PERSPECTIVE: GENETIC ASSIMILATION AND A POSSIBLE EVOLUTIONARY PARADOX: CAN MACROEVOLUTION SOMETIMES BE SO FAST AS TO PASS US BY?

Abstract.— The idea of genetic assimilation, that environmentally induced phenotypes may become genetically fixed and no longer require the original environmental stimulus, has had varied success through time in evolutionary biology research. Proposed by Waddington in the 1940s, it became an area of active empirical research mostly thanks to the efforts of its inventor and his collaborators. It was then attacked as of minor importance during the “hardening” of the neo‐Darwinian synthesis and was relegated to a secondary role for decades. Recently, several papers have appeared, mostly independently of each other, to explore the likelihood of genetic assimilation as a biological phenomenon and its potential importance to our understanding of evolution. In this article we briefly trace the history of the concept and then discuss theoretical models that have newly employed genetic assimilation in a variety of contexts. We propose a typical scenario of evolution of genetic assimilation via an intermediate stage of phenotypic plasticity and present potential examples of the same. We also discuss a conceptual map of current and future lines of research aimed at exploring the actual relevance of genetic assimilation for evolutionary biology.

[1]  P. Doughty Testing the ecological correlates of phenotypically plastic traits within a phylogenetic framework , 1995 .

[2]  E. Jablonka,et al.  'Lamarckian' mechanisms in darwinian evolution. , 1998, Trends in ecology & evolution.

[3]  P. V. Tienderen Morphological variation in Plantago lanceolata : limits of plasticity , 1990 .

[4]  C. Goodnight EPISTASIS AND THE INCREASE IN ADDITIVE GENETIC VARIANCE: IMPLICATIONS FOR PHASE 1 OF WRIGHT'S SHIFTING‐BALANCE PROCESS , 1995, Evolution; international journal of organic evolution.

[5]  S. Gould,et al.  Punctuated equilibria: an alternative to phyletic gradualism , 1972 .

[6]  N. Barton,et al.  PERSPECTIVE: A CRITIQUE OF SEWALL WRIGHT'S SHIFTING BALANCE THEORY OF EVOLUTION , 1997, Evolution; international journal of organic evolution.

[7]  S. Gould,et al.  Exaptation—a Missing Term in the Science of Form , 1982, Paleobiology.

[8]  C. Goodnight THE INFLUENCE OF ENVIRONMENTAL VARIATION ON GROUP AND INDIVIDUAL SELECTION IN A CRESS , 1985, Evolution; international journal of organic evolution.

[9]  Günter P. Wagner,et al.  Adaptation and the Modular Design of Organisms , 1995, ECAL.

[10]  T. Schoener,et al.  ADAPTATION AND CONSTRAINT IN THE EVOLUTION OF SPECIALIZATION OF BAHAMIAN ANOLIS LIZARDS , 1994, Evolution; international journal of organic evolution.

[11]  M J Wade,et al.  Wright's shifting balance theory: an experimental study , 1991, Science.

[12]  S. Gavrilets ON PHASE THREE OF THE SHIFTING‐BALANCE THEORY , 1996, Evolution; international journal of organic evolution.

[13]  Andreas Wagner,et al.  Redundant Gene Functions and Natural Selection , 1997 .

[14]  S. Giessler Analysis of reticulate relationships within the , 1997 .

[15]  J. Tufto The Evolution of Plasticity and Nonplastic Spatial and Temporal Adaptations in the Presence of Imperfect Environmental Cues , 2000, The American Naturalist.

[16]  L. Nunney,et al.  THE MAINTENANCE OF SEX BY GROUP SELECTION , 1989, Evolution; international journal of organic evolution.

[17]  N. Barton ON THE SPREAD OF NEW GENE COMBINATIONS IN THE THIRD PHASE OF WRIGHT'S SHIFTING‐BALANCE , 1992, Evolution; international journal of organic evolution.

[18]  J. Gurevitch,et al.  Sources of variation in leaf shape among two populations of Achillea lanulosa. , 1992, Genetics.

