The genetic theory of adaptation: a brief history

Theoretical studies of adaptation have exploded over the past decade. This work has been inspired by recent, surprising findings in the experimental study of adaptation. For example, morphological evolution sometimes involves a modest number of genetic changes, with some individual changes having a large effect on the phenotype or fitness. Here I survey the history of adaptation theory, focusing on the rise and fall of various views over the past century and the reasons for the slow development of a mature theory of adaptation. I also discuss the challenges that face contemporary theories of adaptation.

[1]  Karl Pearson,et al.  Mathematical contributions to the theory of evolution, On the law of ancestral heredity , 1898, Proceedings of the Royal Society of London.

[2]  F. D. Evolution and Adaptation , 1904, Nature.

[3]  Albert Charles Seward DARWIN AND MODERN SCIENCE , 1910 .

[4]  N. Pierce Origin of Species , 1914, Nature.

[5]  R. Fisher XV.—The Correlation between Relatives on the Supposition of Mendelian Inheritance. , 1919, Transactions of the Royal Society of Edinburgh.

[6]  R A Fisher,et al.  Darwinian evolution of mutations. , 1922, The Eugenics review.

[7]  Clarence Cook Little,et al.  The second international congress of eugenics , 1922 .

[8]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[9]  S. Wright,et al.  Evolution in Mendelian Populations. , 1931, Genetics.

[10]  Julian Huxley,et al.  The new systematics , 1941 .

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

[12]  K. Mather,et al.  POLYGENIC INHERITANCE and NATURAL SELECTION , 1943 .

[13]  H. Muller The Darwinian and modern conceptions of natural selection. , 1949, Proceedings of the American Philosophical Society.

[14]  C. Pigott Genetics and the Origin of Species , 1959, Nature.

[15]  H. Grüneberg,et al.  Introduction to quantitative genetics , 1960 .

[16]  Thornton Page,et al.  The Scientist Speculates: An Anthology of Partly-baked Ideas , 1964 .

[17]  M. Kimura Evolutionary Rate at the Molecular Level , 1968, Nature.

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

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

[20]  W. Provine,et al.  The Origins of Theoretical Population Genetics , 1972 .

[21]  Kenneth Mather,et al.  Biometrical genetics , 1972, Heredity.

[22]  L. Hogben The Origins of Theoretical Population Genetics , 1974, The British Journal for the History of Science.

[23]  Ishay Weissman,et al.  Estimation of parameters and large quantiles based on the K largest observations , 1978, Advances in Applied Probability.

[24]  I. Weissman Estimation of Parameters and Large Quantiles Based on the k Largest Observations , 1978 .

[25]  Ned Glick,et al.  Breaking Records and Breaking Boards , 1978 .

[26]  M. Kimura Model of effectively neutral mutations in which selective constraint is incorporated. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[27]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[28]  John Maynard Smith,et al.  Evolution now : a century after Darwin , 1982 .

[29]  R. Elston The mathematical theory of quantitative genetics , 1982 .

[30]  M. Kimura The Neutral Theory of Molecular Evolution: Introduction , 1983 .

[31]  J. Gillespie A simple stochastic gene substitution model. , 1983, Theoretical population biology.

[32]  M. R. Leadbetter,et al.  Extremes and Related Properties of Random Sequences and Processes: Springer Series in Statistics , 1983 .

[33]  J. Gillespie MOLECULAR EVOLUTION OVER THE MUTATIONAL LANDSCAPE , 1984, Evolution; international journal of organic evolution.

[34]  J H Gillespie,et al.  Natural selection and the molecular clock. , 1986, Molecular biology and evolution.

[35]  S. Kauffman,et al.  Towards a general theory of adaptive walks on rugged landscapes. , 1987, Journal of theoretical biology.

[36]  Gerd Gigerenzer,et al.  The Probabilistic revolution , 1987 .

