Paleobiology and the Origins of Avian Flight

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BIOCHEMISTRY EVOLUTION Correction for “Streamlined analysis schema for high-throughput Correction for “Paleobiology and the origins of avian flight,” by identification of endogenous protein complexes,” by Anna John Ruben, which appeared in issue 7, February 16, 2009, of Malovannaya, Yehua Li, Yaroslava Bulynko, Sung Yun Jung, Yi Proc Natl Acad Sci USA (107:2733–2734; first published February Wang, Rainer B. Lanz, Bert W. O’Malley, and Jun Qin, which 9, 2010; 10.1073/pnas.0915099107). appeared in issue 6, February 9, 2010, of Proc Natl Acad Sci USA Due to a printer’s error, the first sentence of this Commentary (107:2431–2436; first published January 22, 2010; 10.1073/ appeared incorrectly and should read: “When interpreting the pnas.0912599106). paleobiology of long extinct taxa, new fossils, and reinterpretations The authors note that the following acknowledgments were of well-known fossils, sharply at odds with conventional wisdom omitted from the article: never seem to cease popping up.” The online version has been This work was supported in part by National Institutes of Health corrected. (NIH) Grant U19-DK62434, an NIH Nuclear Receptor Signaling Atlas (NURSA) grant (Proteomics Strand) (to B.W.O. and J.Q.), www.pnas.org/cgi/doi/10.1073/pnas.1001826107 NIH NURSA Collaborative Bridging Project Grant U19- DK62434 (to R.B.L.), and NIH Grant CA84199 (to J.Q.). IMMUNOLOGY

www.pnas.org/cgi/doi/10.1073/pnas.1001159107 Correction for “Activation state and intracellular trafficking contribute to the repertoire of endogenous glycosphinogolipids presented by CD1d,” by Karen Muindi, Manuela Cernadas, Gerald F. EVOLUTION M. Watts, Louise Royle, David C. A. Neville, Raymond A. Dwek, Correction for “Complete mitochondrial genome of a Pleisto- Gurdyal S. Besra, Pauline M. Rudd, Terry D. Butters, and Michael cene jawbone unveils the origin of polar bear,” by Charlotte B. Brenner, which appeared in issue 7, February 16, 2010, of Proc Lindqvist, Stephan C. Schuster, Yazhou Sun, Sandra L. Talbot, Natl Acad Sci USA (107:3052–3057; first published January 28, Ji Qi, Aakrosh Ratan, Lynn P. Tomsho, Lindsay Kasson, Eve 2010; 10.1073/pnas.0915056107). Zeyl, Jon Aars, Webb Miller, Ólafur Ingólfsson, Lutz Bachmann, The authors note that the title of their manuscript appeared and Øystein Wiig, which appeared in issue 11, March 16, 2010, of incorrectly. The title should instead appear as “Activation state Proc Natl Acad Sci USA (107:5053–5057; first published March 1, and intracellular trafficking contribute to the repertoire of en- 2010; 10.1073/pnas.0914266107). dogenous glycosphingolipids presented by CD1d.” The title has The authors note that, due to a printer’s error, on page 5054, been corrected online. Additionally, on page 3055, left column, right column, second paragraph, eighth line, “Within this clade, second paragraph, line 14, “However, the GM2 peak that was a we estimated the mean age of the split between the ABC bears prominent GSL glycan eluted from soluble mCD1d was not ob- and the polar bears to be 152 ky, and the mean age for all polar served in the mCD1d-TEV eluates (Figs. 2A and 4; Table 2)” bears as 134 ky, near the end of the Eemian interglacial period should instead appear as “However, the GM2 peak that was a and completely in line with the stratigraphically determined age prominent GSL glycan eluted from soluble mCD1d was not ob- of the Poolepynten subfossil (11),” should instead appear as served in the mCD1d-TEV eluates (Figs. 2B and 4; Table 2).” This “Within this clade, we estimated the mean age of the split be- error does not affect the conclusions of the article. tween the ABC bears and the polar bears to be 152 ky, and the www.pnas.org/cgi/doi/10.1073/pnas.1001448107 mean age for all polar bears as 134 ky, near the beginning of the Eemian interglacial period and completely in line with the stratigraphically determined age of the Poolepynten subfossil (11).” This error does not affect the conclusions of the article. This error has been corrected online and in print.

