Contingency, convergence and hyper-astronomical numbers in biological evolution.

Counterfactual questions such as "what would happen if you re-run the tape of life?" turn on the nature of the landscape of biological possibilities. Since the number of potential sequences that store genetic information grows exponentially with length, genetic possibility spaces can be so unimaginably vast that commentators frequently reach of hyper-astronomical metaphors that compare their size to that of the universe. Re-run the tape of life and the likelihood of encountering the same sequences in such hyper-astronomically large spaces is infinitesimally small, suggesting that evolutionary outcomes are highly contingent. On the other hand, the wide-spread occurrence of evolutionary convergence implies that similar phenotypes can be found again with relative ease. How can this be? Part of the solution to this conundrum must lie in the manner that genotypes map to phenotypes. By studying simple genotype-phenotype maps, where the counterfactual space of all possible phenotypes can be enumerated, it is shown that strong bias in the arrival of variation may explain why certain phenotypes are (repeatedly) observed in nature, while others never appear. This biased variation provides a non-selective cause for certain types of convergence. It illustrates how the role of randomness and contingency may differ significantly between genetic and phenotype spaces.

[1]  Kamaludin Dingle,et al.  Probabilistic bias in genotype-phenotype maps , 2014 .

[2]  FRANK B. SALISBURY,et al.  Natural Selection and the Complexity of the Gene , 1969, Nature.

[3]  P Schuster,et al.  Evolution in Silico and in Vitro: The RNA Model , 2001, Biological chemistry.

[4]  Stephen C. Meyer,et al.  Signature in the Cell , 2009 .

[5]  J. L. King,et al.  Non-Darwinian evolution. , 1969, Science.

[6]  C. Levinthal How to fold graciously , 1969 .

[7]  Anthony D. Keefe,et al.  Functional proteins from a random-sequence library , 2001, Nature.

[8]  A. Bennett The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[9]  R. Fraser The structure of deoxyribose nucleic acid. , 2004, Journal of structural biology.

[10]  The statistics of string/M theory vacua , 2003, hep-th/0303194.

[11]  A. Wagner Robustness and Evolvability in Living Systems , 2005 .

[12]  Philip A. Romero,et al.  Exploring protein fitness landscapes by directed evolution , 2009, Nature Reviews Molecular Cell Biology.

[13]  Luca Konig,et al.  The Blind Watchmaker Why The Evidence Of Evolution Reveals A Universe Without Design , 2016 .

[14]  G. Edelman Building a Picture of the Brain a , 1999, Annals of the New York Academy of Sciences.

[15]  A. Stoltzfus,et al.  Mendelian-Mutationism: The Forgotten Evolutionary Synthesis , 2014, Journal of the history of biology.

[16]  J. Huxley Evolution: The Modern Synthesis , 1943 .

[17]  G. R. McGhee Convergent Evolution: Limited Forms Most Beautiful , 2011 .

[18]  Eugene V Koonin,et al.  Origin and evolution of the genetic code: The universal enigma , 2008, IUBMB life.

[19]  M. Pigliucci Sewall Wright’s adaptive landscapes: 1932 vs. 1988 , 2008 .

[20]  Jonathan Perreault,et al.  The ubiquitous hammerhead ribozyme. , 2012, RNA.

[21]  D. Schluter,et al.  Does evolutionary theory need a rethink? , 2014, Nature.

[22]  Peter Clote,et al.  How optimal is the genetic code? , 1997, German Conference on Bioinformatics.

[23]  Jack W. Szostak,et al.  In vitro evolution suggests multiple origins for the hammerhead ribozyme , 2001, Nature.

[24]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[25]  D. Noble Evolution beyond neo-Darwinism: a new conceptual framework , 2015, Journal of Experimental Biology.

[26]  Walter Fontana,et al.  Fast folding and comparison of RNA secondary structures , 1994 .

[27]  A. D. D. Species and Varieties: Their Origin by Mutation , 1907, Nature.

[28]  P. W. V. D. Pas The correspondence of Hugo de Vries and Charles Darwin. , 1970 .

[29]  T. Dobzansky Genetic structure of natural populations. , 1946, Year book - Carnegie Institution of Washington.

[30]  Uri Alon,et al.  The genetic code is nearly optimal for allowing additional information within protein-coding sequences. , 2007, Genome research.

[31]  Kamaludin Dingle,et al.  The structure of the genotype–phenotype map strongly constrains the evolution of non-coding RNA , 2015, Interface Focus.

[32]  Thomas S. Ray,et al.  Life's Solution: Inevitable Humans in a Lonely Universe , 2006, Artificial Life.

[33]  The Runes of Evolution: How the Universe became Self-Aware , 2015 .

[34]  John H. White,et al.  How much of protein sequence space has been explored by life on Earth? , 2008, Journal of The Royal Society Interface.

[35]  George R. McGhee,et al.  The Geometry of Evolution: Adaptive Landscapes and Theoretical Morphospaces , 2006 .

[36]  M. Feldman,et al.  The extended evolutionary synthesis: its structure, assumptions and predictions , 2015, Proceedings of the Royal Society B: Biological Sciences.

[37]  S. Kauffman At Home in the Universe: The Search for the Laws of Self-Organization and Complexity , 1995 .

[38]  F. Hoyle,et al.  The Universe: Past and Present Reflections , 1982 .

[39]  F. Crick,et al.  Molecular Structure of Nucleic Acids: A Structure for Deoxyribose Nucleic Acid , 1953, Nature.

[40]  K. Dill Polymer principles and protein folding , 1999, Protein science : a publication of the Protein Society.

[41]  Sebastian E. Ahnert,et al.  Genetic Correlations Greatly Increase Mutational Robustness and Can Both Reduce and Enhance Evolvability , 2015, PLoS Comput. Biol..

[42]  F. H. C. CRICK,et al.  Origin of the Genetic Code , 1967, Nature.

[43]  C. Levinthal Are there pathways for protein folding , 1968 .

[44]  R. Lenski,et al.  The Deep Structure of Biology Is Convergence Sufficiently Ubiquitous to Give a Directional Signal ? , 2008 .

[45]  L. Hurst,et al.  The Genetic Code Is One in a Million , 1998, Journal of Molecular Evolution.

[46]  A. L. MACKAY,et al.  Optimization of the Genetic Code , 1967, Nature.

[47]  A. Minelli,et al.  The changing role of the embryo in evolutionary thought: roots of Evo-Devo , 2006, Heredity.

[48]  Andrew Sclater The extent of Charles Darwin’s knowledge of Mendel , 2006, Journal of Biosciences.

[49]  Ard A. Louis,et al.  The Arrival of the Frequent: How Bias in Genotype-Phenotype Maps Can Steer Populations to Local Optima , 2014, PloS one.

[50]  J. Maynard Smith Natural Selection and the Concept of a Protein Space , 1970 .