Adaptive evolution on neutral networks

We study the evolution of large but finite asexual populations evolving in fitness landscapes in which all mutations are either neutral or strongly deleterious. We demonstrate that despite the absence of higher fitness genotypes, adaptation takes place as regions with more advantageous distributions of neutral genotypes are discovered. Since these discoveries are typically rare events, the population dynamics can be subdivided into separate epochs, with rapid transitions between them. Within one epoch, the average fitness in the population is approximately constant. The transitions between epochs, however, are generally accompanied by a significant increase in the average fitness. We verify our theoretical considerations with two analytically tractable bitstring models.

• Publication year

  2001

• Venue

  Bulletin of Mathematical Biology

• Publication date

  2001-01-03

• Fields of study

  Biology, Physics, Computer Science, Mathematics, Medicine

• Identifiers
  DOI 10.1006/BULM.2001.0244arXiv physics/0101021PMID 11497165
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The Hypercycle: A principle of natural self-organization

  2009cited by this paper
• Evolution of digital organisms at high mutation rates leads to survival of the flattest

  2001cited by this paper
• Adaptation of epistatic effects via selection for reduced mutational load

  2000cited by this paper
• Interaction between directional epistasis and average mutational effects

  2000cited by this paper
• Neutral evolution of mutational robustness.

  1999influential reference
• Statistical Dynamics of the Royal Road Genetic Algorithm

  1999influential reference
• Evolutionary Dynamics in Time-dependent Environments

  1999cited by this paper
• Dynamic fitness landscapes in molecular evolution

  1999cited by this paper
• Metastable evolutionary dynamics: Crossing fitness barriers or escaping via neutral paths?

  1999cited by this paper
• A Dynamical Theory of Speciation on Holey Adaptive Landscapes

  1998cited by this paper
• IR-98-039 / April Continuity in Evolution : On the Nature of Transitions

  1998cited by this paper
• Evolution and speciation on holey adaptive landscapes.

  1997cited by this paper
• Finite populations induce metastability in evolutionary search

  1997influential reference
• Punctuated Evolution Caused by Selection of Rare Beneficial Mutations

  1996cited by this paper
• Smoothness within ruggedness: the role of neutrality in adaptation.

  1996cited by this paper
• Evolutionary Dynamics and Optimization: Neutral Networks as Model-Landscapes for RNA Secondary-Structure Folding-Landscapes

  1995cited by this paper
• Self-organized criticality in living systems

  1994cited by this paper
• Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations.

  1994cited by this paper
• What is a quasispecies?

  1992cited by this paper
• Evolution in a flat fitness landscape

  1991cited by this paper
• Punctuated Equilibria in Genetic Search

  1991cited by this paper
• Diffusion Models of Population Genetics

  1990cited by this paper
• Deleterious mutations and the evolution of sexual reproduction

  1988cited by this paper
• Stationary mutant distributions and evolutionary optimization.

  1988cited by this paper
• Molecular quasi-species.

  1988cited by this paper
• Evolution on sequence space and tensor products of representation spaces

  1988cited by this paper
• Spectral properties of Eigen evolution matrices

  1987cited by this paper
• Self-replication with errors. A model for polynucleotide replication.

  1982cited by this paper
• The Hypercycle. A Principle of Natural Self Organization.

  1981cited by this paper
• Punctuated equilibria: the tempo and mode of evolution reconsidered

  1977cited by this paper
• Models in Paleobiology

  1972cited by this paper
• Punctuated equilibria: an alternative to phyletic gradualism

  1972cited by this paper
• Mathematical Topics in Population Genetics.

  1972cited by this paper
• Genetic Loads and the Cost of Natural Selection

  1970cited by this paper
• The mutational load with epistatic gene interactions in fitness.

  1966cited by this paper
• Our load of mutations.

  1950cited by this paper
• The Effect of Variation of Fitness

  1937influential reference
• A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation

  1927cited by this paper
• Unravelling the Evolutionary Advantage of Sex : a Commentary on ' Mutation–selection Balance and the Evolutionary Advantage of Sex and Recombination '

  year unknowncited by this paper

• Evolutionary Developmental Biology Can Serve as the Conceptual Foundation for a New Design Paradigm in Artificial Intelligence

  2025cites this paper
• Evolution, Future of AI, and Singularity

  2025cites this paper
• On the Parallels Between Evolutionary Theory and the State of AI

  2025cites this paper
• A Minimal CA-Based Model Capturing Evolutionarily Relevant Features of Biological Development

  2025cites this paper
• Evolution takes multiple paths to evolvability when facing environmental change

  2024cites this paper
• Innovation in viruses: fitness valley crossing, neutral landscapes, or just duplications?

