Adaptation sensu Sewall Wright: evolution over rugged fitness landscapes
Final Report Abstract
Subject of our project were models of adaptation at the molecular level. Such models were developed since the early 1960s. In contrast to phenotypic evolution, these models were sequence-based. The key insight at that time was that real adaptation occurs in sequence space. In the 1980s, Stuart Kauffman and others set out to discover the laws that describe adaptation through sequence space. Their approach emphasized the idea that a sequence space may exhibit multiple local fitness optima and can be pictured as a „fitness landscape“ (sensu Sewall Wright). We investigated the evolution of DNA sequences giving rise to various molecular entities, such as RNA secondary structures. The data for this project were retrieved from genomic studies of vertebrate and Drosophila species. Because of the molecular interactions underlying these entities (in particular due to Watson-Crick pairing in RNA structures), we observed that fitness is not defined by single nucleotidesin a sequence but by potentially complex combinations of nucleotides (for instance,interacting Watson-Crick pairsor higher-order structures). As a consequence, we found that recombination between interacting nucleotides may play an important role in determining the speed of evolution, unlike in simple models of Darwinian evolution. Due to the molecular interaction between nucleotides, the rate of adaptation is usually reduced, indicating that evolution has to go through adaptive valleys to reach the peak of highest population fitness. However, we also found that these valleys of reduced fitness are usually not very deep because evolution in a fitness landscape with multiple peaks may proceed along ridges of relatively constant fitness instead of going through valleys.
Publications
- (2007): Evolution of genes and genomes on the Drosophila phylogeny. Nature 450: 203-218
Drosophila 12 Genomes Consortium
- (2008): Analyzing the evolution of RNA secondary structures in vertebrate introns using Kimura’s model of compensatory fitness interactions. Mol. Biol. Evol. 25: 2483-2492
Piskol, R. and W. Stephan
- (2008): Determining the relationship of gene expression and global mRNA stability in Drosophila melanogaster and Escherichia coli using linear models. Gene 424: 102-107
Eck, S. and W. Stephan
- (2009) Evolutionary selection between alternative modes of gene regulation.Proc. Natl. Acad. Sci. USA 106, 8841–8846
U. Gerland and T. Hwa
- (2011) Emergence of information transmission in a prebiotic RNA reactor.Physical Review Letters 107, 018101
B. Obermayer, H. Krammer, D. Braun, and U. Gerland
- (2011): Selective constraints in conserved non-coding RNAs of drosophilid and hominid genomes. Mol. Biol. Evol. 28: 1519-1529
Piskol, R. and W. Stephan
- (2011): The role of effective population size in compensatory evolution. Genome Biol. Evol. 3: 528-538
Piskol, R. and W. Stephan
- (2011)The prebiotic evolutionary advantage of transferring genetic information from RNA to DNA.Nucleic Acids Research 39, 8135-47
K. Leu, B. Obermayer, S. Rajamani, U. Gerland, and I.A. Chen
- (2013) Cascade of Reduced Speed and Accuracy After Errors in Enzyme-Free Copying of Nucleic Acid Sequences. J. Am. Chem. Soc. 135, 354–366
K. Leu, E. Kervio, B. Obermayer, R. Turk-MacLeod, C. Yuan, J. Luevano, E. Chen, U. Gerland, C. Richert, and I.A. Chen
(See online at https://doi.org/10.1021/ja3095558) - (2013), The Paradox of Dual Roles in the RNA World: Resolving the Conflict Between Stable Folding and Templating Ability. J. Mol. Evol. 77, 55–63
N.A. Ivica, B. Obermayer, G.W. Campbell, S. Rajamani, U. Gerland, and I.A. Chen
- (2016): A model of compensatory molecular evolution involving multiple sites in RNA molecules. J. theor. Biol. 388: 96-107
Kusumi, J., M. Ichinose, M. Takefu, R. Piskol, W. Stephan, and M. Iizuka
(See online at https://doi.org/10.1016/j.jtbi.2015.10.008)