Article Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds Graphical Abstract Authors Rui Pei, Michael Pittman, Pablo A. Goloboff, ..., Mark A. Norell, Stephen L. Brusatte, Xing Xu Correspondence [email protected] In Brief Pei et al. use an updated phylogeny of early birds and their closest relatives to reconstruct powered flight potential, showing it evolved at least three times. Many ancestors of the closest bird relatives neared thresholds of powered flight potential, suggesting broad experimentation with wing-assisted locomotion before theropod flight evolved. Highlights d Support Deinonychosauria as sister taxon to birds and Anchiornithinae as early birds d Powered flight potential evolved R3 times: once in birds and twice in dromaeosaurids d Many ancestors of bird relatives neared thresholds of powered flight potential d Broad experimentation with wing-assisted locomotion before theropod flight evolved Pei et al., 2020, Current Biology 30, 1–14 October 5, 2020 ª 2020 The Author(s). Published by Elsevier Inc. https://doi.org/10.1016/j.cub.2020.06.105 ll Please cite this article in press as: Pei et al., Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds, Current Biology (2020), https://doi.org/10.1016/j.cub.2020.06.105 ll OPEN ACCESS Article Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds Rui Pei,1,10 Michael Pittman,2,10,11,* Pablo A. Goloboff,3 T. Alexander Dececchi,4 Michael B. Habib,5 Thomas G. Kaye,6 Hans C.E. Larsson,7 Mark A. Norell,8 Stephen L. Brusatte,9 and Xing Xu1 1Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology & Paleoanthropology, Chinese Academy of Sciences, Beijing 100044, China 2Vertebrate Palaeontology Laboratory, Division of Earth and Planetary Science, The University of Hong Kong, Pokfulam, Hong Kong SAR, China 3Unidad Ejecutora Lillo, Consejo Nacional de Investigaciones Cientı´ficas yTecnicas (CONICET), Tucuma´ n, Tucuma´ n, Argentina 4Division of Natural Sciences, Mount Marty College, Yankton, SD 57078, USA 5Dinosaur Institute, Natural History Museum of Los Angeles County, Los Angeles, CA 90007, USA 6Foundation for Scientific Advancement, Sierra Vista, AZ 85650, USA 7Redpath Museum, McGill University, Montreal, QC H3A 0C4, Canada 8Division of Paleontology, American Museum of Natural History, New York City, NY 10024, USA 9School of Geosciences, University of Edinburgh, Edinburgh EH9 3FE, UK 10These authors contributed equally 11Lead Contact *Correspondence: [email protected] https://doi.org/10.1016/j.cub.2020.06.105 SUMMARY Uncertainties in the phylogeny of birds (Avialae) and their closest relatives have impeded deeper understand- ing of early theropod flight. To help address this, we produced an updated evolutionary hypothesis through an automated analysis of the Theropod Working Group (TWiG) coelurosaurian phylogenetic data matrix. Our larger, more resolved, and better-evaluated TWiG-based hypothesis supports the grouping of dromaeosaurids + troodontids (Deinonychosauria) as the sister taxon to birds (Paraves) and the recovery of Anchiornithinae as the earliest diverging birds. Although the phylogeny will continue developing, our cur- rent results provide a pertinent opportunity to evaluate what we know about early theropod flight. With our results and available data for vaned feathered pennaraptorans, we estimate the potential for powered flight among early birds and their closest relatives. We did this by using an ancestral state reconstruction analysis calculating maximum and minimum estimates of two proxies of powered flight potential—wing loading and specific lift. These results confirm powered flight potential in early birds but its rarity among the ancestors of the closest avialan relatives (select unenlagiine and microraptorine dromaeosaurids). For the first time, we find a broad range of these ancestors neared the wing loading and specific lift thresholds indicative of pow- ered flight potential. This suggests there was greater experimentation with wing-assisted locomotion before theropod flight evolved than previously appreciated. This study adds invaluable support for multiple origins of powered flight potential in theropods (R3 times), which we now know was from ancestors already nearing associated thresholds, and provides a framework for its further study. INTRODUCTION avian-like sleeping posture [24]. As a result of these advances, the origin of birds has emerged as one of the best documented ex- The origin of birds (Avialae) and modern powered flapping flight amples of a major macroevolutionary transition. Despite the exten- were iconic events in the history of life. Recent studies of early birds sive array of new specimens and data, the phylogenetic