  2024cites this paper
• Late Bloomers, First Glances, Second Chances: Exploration of the Mechanisms Behind Fitness Diversity

  2024cites this paper
• A Law of Redundancy Compounds the Problem of Cancer and Precision Medicine

  2023cites this paper
• Bluetongue Research at a Crossroads: Modern Genomics Tools Can Pave the Way to New Insights.

  2022cites this paper
• [The impact of neutral mutations on genome evolvability].

  2022cites this paper
• Conflicting effects of recombination on the evolvability and robustness in neutrally evolving populations

  2022cites this paper
• Effects of recombination on the evolvability, genetic diversity and mutational robustness of neutrally evolving populations

  2022cites this paper
• A Family of Fitness Landscapes Modeled through Gene Regulatory Networks

  2021cites this paper
• Sword of Damocles or choosing well. Population genetics sheds light into the future of the COVID-19 pandemic and SARS-CoV-2 new mutant strains.

  2021cites this paper
• Evolvability, Neutrality and Search Difficulty

  2021cites this paper
• Environmental flexibility does not explain metabolic robustness

  2020cites this paper
• The Impact of Neutral Mutations on Genome Evolvability.

  2020cites this paper
• From genotypes to organisms: State-of-the-art and perspectives of a cornerstone in evolutionary dynamics.

  2020cites this paper
• Recombination and mutational robustness in neutral fitness landscapes

  2019cites this paper
• Evolution Rapidly Optimizes Stability and Aggregation in Lattice Proteins Despite Pervasive Landscape Valleys and Mazes

  2019cites this paper
• On the networked architecture of genotype spaces and its critical effects on molecular evolution

  2018cites this paper
• Mapping the Peaks: Fitness Landscapes of the Fittest and the Flattest

  2018cites this paper
• Computing the Extended Synthesis: Mapping the Dynamics and Conceptual Structure of the Evolvability Research Front

  2017cites this paper
• The space of genotypes is a network of networks: implications for evolutionary and extinction dynamics

  2017cites this paper
• Rôle de la protéine PB1 dans la fidélité du complexe polymérase des virus influenza

  2017cites this paper
• Computing the Extended Synthesis: Mapping the Dynamics and Conceptual Structure of the Evolvability Research Front.

  2017cites this paper
• Dimension Reduction and Signal Decomposition for Genotype-Phenotype Relations

  2017cites this paper
• Natural selection can favor ratchet robustness over mutational robustness

  2017cites this paper
• Robustness, evolvability and phenotypic complexity: insights from evolving digital circuits

  2017cites this paper
• Attenuation of RNA viruses by redirecting their evolution in sequence space

  2017cites this paper
• Quantitative Analysis of Evolvability using Vertex Centralities in Phenotype Network

  2016cites this paper
• Robustness to Faults Promotes Evolvability: Insights from Evolving Digital Circuits

  2016cites this paper
• Morphological inversion of complex diffusion

  2016cites this paper
• Neutral network assortativity shapes whether selective pressure promotes or hinders robustness

  2016influential citation
• Genetic Code Evolution Reveals the Neutral Emergence of Mutational Robustness, and Information as an Evolutionary Constraint

  2015cites this paper
• Pervasive robustness in biological systems

  2015cites this paper
• Tipping points and early warning signals in the genomic composition of populations induced by environmental changes

  2015cites this paper
• The Effects of Recombination on Phenotypic Exploration and Robustness in Evolution

  2014cites this paper
• Population Exploration on Genotype Networks in Genetic Programming

  2014cites this paper
• Evolutionary game theory using agent-based methods.

  2014cites this paper
• Critical mutation rates in small populations

  2014cites this paper
• Robustness and Evolvability of Recombination in Linear Genetic Programming

  2013cites this paper
• Congruent Evolution of Fitness and Genetic Robustness in Vesicular Stomatitis Virus

  2013cites this paper
• ParadisEO-MO: from fitness landscape analysis to efficient local search algorithms

  2013cites this paper
• The evolutionary ecology of technological innovations

  2013cites this paper
• Macroevolution in silico: scales, constraints and universals

  2013cites this paper
• Experiments on the role of deleterious mutations as stepping stones in adaptive evolution

  2013cites this paper
• Viral mutation rates: modelling the roles of within-host viral dynamics and the trade-off between replication fidelity and speed

  2013cites this paper
• A Nonadaptive Origin of a Beneficial Trait: In Silico Selection for Free Energy of Folding Leads to the Neutral Emergence of Mutational Robustness in Single Domain Proteins

  2013cites this paper
• Positional Information Storage in Sequence Patterns

  2013cites this paper
• Critical Mutation Rate Has an Exponential Dependence on Population Size in Haploid and Diploid Populations

  2013cites this paper
• Neutrality in the Graph Coloring Problem

  2013cites this paper
• Dissecting the molecular basis of foot-and-mouth disease virus evolution