[37]  Alan S. Perelson,et al.  Theoretical Immunology, Part One , 1988 .

[38]  E. D. Weinberger,et al.  A more rigorous derivation of some properties of uncorrelated fitness landscapes , 1988 .

[39]  C. A. Macken,et al.  Protein evolution on rugged landscapes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[40]  N. Barton,et al.  Evolutionary quantitative genetics: how little do we know? , 1989, Annual review of genetics.

[41]  S. Rice A geometric model for the evolution of development , 1990 .

[42]  J. Gillespie The causes of molecular evolution , 1991 .

[43]  Weinberger,et al.  Local properties of Kauffman's N-k model: A tunably rugged energy landscape. , 1991, Physical review. A, Atomic, molecular, and optical physics.

[44]  Lynn Nadel,et al.  1990 Lectures in Complex Systems , 1991 .

[45]  A. Perelson,et al.  Evolutionary walks on rugged landscapes , 1991 .

[46]  T. Ohta THE NEARLY NEUTRAL THEORY OF MOLECULAR EVOLUTION , 1992 .

[47]  Flyvbjerg,et al.  Coevolution in a rugged fitness landscape. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[48]  H. A. Orr,et al.  The Genetics of Adaptation: A Reassessment , 1992, The American Naturalist.

[49]  Flyvbjerg,et al.  Evolution in a rugged fitness landscape. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[50]  S. Tanksley Mapping polygenes. , 1993, Annual review of genetics.

[51]  Weinberger,et al.  RNA folding and combinatory landscapes. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[52]  J. Maienschein Growth of biological thought , 1994, Nature.

[53]  A. Perelson,et al.  Protein evolution on partially correlated landscapes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Schemske,et al.  Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus) , 1995, Nature.

[55]  D. Hartl,et al.  Compensatory nearly neutral mutations: selection without adaptation. , 1996, Journal of theoretical biology.

[56]  Z B Zeng,et al.  Genetic analysis of a morphological shape difference in the male genitalia of Drosophila simulans and D. mauritiana. , 1996, Genetics.

[57]  N. Takahata Neutral theory of molecular evolution. , 1996, Current opinion in genetics & development.

[58]  S. Heath,et al.  Imperfect genes, Fisherian mutation and the evolution of sex. , 1997, Genetics.

[59]  J. Bull,et al.  Exceptional convergent evolution in a virus. , 1997, Genetics.

[60]  M. Kearsey,et al.  QTL analysis in plants; where are we now? , 1998, Heredity.

[61]  D. Schemske,et al.  Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). , 1998, Genetics.

[62]  Narayanaswamy Balakrishnan,et al.  Records: Arnold/Records , 1998 .

[63]  J. Doebley,et al.  Of genes and genomes and the origin of maize. , 1998, Trends in genetics : TIG.

[64]  H. A. Orr,et al.  THE POPULATION GENETICS OF ADAPTATION: THE DISTRIBUTION OF FACTORS FIXED DURING ADAPTIVE EVOLUTION , 1998, Evolution; international journal of organic evolution.

[65]  Nick Barton,et al.  Evolutionary biology: The geometry of adaptation , 1998, Nature.

[66]  Jody Hey,et al.  The limits of selection during maize domestication , 1999, Nature.

[67]  H. A. Orr,et al.  The evolutionary genetics of adaptation: a simulation study. , 1999, Genetical research.

[68]  P. Stadler,et al.  Random field models for fitness landscapes , 1999 .

[69]  J. Bull,et al.  Different trajectories of parallel evolution during viral adaptation. , 1999, Science.

[70]  D. Stern,et al.  Divergence of larval morphology between Drosophila sechellia and its sibling species caused by cis-regulatory evolution of ovo/shaven-baby. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[71]  L. Cook The Genetical Theory of Natural Selection — A Complete Variorum Edition , 2000, Heredity.

