Phylogenomic evidence for multiple losses of flight in ratite birds
John Harshman a,b,c, Edward L. Braun d,e,c, Michael J. Braun f,g,c, Christopher J. Huddleston f, Rauri C. K. Bowie a,h,i, Jena L. Chojnowski d, Shannon J. Hackett a, Kin-Lan Han d,f,g, Rebecca T. Kimball d, Ben D. Marks j, Kathleen J. Miglia k, William S. Moore k, Sushma Reddy a, Frederick H. Sheldon j, David W. Steadman l, Scott J. Steppan m, Christopher C. Witt j,n, and Tamaki Yuri d,f
aZoology Department, Field Museum of Natural History, 1400 South Lakeshore Drive, Chicago, IL 60605;
b4869 Pepperwood Way, San Jose, CA 95124;
dDepartment of Zoology, University of Florida, Gainesville, FL 32611;
fDepartment of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, 4210 Silver Hill Road, Suitland, MD 20746;
gBehavior, Ecology, Evolution, and Systematics Program, University of Maryland, College Park, MD 20742;
hMuseum of Vertebrate Zoology and Department of Integrative Biology, University of California, Berkeley, CA 94720;
iDepartment of Science and Technology/National Resource Foundation Centre of Excellence at the Percy FitzPatrick Institute, Department of Botany and Zoology, Stellenbosch University, Matieland 7602, South Africa;
jMuseum of Natural Science, 119 Foster Hall, Louisiana State University, Baton Rouge, LA 70803;
kDepartment of Biological Sciences, Wayne State University, 5047 Gullen Mall, Detroit, MI 48202;
lFlorida Museum of Natural History, University of Florida, Gainesville, FL 32611;
mDepartment of Biological Science, Florida State University, Tallahassee, FL 32306; and
nDepartment of Biology and Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM 87131
Edited by Morris Goodman, Wayne State University School of Medicine, Detroit, MI, and approved July 17, 2008
cJ.H., E.L.B., and M.J.B. contributed equally to this work. (received for review April 2, 2008)
Ratites (ostriches, emus, rheas, cassowaries, and kiwis) are large, flightless birds that have long fascinated biologists. Their current distribution on isolated southern land masses is believed to reflect the breakup of the paleocontinent of Gondwana. The prevailing view is that ratites are monophyletic, with the flighted tinamous as their sister group, suggesting a single loss of flight in the common ancestry of ratites. However, phylogenetic analyses of 20 unlinked nuclear genes reveal a genome-wide signal that unequivocally places tinamous within ratites, making ratites polyphyletic and suggesting multiple losses of flight. Phenomena that can mislead phylogenetic analyses, including long branch attraction, base compositional bias, discordance between gene trees and species trees, and sequence alignment errors, have been eliminated as explanations for this result. The most plausible hypothesis requires at least three losses of flight and explains the many morphological and behavioral similarities among ratites by parallel or convergent evolution. Finally, this phylogeny demands fundamental reconsideration of proposals that relate ratite evolution to continental drift.
convergence, flightlessness, Paleognath, homoplasy, vicariance biogeography
eTo whom correspondence should be addressed at: Department of Zoology, P.O. Box 118525, University of Florida, Gainesville, FL 32611.E-mail: firstname.lastname@example.org
Author contributions: J.H., E.L.B., M.J.B., S.J.H., R.T.K., W.S.M., F.H.S., and D.W.S. designed research; J.H., E.L.B., M.J.B., C.J.H., R.C.K.B., J.L.C., S.J.H., K.-L.H., R.T.K., B.D.M., K.J.M., S.R., S.J.S., C.C.W., and T.Y. performed research; J.H., E.L.B., M.J.B., and C.J.H. analyzed data; and J.H., E.L.B., and M.J.B. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: New DNA sequences are deposited in GenBank (accession nos. EU805776–EU805796, andEU822937). Alignments and trees have been deposited in TreeBase (study accession no. S2138).
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o A group is polyphyletic if its defining characters are convergent (29). Ratites have long been defined by the absence of a keel on their sternum (e.g., ref. 3), a character related to flightlessness. Our analyses (see below) indicate the common ancestor of ratites was likely capable of flight and thus had a keeled sternum and was not a ratite.
© 2008 by The National Academy of Sciences of the USA