures, reflecting larger pupil sizes that increase light sensitivity (9). The endosseous cochlear ensory specializations are some of the bling in some water birds, require limited sen- duct is intimately linked to hearing perform- most distinctive vertebrate innovations sory anatomical changes (3). However, most ance (e.g., sensitivity and frequency range) be- (1, 2) and are common as adaptations nocturnal birds have conspicuous modifica- cause it houses the basilar papilla or cochlea http://science.sciencemag.org/ S to low-light activity in birds and mam- tions of the visual system, and specialized (10). The elongate mammalian cochlea has mals. Facultative nocturnal behaviors of nocturnal foragers ofactivepreycombine been an area of continued evolutionary in- living birds, such as tactile probing and dab- adaptations of both vision and hearing (4). novation [e.g., (11, 12)], demonstrating the ABC 0.6 Caprimulgus cayennensis Gekko †Haplocheirus gecko Steatornis †Shuvuuia caripensis Aegotheles on May 16, 2021 cristatus †Megapnosaurus 0.4 Micropsitta finschii 4mm 40mm †Velociraptor Tyto alba D E †Ornithomimus optic ratio Coturnix coturnix †Lufengosaurus 0.2 Anolis sagrei †Archaeopteryx †Riojasaurus †Psittacosaurus of nocturnal vision †Prosaurolophus Increasing probability †Diplodocus living birds Phrynosoma †Erlikosaurus living mcallii squamates 0.0 fossils 4mm 40mm 0.0 0.5 1.0 geometric mean Fig. 1. Optic ratio by geometric mean of optic measurements for living birds, squamates, and nonavialan theropods. (A) Scatterplot of optic ratio versus geometric mean of orbit and scleral ring measurements for extant birds and reptiles and extinct species. See data S3. (B to E) Scleral ossicle ring anatomy in (B) Aegotheles cristatus, (C) H. sollers, (D) Micropsitta finchii, and (E) Erlikosaurus andrewsi (29). Blue indicates nocturnality, green indicates non-nocturnality, and color gradient indicates the posterior probability of nocturnality (data S3) (19). † indicates extinct species. 1Evolutionary Studies Institute, University of the Witwatersrand, 1 Jan Smuts Avenue, Johannesburg 2000, South Africa. 2Oxford University Museum of Natural History, University of Oxford, Parks Road, Oxford OX1 3PW, UK. 3W.M. Keck Science Department, Claremont McKenna, Scripps, and Pitzer Colleges, 925 N Mills Ave., Claremont, CA 91711, USA. 4Dinosaur Institute, Los Angeles County Museum of Natural History, 900 Exposition Boulevard, Los Angeles, CA 90007, USA. 5Division of Paleontology, American Museum of Natural History, Central Park West at 79th Street, New York, NY 10024, USA. 6Department of Psychological and Brain Sciences, Johns Hopkins University, 3400 North Charles St., Baltimore, MD 21218, USA. 7Department of Anatomy and Cell Biology, Carver College of Medicine, University of Iowa, 51 Newton Road, 100 Bowen Science Building, Iowa City, IA 52242, USA. 8Department of Anatomy, College of Graduate Studies, Midwestern University, 19555 N 59th Avenue, Glendale, AZ 85308, USA. 9Department of Natural Sciences, National Museums Scotland, Chambers Street, Edinburgh EH1 1JF, UK. 10School of Geosciences, University of Edinburgh, Grant Institute, Hutton Road, Edinburgh EH9 3FE, UK. 11Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, 142 Xizhimenwai Street, Beijing 100044, China. 12Chinese Academy of Sciences Center for Excellence in Life and Paleoenvironment, Beijing 100044, China. 13Department of Biological Sciences, The George Washington University, 2029 G St. NW, Washington, DC 20052, USA. 14Department of Earth Sciences, University of Oxford, South Parks Road, Oxford OX1 3AN, UK. †These authors contributed equally to this work. *Corresponding author. Email: [email protected] Choiniere et al., Science 372, 610–613 (2021) 7 May 2021 1of4 RESEARCH | REPORT importance of hearing in their foraging strat- AB C egies. Bird species that rely on auditory cues skr for foraging, such as owls, have an elongate fm endosseous cochlear duct, alongside other ana- eor tomical modifications (13). oc Our analyses show visual and auditory ad- bcf aptations to nocturnality in alvarezsauroids, sbl an enigmatic theropod lineage that spanned the Late Jurassic to Late Cretaceous. Early branching alvarezsauroids, such as Haplocheirus sollers, retain generalized theropod features that suggest a relatively unspecialized pred- †Shuvuuia deserti atory ecology (14). However, late-branching alvarezsauroids such as Shuvuuia deserti have a curious mixture of derived traits, including D E F birdlike skulls, cursorial hindlimbs, and short, skr functionally monodactyl forelimbs interpreted as adaptations for scratch digging (15, 16). These features are the source of continued eor speculation and debate about alvarezsauroid paleoecology (15–18). fm Downloaded from oc sbl Our digital reconstructions of the scleral rings of the alvarezsauroids Haplocheirus and bcf Shuvuuia show a proportionally large eye with an extremely wide aperture (Fig. 1 and figs. S1 Tyto alba to S5) (19). Phylogenetic flexible discriminant analysis of the scleral ring and orbit morphol- Fig. 2. Comparative anatomy of the endosseous cochlear duct of S. deserti (uncrushed adult http://science.sciencemag.org/ ogy, extended from previous analyses (9), has a specimen IGM100/1304) and the extant barn owl T. alba. (A to C) S. deserti uncrushed adult mean accuracy of 92.0% for the classification of specimen (IGM100/1304). (D to F) Extant barn owl T. alba. (A and D) Posterior views of braincases extant species as nocturnal or non-nocturnal. showing external anatomy. (B and E) Transparent CT renderings of braincase in posterior view, Among theropods, the highest posterior prob- showing endosseous labyrinths. (C and F) Digital reconstructions of the endosseous labyrinths in lateral abilities for nocturnal vision (ppnocturnal) are view.Scalebars,5mm(BandE)and2.5mm(CandF).bcf,braincasefloor;eor,externaloticregion; for Haplocheirus (ppnocturnal > 0.99), Shuvuuia fm, foramen magnum; oc, occipital condyle; sbl, secondary bony lamina; skr, skull roof. † indicates (ppnocturnal > 0.87), and the coelophysoid extinct species. Megapnosaurus (ppnocturnal > 0.99) (Fig. 1 and table S1). These have morphologies similar to those of birds that have specialized low- light visual systems (Fig. 1) but are differ- birds corroborates our interpretation of rela- secondarily herbivorous Therizinosauria; and in on May 16, 2021 ent from those of other theropods, including tive duct elongation as related to nocturnality alvarezsauroids, including the Jurassic to Early many for which nocturnality was previous- and other foraging traits (Fig. 3, table S2, and Cretaceous taxa Haplocheirus and Xiyunykus ly inferred at a much less stringent prob- figs. S6 to S10) (19). Owls (Strigiformes); large- (Fig. 3). The barn owl (T. alba), Shuvuuia ,and ability threshold (ppnocturnal >ppdiurnal and bodied, nocturnal Strisores (e.g., owlet night- an undescribed troodontid [Mongolian Institute ppcathemeral)(6). jars, pootoos, frogmouths, and the echolocating for Geology (IGM) 100/1126] are outliers that Micro–computed tomography (CT) reveals oilbird); and some other taxa have moderately demonstrate auditory specialization, even com- anatomical specialization of the endosseous or greatly elongated ducts (Fig. 3), whereas pared with
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