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6118 | PNAS | March 30, 2010 | vol. 107 | no. 13 www.pnas.org Downloaded by guest on September 29, 2021 COMMENTARY

Paleobiology and the origins of avian ﬂight

John Ruben1 Oregon State University, Corvallis, OR 97331

hen interpreting the paleobiology of long extinct taxa, W new fossils, and reinterpretations of well-known fossils, sharply at odds with conventional wisdom never seem to cease popping up. Given the vagaries of the fossil record, current notions of near resolution of many of the most basic questions about long-extinct forms should probably be regarded with caution. Even major aspects of the paleobiology of intensely studied, recently extinct taxa (<10,000 yrs.) remain un- resolved [e.g., the cause(s) of late Pleisto- cene large-mammal disappearances (1) and the lifestyles of specialized forms Fig. 1. Naturalist William Beebe’s hypothetical, intermediate gliding stage in the origin of birds and (sabre-tooths) (2)]. Little wonder then bird flight (modified from ref. 12). Beebe’s proposal appeared in 1915 (12) but was almost prescient in its that so fascinating a subject as the origins morphological similarity to the recently discovered Microraptor gui (11) and that animal’s likely tet- of birds and bird flight, both of which rapteryx gliding posture [see Alexander et al. (4)]. almost surely occurred more than 150 million years ago, have stirred such pub- apparent feathers, or feather-like struc- porting a trees-down origin for avian licly visible and intense, nearly century- tures, on a number of late Mesozoic Era flight. Given the nature of the contro- long, controversies (3). In this context, theropods (7). versy, perhaps it is not overly surprising perhaps the most hotly debated and fun- Concomitant with shifting conventional that the recently discovered Microraptor, damental issue relates to the origin of wisdom that birds were derived from cur- as well as Xu et al.’s interpretation of avian flight: Did proto-birds take to the sorial theropods, many late 20th century its tetrapteryx flight posture, is eerily air as arboreal gliders where gravity was authors, including John Ostrom, advo- ’ fl similar to naturalist William Beebe s the primary source of ying energy (from cated a cursorial, or ground-upward (as “ ” 1915 hypothetical tetrapteryx stage in the trees-down ), or as swift, cursorial opposed to a trees–down), origin for fl “ the origin of avian ight (Fig. 1) (12). ground dwellers (from the ground- powered flight in birds (8). Throughout ” Nevertheless, advocates for a cursorial, upward )? In PNAS, Alexander et al. (4) this period, skeptics pointed to substantial “ ” “ ground-upward origin ( aerial cursors )for describe results of a novel paleobio- aerodynamic difficulties associated with ” avian flight remain. They assert that hin- logical study: three-dimensional model- the cursorial, ground-upward hypothesis fl Microraptor based, empirical data that provide im- dlimb ight feathers in were (9). Nevertheless, by the beginning of this somehow oriented in such a manner that portant insight into this old question. century, extant birds were described, in fi interference with running would have been Although an af nity between theropod many scientific and lay communities, as fl dinosaurs and birds has long been recog- “ ” minimized. Supposedly, ight in a cursorial living dinosaurs, and the ground-upward Microraptor would necessarily have been nized, for most of the 20th century, pale- scenario had, in many circles, become ac- biplane-like, wherein the hindlimb wings/ ontologists generally accepted that an cepted wisdom (10). feathers (but not the skeleton) would ancestor–descendant relationship Not so fast. In 2003, Xu et al. (11) have been horizontally situated, but well between these groups was unlikely (3). described a fully feathered specimen of below and somewhat behind those of Among the traits distinguishing the two the small basal dromaeosaur Microraptor taxa, the earliest known bird, Archae- that bore four wings of fully modern, the forelimb (13). opteryx (Late Jurassic Period, ≈150 m.y.), fl Clearly, these two interpretations of asymmetrical ight feathers on its fore- Microraptor seemed to have been primarily arboreal; limbs and legs. As Xu stated: The meta- are broadly at odds with one known theropods were exclusively curso- another and imply profoundly different tarsus [hindlimb] feathers are inconsistent fl rial. Avian flight was widely thought to with the suggestions that basal dromaeo- scenarios for the origin of avian ight. have originated in gliding, arboreal proto- saurs are cursorial animals because such Given that direct observation of living Microraptor birds (i.e., the trees-down scenario). long feathers on the feet would be a hin- is not on the horizon, That accepted wisdom was turned on its drance for a small cursorial animal. It is Alexander et al. (4) present results from head in the 1970s when Yale’s John Os- unlikely that a small dromaeosaur could what is probably the best available ap- trom reanalyzed the skeletons of Archae- run fast with such an unusual integument proach to provide some empirical opteryx and the cursorial dromeosaurine and this provides negative evidence for the resolution to this question: Glide tests theropods (“raptors”) (5). He concluded ground-up hypothesis for the origin of were performed by using three- that, in fact, birds were closely related to avian flight. Xu et al. reconstructed limbs dimensional life-size scale models on the theropod dinosaurs and were more or of four-winged Microraptor as tandem less directly derived from the raptors. wings like those of insects and gliding fish Thereafter, Ostrom’s scenario for avian where, during flight, all wings are Author contributions: J.R. wrote the paper. origins was bolstered by cladistic analyses spread horizontally in a “tetrapteryx” The author declares no conflict of interest. consistent with a dromaeosaur-bird line- fashion. They concluded that Microraptor See companion article on page 2972. 1 age (6) and with the discovery of was probably a tree-dweller, thus sup- E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.0915099107 PNAS | February 16, 2010 | vol. 107 | no. 7 | 2733–2734 skeleton of one individual that had model, it required an anatomically un- suggest that many clearly cursorial been prepared “in the round.” Glide likely, especially massive, and ungainly theropods previously thought to have tests of the model were conducted with head for aerodynamic stability. been feathered may not have been so hindwings abducted and extended So, is the answer, after all, a hybrid (14) and that dromaeosaurs, the laterally (tetrapteryx), as well as with the of the two old theories, i.e., avian group that birds are assumed to have previously described biplane config- origins from an arboreal, gliding been derived from, may not even uration. Although the biplane theropod dinosaur? Perhaps, but then have been dinosaurs (15). What pops up model glided almost as well as the other this is paleobiology—very recent data next is anyone’s guess.