  2012cites this paper
• Evolving Distributed Algorithms With Genetic Programming

  2012cites this paper
• Emergent Diversity in an Open-Ended Evolving Virtual Community

  2012cites this paper
• Project-Team Dolphin ParadisEO-MO : From Fitness Landscape Analysis to Efficient Local Search Algorithms

  2012cites this paper
• Hepatitis C quasispecies adaptation in the setting of a variable fidelity polymerase

  2012cites this paper
• Evolutionary dynamics on multiple scales: a quantitative analysis of the interplay between genotype, phenotype, and fitness in linear genetic programming

  2012cites this paper
• Critical mutation rate has an exponential dependence on population size

  2011influential citation
• Biased mutational pattern and quasispecies hypothesis in H5N1 virus

  2011cites this paper
• NILS: A Neutrality-Based Iterated Local Search and Its Application to Flowshop Scheduling

  2011cites this paper
• On the Neutrality of Flowshop Scheduling Fitness Landscapes

  2011cites this paper
• A biophysical protein folding model accounts for most mutational fitness effects in viruses

  2011influential citation
• Critical Properties of Complex Fitness Landscapes

  2010cites this paper
• Phenotypic effect of mutations in evolving populations of RNA molecules

  2010cites this paper
• Does Mutational Robustness Inhibit Extinction by Lethal Mutagenesis in Viral Populations?

  2010influential citation
• Simple genomes, complex interactions: epistasis in RNA virus.

  2010cites this paper
• Pseudaptations and the Emergence of Beneficial Traits

  2010cites this paper
• Algorithme Évolutionnaire à États pour l'Optimisation Difficile. (States-based Evolutionary Algorithm for Difficult Optimization)

  2010influential citation
• A trade-off between neutrality and adaptability limits the optimization of viral quasispecies.

  2009cites this paper
• Evolutionary dynamics on networks of selectively neutral genotypes: effects of topology and sequence stability.

  2009cites this paper
• Why Is Optimization Difficult?

  2009cites this paper
• The role of weak selection and high mutation rates in nearly neutral evolution.

  2009cites this paper
• Probing Evolutionary Repeatability: Neutral and Double Changes and the Predictability of Evolutionary Adaptation

  2009cites this paper
• Nature-inspired optimisation: Improvements to the Particle Swarm Optimisation Algorithm and the Bees Algorithm

  2009cites this paper
• Simple quasispecies models for the survival-of-the-flattest effect: The role of space.

  2008cites this paper
• Robustness and evolution: concepts, insights and challenges from a developmental model system

  2008cites this paper
• Emergence of species in evolutionary “simulated annealing”

  2008cites this paper
• Modularity in a Computational Model of Embryogeny

  2008cites this paper
• Understanding protein evolution: from protein physics to Darwinian selection.

  2008cites this paper
• Neutral network sizes of biological RNA molecules can be computed and are not atypically small

  2008cites this paper
• The Topology of the Protein Network Influences the Dynamics of Gene Order: From Systems Biology to a Systemic Understanding of Evolution

  2008cites this paper
• The evolutionary dynamics of neutral networks : lessons from RNA

  2008cites this paper
• Evolution of complex dynamics.

  2008cites this paper
• Evolution of Coadaptation in a Subdivided Population

  2007cites this paper
• Complex adaptation and system structure

  2007cites this paper
• A long-term evolutionary pressure on the amount of noncoding DNA.

  2007cites this paper
• Hidden Dimensions in Protein Evolution: Stability, Mutational Robustness, and Evolvability

  2007influential citation
• Fitness landscape of the cellular automata majority problem: View from the "Olympus"

  2007cites this paper
• EFFECTS OF POPULATION SIZE AND MUTATION RATE ON THE EVOLUTION OF MUTATIONAL ROBUSTNESS

  2007influential citation
• Evolutionary coupling between the deleteriousness of gene mutations and the amount of non-coding sequences.

  2007cites this paper
• Evolution favors protein mutational robustness in sufficiently large populations

  2007influential citation
• Reducing the Number of Fitness Evaluations in Graph Genetic Programming Using a Canonical Graph Indexed Database

  2007cites this paper
• Exact solution of the Eigen model with general fitness functions and degradation rates.

  2006cites this paper
• Balancing Robustness and Evolvability

  2006cites this paper
• In silico predicted robustness of viroids RNA secondary structures. I. The effect of single mutations.

  2006cites this paper
• Deceptiveness and neutrality the ND family of fitness landscapes

  2006cites this paper
• Codon Usage and Selection on Proteins

  2006influential citation
• Chapter 8 – Conclusions

  2006cites this paper
• Emergent Robustness in Competition Between Autocatalytic Chemical Networks

  2006cites this paper