Yong-Yi Shen a,b,c, Lu Liang a,c, Zhou-Hai Zhu b, Wei-Ping Zhou a,d, David M. Irwin e,f, and Ya-Ping Zhang a,b,1
aState Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China;
bLaboratory for Conservation and Utilization of Bio-resources, Yunnan University, Kunming 650091, China;
cGraduate School of the Chinese Academy of Sciences, Beijing 100000, China;
dDepartment of Molecular and Cell Biology, School of Life Sciences, University of Science and Technology of China, Hefei, Anhui 230026, China;
eDepartment of Laboratory Medicine and Pathobiology, University of Toronto, Toronto, ON, Canada M5S 1A8; and
fBanting and Best Diabetes Centre, University of Toronto, Toronto, ON, Canada M5S 1A8
Edited* by David M. Hillis, University of Texas, Austin, TX, and approved March 30, 2010 (received for review October 31, 2009)
Bat flight poses intriguing questions about how flight independently developed in mammals. Flight is among the most energy-consuming activities. Thus, we deduced that changes in energy metabolism must be a primary factor in the origin of flight in bats. The respiratory chain of the mitochondrial produces 95% of the adenosine triphosphate (ATP) needed for locomotion. Because the respiratory chain has a dual genetic foundation, with genes encoded by both the mitochondrial and nuclear genomes, we examined both genomes to gain insights into the evolution of flight within mammals. Evidence for positive selection was detected in 23.08% of the mitochondrial-encoded and 4.90% of nuclear-encoded oxidative phosphorylation (OXPHOS) genes, but in only 2.25% of the nuclear-encoded nonrespiratory genes that function in mitochondria or 1.005% of other nuclear genes in bats. To address the caveat that the two available bat genomes are of only draft quality, we resequenced 77 OXPHOS genes from four species of bats. The analysis of the resequenced gene data are in agreement with our conclusion that a significantly higher proportion of genes involved in energy metabolism, compared with background genes, show evidence of adaptive evolution specific on the common ancestral bat lineage. Both mitochondrial and nuclear-encoded OXPHOS genes display evidence of adaptive evolution along the common ancestral branch of bats, supporting our hypothesis that genes involved in energy metabolism were targets of natural selection and allowed adaptation to the huge change in energy demand that were required during the origin of flight.
Chiroptera genetic foundation mitochondria OXPHOS
1To whom correspondence should be addressed. E-mail:firstname.lastname@example.org.
Author contributions: Y.-Y.S. and Y.-P.Z. designed research; Y.-Y.S. and L.L. performed research; Y.-Y.S., Z.-H.Z., W.-P.Z., and Y.-P.Z. analyzed data; and Y.-Y.S., D.M.I., and Y.-P.Z. wrote the paper.
The authors declare no conflict of interest.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. GQ427677–GQ427913 andGU292797-GU292809).
↵*This Direct Submission article had a prearranged editor.
This article contains supporting information online at www.pnas.org/cgi/content/full/0912613107/DCSupplemental.
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