[19]  T. Guilford,et al.  Aposematism: To be red or dead , 2000 .

[20]  S. Scheiner Genetics and Evolution of Phenotypic Plasticity , 1993 .

[21]  C. Fenster,et al.  Developmental Homeostasis and Floral Form: Evolutionary Consequences and Genetic Basis , 1997, International Journal of Plant Sciences.

[22]  M. West-Eberhard Phenotypic Plasticity and the Origins of Diversity , 1989 .

[23]  P. Cornillon,et al.  Autoregressive models for estimating phylogenetic and environmental effects: accounting for within-species variations. , 2000, Journal of theoretical biology.

[24]  J. Stewart,et al.  MOLECULAR EVIDENCE FOR HOMOPLOID RETICULATE EVOLUTION AMONG AUSTRALIAN SPECIES OF GOSSYPIUM , 1991, Evolution; international journal of organic evolution.

[25]  S. Lindquist,et al.  Hsp90 as a capacitor for morphological evolution , 1998, Nature.

[26]  C. Pál,et al.  Plasticity, memory and the adaptive landscape of the genotype , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[27]  J. Gurevitch,et al.  Boundary layer properties of highly dissected leaves: an investigation using an electrochemical fluid tunnel. , 1990 .

[28]  PLASTICITY TO LIGHT CUES AND RESOURCES IN ARABIDOPSIS THALIANA: TESTING FOR ADAPTIVE VALUE AND COSTS , 2000, Evolution; international journal of organic evolution.

[29]  I. Mysterud Unto others: The evolution and psychology of unselfish behavior , 1999 .

[30]  P. Alberch From genes to phenotype: dynamical systems and evolvability , 2004, Genetica.

[31]  M. Pigliucci,et al.  Phenotypic Evolution: A Reaction Norm Perspective , 1998 .

[32]  S. Jain,et al.  Phenotypic Placticity of Avena fatua and A. barbata , 1968, The American Naturalist.

[33]  J. Clausen,et al.  THE BALANCE BETWEEN COHERENCE AND VARIATION IN EVOLUTION. , 1960, Proceedings of the National Academy of Sciences of the United States of America.

[34]  J. Clausen,et al.  Effect of varied environments on western North American plants , 1940 .

[35]  C. Waddington,et al.  Selection of the Genetic Basis for an Acquired Character , 1952, Nature.

[36]  A. C. Fabergé,et al.  Breakage of Chromosomes Produced by Ultra-violet Radiation in Drosophila , 1952, Nature.

[37]  Giles Mayley,et al.  Landscapes, Learning Costs, and Genetic Assimilation , 1996, Evolutionary Computation.

[38]  J. Kenyon MODELS OF RETICULATE EVOLUTION IN THE CORAL GENUS ACROPORA BASED ON CHROMOSOME NUMBERS: PARALLELS WITH PLANTS , 1997, Evolution; international journal of organic evolution.

[39]  A. D. Bradshaw,et al.  Evolutionary Significance of Phenotypic Plasticity in Plants , 1965 .

[40]  S. Sultan Evolutionary Implications of Phenotypic Plasticity in Plants , 1987 .

[41]  L. Dugatkin,et al.  Group Selection and Assortative Interactions , 1997, The American Naturalist.

[42]  S. Sultan Phenotypic plasticity and plant adaptation , 1995 .

[43]  J. Gurevitch Variation in leaf dissection and leaf energy budgets among populations of Achillea from an altitudinal gradient , 1988 .

[44]  I. Eshel,et al.  Canalization, genetic assimilation and preadaptation. A quantitative genetic model. , 1998, Genetics.

[45]  S. Gilbert Ecological developmental biology: developmental biology meets the real world. , 2001, Developmental biology.

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

[47]  E. Mayr,et al.  The Evolutionary synthesis : perspectives on the unification of biology , 1980 .

[48]  Pigliucci,et al.  Evolution of phenotypic plasticity a comparative approach in the phylogenetic neighbourhood of Arabidopsis thaliana , 1999 .

[49]  J. Baldwin A New Factor in Evolution , 1896, The American Naturalist.

