A phylogenetic method for detecting positive epistasis in gene sequences and its application to RNA virus evolution

被引:40
作者
Shapiro, Beth
Rambaut, Andrew
Pybus, Oliver G.
Holmes, Edward C.
机构
[1] Univ Oxford, Dept Zool, Oxford OX1 3PS, England
[2] Penn State Univ, Dept Biol, Mueller Lab, Ctr Infect Dis Dynam, Philadelphia, PA USA
基金
英国惠康基金;
关键词
coevolution; phylogenetics; RNA viruses; viral evolution; epistasis;
D O I
10.1093/molbev/msl037
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
RNA virus genomes are compact, often containing multiple overlapping reading frames and functional secondary structure. Consequently, it is thought that evolutionary interactions between nucleotide sites are commonplace in the genomes of these infectious agents. However, the role of epistasis in natural populations of RNA viruses remains unclear. To investigate the pervasiveness of epistasis in RNA viruses, we used a parsimony-based computational method to identify pairs of co-occurring mutations along phylogenies of 177 RNA virus genes. This analysis revealed widespread evidence for positive epistatic interactions at both synonymous and nonsynonymous nucleotide sites and in both clonal and recombining viruses, with the majority of these interactions spanning very short sequence regions. These findings have important implications for understanding the key aspects of RNA virus evolution, including the dynamics of adaptation. Additionally, many comparative analyses that utilize the phylogenetic relationships among gene sequences assume that mutations represent independent, uncorrelated events. Our results show that this assumption may often be invalid.
引用
收藏
页码:1724 / 1730
页数:7
相关论文
共 30 条
[1]   CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING [J].
BENJAMINI, Y ;
HOCHBERG, Y .
JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) :289-300
[2]   Evidence for positive epistasis in HIV-1 [J].
Bonhoeffer, S ;
Chappey, C ;
Parkin, NT ;
Whitcomb, JM ;
Petropoulos, CJ .
SCIENCE, 2004, 306 (5701) :1547-1550
[3]  
Burch CL, 1999, GENETICS, V151, P921
[4]   Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission [J].
Chare, ER ;
Holmes, EC .
JOURNAL OF GENERAL VIROLOGY, 2004, 85 :3149-3157
[5]   Mutation rates among RNA viruses [J].
Drake, JW ;
Holland, JJ .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 1999, 96 (24) :13910-13913
[6]   Test of synergistic interactions among deleterious mutations in bacteria [J].
Elena, SF ;
Lenski, RE .
NATURE, 1997, 390 (6658) :395-398
[7]   A hidden Markov Model approach to variation among sites in rate of evolution [J].
Felsenstein, J ;
Churchill, GA .
MOLECULAR BIOLOGY AND EVOLUTION, 1996, 13 (01) :93-104
[8]   Localization of the single-stranded RNA-binding domains of bluetongue virus nonstructural protein NS2 [J].
Fillmore, GC ;
Lin, H ;
Li, JKK .
JOURNAL OF VIROLOGY, 2002, 76 (02) :499-506
[9]   Cofolding organizes alfalfa mosaic virus RNA and coat protein for replication [J].
Guogas, LM ;
Filman, DJ ;
Hogle, JM ;
Gehrke, L .
SCIENCE, 2004, 306 (5704) :2108-2111
[10]   RNA-based phylogenetic methods: application to mammalian mitochondrial RNA sequences [J].
Hudelot, C ;
Gowri-Shankar, V ;
Jow, H ;
Rattray, M ;
Higgs, PG .
MOLECULAR PHYLOGENETICS AND EVOLUTION, 2003, 28 (02) :241-252