[72]  H. A. Orr,et al.  ADAPTATION AND THE COST OF COMPLEXITY , 2000, Evolution; international journal of organic evolution.

[73]  Paul Embrechts,et al.  Extremes and Integrated Risk Management , 2000 .

[74]  Corbin D. Jones,et al.  Detecting the undetected: estimating the total number of loci underlying a quantitative trait. , 2000, Genetics.

[75]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[76]  Art Poon,et al.  COMPENSATING FOR OUR LOAD OF MUTATIONS: FREEZING THE MELTDOWN OF SMALL POPULATIONS , 2000, Evolution; international journal of organic evolution.

[77]  H. A. Orr,et al.  The genetics of species differences. , 2001 .

[78]  M Imhof,et al.  Fitness effects of advantageous mutations in evolving Escherichia coli populations. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[79]  A F Bennett,et al.  Genetic architecture of thermal adaptation in Escherichia coli. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[80]  B. Drossel Biological evolution and statistical physics , 2001, cond-mat/0101409.

[81]  P. Gerrish The rhythm of microbial adaptation , 2001, Nature.

[82]  N. Barton The role of hybridization in evolution , 2001, Molecular ecology.

[83]  J. Bull,et al.  Profiles of adaptation in two similar viruses. , 2001, Genetics.

[84]  J. Gillespie IS THE POPULATION SIZE OF A SPECIES RELEVANT TO ITS EVOLUTION? , 2001, Evolution; international journal of organic evolution.

[85]  Trudy F. C. Mackay,et al.  Quantitative trait loci in Drosophila , 2001, Nature Reviews Genetics.

[86]  Shizhong Xu QTL analysis in plants. , 2002, Methods in molecular biology.

[87]  P. Gerrish,et al.  Fitness Effects of Fixed Beneficial Mutations in Microbial Populations , 2002, Current Biology.

[88]  H. A. Orr,et al.  THE POPULATION GENETICS OF ADAPTATION: THE ADAPTATION OF DNA SEQUENCES , 2002, Evolution; international journal of organic evolution.

[89]  A. Parsons,et al.  Mode of selection and experimental evolution of antifungal drug resistance in Saccharomyces cerevisiae. , 2003, Genetics.

[90]  H. A. Orr,et al.  The distribution of fitness effects among beneficial mutations. , 2003, Genetics.

[91]  D. Schemske,et al.  Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers , 2003, Nature.

[92]  John J. Welch,et al.  MODULARITY AND THE COST OF COMPLEXITY , 2003, Evolution; international journal of organic evolution.

[93]  Clifford H. Taubes,et al.  Towards a theory of evolutionary adaptation , 2004, Genetica.

[94]  H. A. Orr,et al.  Theories of adaptation: what they do and don’t say , 2005, Genetica.

[95]  D. Schluter,et al.  The Genetic Architecture of Parallel Armor Plate Reduction in Threespine Sticklebacks , 2004, PLoS biology.

[96]  D. Schluter,et al.  Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks , 2004, Nature.

[97]  Rafael Sanjuán,et al.  The distribution of fitness effects caused by single-nucleotide substitutions in an RNA virus. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[98]  E. Weinberger,et al.  Correlated and uncorrelated fitness landscapes and how to tell the difference , 1990, Biological Cybernetics.

[99]  N. Barton Fitness Landscapes and the Origin of Species , 2004 .

[100]  J. Doebley The genetics of maize evolution. , 2004, Annual review of genetics.

[101]  Catherine A. Wilson,et al.  Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[102]  R. Punnett Mimicry in Butterflies , 2005, Zeitschrift für induktive Abstammungs- und Vererbungslehre.

[103]  Stuart A. Kauffman,et al.  ORIGINS OF ORDER , 2019, Origins of Order.

[104]  L. Penrose,et al.  THE CORRELATION BETWEEN RELATIVES ON THE SUPPOSITION OF MENDELIAN INHERITANCE , 2022 .