1. Barnosky AD, Koch PL, Feranec RS, Wing SL, Shabel AB 6. Gauthier JA (1986) Saurischian monophyly and the ori- 12. Beebe CW (1915) A tetrapteryx stage in the ancestry of (2004) Assessing the causes of late pleistocene extinc- gin of birds. Mem Calif Acad Sci 8:1–55. birds. Zoologica 2:38–52. tions on the continents. Science 306:70–75. 7. Norrell MA, Xu X (2005) Feathered dinosaurs. Annu 13. Chatterjee S, Templin RJ (2007) Biplane wing planform 2. Slater GJ, Valkenburgh BV (2008) Long in the tooth: Rev Earth Planet Sci 33:277–299. and flight performance of the feathered dinosaur Mi- Evolution of sabertooth cat cranial shape. Paleobiology 8. Ostrom JA (1979) Bird flight: How did it begin? Am Sci croraptor gui. Proc Natl Acad Sci USA 104:1576–1580. – 34:403 419. 67:46–56. 14. Lingham-Soliar T, Feduccia A, Wang X (2007) A new Chi- 3. Feduccia A (1999) The Origin and Evolution of Birds 9. Norberg U (1990) Vertebrate Flight: Mechanics, Physi- nese specimen indicates that ‘protofeathers’ in the early (Yale Univ Press, New Haven, CT), p 466. Cretaceous theropod dinosaur Sinosauropteryx are de- 4. Alexander DE, Gong E, Martin LD, Burnham DA, Falk AR ology, Morphology, Ecology and Evolution. Zoophysi- fi (2010) Model tests of gliding with different hindwing con- ology Series (Springer, New York), Vol 27, p 298. graded collagen bers. Proc R Soc Lond B Biol Sci 274: – figurations in the four-winged dromaeosaurid, Microrap- 10. Pough FH, Janis CM, Heiser JB (2009) Vertebrate Life 1823 1829. tor gui. Proc Natl Acad Sci USA 107:2972–2976. (Pearson Benjamin Cummings, San Francisco), p 688. 15. James FC, Pourtless JA IV (2009) Cladistics and the origin of 5. Ostrom JH (1976) Archaeopteryx and the origin of 11. Xu X, et al. (2003) Four-winged dinosaurs from China. birds: A review and two new analyses. Ornithol Monogr birds. Biol J Linn Soc 8:91–182. Nature 421:335–340. 66:1–78.

2734 | www.pnas.org/cgi/doi/10.1073/pnas.0915099107 Ruben