25 JANUARY 2013 VOL 339 SCIENCE
Guojie Zhang,1,2*† Christopher Cowled,3Zhengli Shi,4 Zhiyong Huang,1 Kimberly A. Bishop-Lilly, Xiaodong Fang,1 James W. Wynne,3 Zhiqiang Xiong,1 Michelle L. Baker,3 Wei Zhao,1 Mary Tachedjian,3 Yabing Zhu,1 Peng Zhou,3,4 Xuanting Jiang,1 Justin Ng,3 Lan Yang,1 Lijun Wu,4 Jin Xiao,1 Yue Feng,1 Yuanxin Chen,1 Xiaoqing Sun,1 Yong Zhang,1 Glenn A. Marsh,3 Gary Crameri,3 Christopher C. Broder,6 Kenneth G. Frey,5
Lin-Fa Wang,3,7† Jun Wang1,8,9
Bats are the only mammals capable of sustained flight and are notorious reservoir hosts for some of the world’s most highly pathogenic viruses, including Nipah, Hendra, Ebola, and severe acute respiratory syndrome (SARS). To identify genetic changes associated with the development of bat-specific traits, we performed whole-genome sequencing and comparative analyses of two distantly related species, fruit bat Pteropus alecto and insectivorous bat Myotis davidii. We discovered an unexpected concentration of positively selected genes in the DNA damage checkpoint and nuclear factor kB pathways that may be related to the origin of flight, as well as expansion and contraction of important gene families. Comparison of bat genomes with other mammalian species has provided new insights into bat biology and evolution.
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The most conspicuous feature of bats, distinguishing them from all other mammalian species, is the capacity for sustained flight. Positive selection in the oxidative phosphorylation (OXPHOS) pathway suggests that increased metabolic capacity played a key role in its evolution (3), yet the by-products of oxidative metabolism [such as reactive oxygen species (ROS)] can produce harmful side effects including DNA damage (4). We hypothesize that genetic changes during the evolution of flight in bats likely included adaptations to limit collateral damage caused by by-products of elevated metabolic rate. Another phenomenon that has sparked intense interest in recent years is the discovery that bats maintain and disseminate numerous deadly viruses (5). In this context, we further hypothesize that the long-term coexistence of bats and viruses must have imposed strong selective pressures on the bat genome, and the genes most likely to reflect this are those directly related to the first line of antiviral defense—the innate immune system.
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In summary, comparative analysis of P. alecto and M. davidii genomes has provided insight into the phylogenetic placement of bats and has revealed evidence of genetic changes that may have contributed to their evolution. Gene duplication events played a particularly prominent role in the evolution of Myotis bats and may have helped contribute to their speciation. Concentration of positively selected genes in the DNA damage checkpoint pathway in bats may indicate an important step in the evolution of flight, whereas evidence of change in components shared by the DNA damage pathway and the innate immune system raises the interesting possibility that flight-induced adaptations have had inadvertent effects on bat immune function and possibly also life expectancy (24). The data generated by this study will help to address major gaps in our understanding of bat biology and to provide new directions for future research.
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Comparative Analysis of Bat Genomes Provides Insight into the Evolution of Flight and Immunity