relation- and their closest dinosaurian relatives (non-avialan paravian thero- ships within and between paravian clades have been challenging pods) have provided key insights into this major evolutionary tran- to reconstruct, and uncertainties continue to present obstacles to- sition. It is now clear that anatomies and behaviors traditionally ward reaching consensus and improving resolution at important associated with birds were first acquired by non-avialan dinosaurs nodes. before the origin of birds and modern powered flapping flight. Traditionally, dromaeosaurids and troodontids were united These include smaller body size, accelerated evolutionary rates together as the Deinonychosauria by the ‘‘sickle claw’’ of their [1–3], early feathers of ‘‘modern’’ aspect [4–17], complex plumage second toe and other characters [2, 25–28]. They were consid- coloration, flapping-based locomotion, non-powered flight capa- ered the sister group of birds and were altogether known as bilities (among some non-avialan paravians; M. Habib, et al., the Paraves [2, 25–28]. The rapid discovery of paravian species 2012, Geol. Assoc. Can., abstract) [18–22, 23], and even an over the last decade [13, 14, 17, 28–32], especially from East Current Biology 30, 1–14, October 5, 2020 ª 2020 The Author(s). Published by Elsevier Inc. 1 This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Please cite this article in press as: Pei et al., Potential for Powered Flight Neared by Most Close Avialan Relatives, but Few Crossed Its Thresholds, Current Biology (2020), https://doi.org/10.1016/j.cub.2020.06.105 ll OPEN ACCESS Article Asia, has called this into question. Most notably, many of the his- more analytical iterations can be made in the same time as a torically diagnostic features of Dromaeosauridae, Troodontidae, handful of manual analyses would take. We hope this automated and Deinonychosauria are now recognized as synapomorphies analytical pipeline can increase our community’s access to more of more inclusive theropod groups (e.g., Maniraptora) or in in-depth parsimony-based analyses. some cases appear to have been acquired convergently in We use our more resolved and better evaluated TWiG-based different taxa. The number of evolutionary hypotheses has phylogeny to infer when and how the potential for powered flight grown with these new fossil discoveries [1, 2, 4, 13, 14, 28, 30, developed in early birds and their closest relatives. Previous 32–37]. They now encompass a range of possible interrelation- work has proposed that powered theropod flight evolved once ships between birds and other paravians, even challenging the or maybe even multiple times [18, 41, 42]. It has even been sug- monophyly of Deinonychosauria and the composition of stem gested that birds should be defined by the possession of flight avialans [4, 13, 33–35, 38]. A primary issue concerns troodon- alone, as an apomorphic feature [43]. With the phylogenetic tids, which have been grouped with either dromaeosaurids [2, placement of the iconic early bird Archaeopteryx with Deinony- 4, 28, 32, 33] as the traditional Deinonychosauria or with Avialae chosauria, a single origin of powered flight has been proposed [13, 14, 34, 35] exclusive of dromaeosaurids. Each phylogenetic at Paraves, polarizing the evolution of proportionally longer and hypothesis has different implications on the origin of birds and more robust arms at that node [4]. However, the wing and the morphological, biomechanical, and ecological states of their body dimensions of many early-diverging paravians do not sur- transitional antecedents. pass the minimal thresholds for flight ability [18] as defined in We contribute toward addressing these prevailing phyloge- modern birds and other taxa [44–46]. A quantitative study found netic issues by presenting an updated parsimony-based recon- that non-volant flapping-based locomotion was confined to Par- struction of paravian interrelationships by using the large coe- aves: flap running, wing-assisted incline running (WAIR), and lurosaurian theropod phylogenetic dataset of the Theropod wing-assisted leaping [18]. In showing that this was optimized Working Group (TWiG), produced by a long-standing consortium at Paraves and that significant capabilities were derived inde- of international theropod experts [1] (and references therein). Up- pendently in microraptorine dromaeosaurids and avialans [18], dated with recently discovered taxa, our expanded version of the that study supported the potential for multiple origins of powered TWiG dataset includes nine new dromaeosaurid terminal taxa flight in theropods. However, that study was restricted by a prob- (Acheroraptor, Changyuraptor,