[50]  Mark Kirkpatrick,et al.  Quantum Evolution and Punctuated Equilibria in Continuous Genetic Characters , 1982, The American Naturalist.

[51]  G. Holloway,et al.  Phenotypic Plasticity: Beyond Nature and Nurture , 2002, Heredity.

[52]  G. Sword A role for phenotypic plasticity in the evolution of aposematism , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[53]  COSTS OF PLASTICITY IN FORAGING CHARACTERISTICS OF THE CLONAL PLANT RANUNCULUS REPTANS , 2000, Evolution; international journal of organic evolution.

[54]  R. Shine,et al.  Reconstructing ancestral reaction norms : an example using the evolution of reptilian viviparity , 1996 .

[55]  Imre Lakatos,et al.  The Methodology of Scientific Research Programmes , 1978 .

[56]  J. Klein PHYLETIC GRADUALISM VERSUS PUNCTUATED EQUILIBRIA : WHY CASE HISTORIES DO NOT SUFFICE , 1995 .

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

[58]  C. Waddington Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[59]  David B Goldstein,et al.  MAINTENANCE OF POLYGENIC VARIATION IN SPATIALLY STRUCTURED POPULATIONS: ROLES FOR LOCAL MATING AND GENETIC REDUNDANCY , 1992, Evolution; international journal of organic evolution.

[60]  F. B. Pickett,et al.  Seeing double: appreciating genetic redundancy. , 1995, The Plant cell.

[61]  Russell D. Gray,et al.  Replicator II – Judgement Day , 1997 .

[62]  Carl D. Schlichting,et al.  The Evolution of Phenotypic Plasticity in Plants , 1986 .

[63]  C. Waddington,et al.  GENETIC ASSIMILATION OF AN ACQUIRED CHARACTER , 1953 .

[64]  V. Savolainen,et al.  Phylogeny of the Celastraceae inferred from phytochrome B gene sequence and morphology. , 2001, American journal of botany.

[65]  S Wright,et al.  "Surfaces" of selective value. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[66]  Eva Jablonka,et al.  Epigenetic inheritance in evolution , 1998 .

[67]  Patrick C Phillips,et al.  PEAK SHIFTS AND POLYMORPHISM DURING PHASE THREE OF WRIGHT'S SHIFTING‐BALANCE PROCESS , 1993, Evolution; international journal of organic evolution.

[68]  EVOLUTIONARY IMPLICATIONS OF PHENOTYPIC PLASTICITY IN THE HINDLIMB OF THE LIZARD ANOLIS SAGREI , 2000, Evolution; international journal of organic evolution.

[69]  Michael D. Vose,et al.  Rapid parapatric speciation on holey adaptive landscapes , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  Stephen P Ellner,et al.  A SPATIALLY EXPLICIT STOCHASTIC MODEL DEMONSTRATES THE FEASIBILITY OF WRIGHT'S SHIFTING BALANCE THEORY , 1998, Evolution; international journal of organic evolution.

[71]  S. Gavrilets Evolution and speciation on holey adaptive landscapes. , 1997, Trends in ecology & evolution.

[72]  D. Schluter,et al.  A COMPARISON OF TWO STICKLEBACKS , 1994, Evolution; international journal of organic evolution.

[73]  M. Pigliucci,et al.  Control of Phenotypic Plasticity Via Regulatory Genes , 1993, The American Naturalist.

[74]  A. Cobb,et al.  An Investigation of Wound Healing in Sugar Beet Roots Using Light and Fluorescence Microscopy , 2001 .

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

[76]  S. Giessler Analysis of reticulate relationships within the Daphnia longispina species complex. Allozyme phenotype and morphology , 1997 .

[77]  K. Crandall,et al.  Intraspecific gene genealogies: trees grafting into networks. , 2001, Trends in ecology & evolution.

[78]  Was Wright right? , 1991, Science.

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

[80]  B. Walsh,et al.  Evolutionary Quantitative Genetics , 2019, Handbook of Statistical Genomics.

[81]  C. Pál,et al.  Epigenetic inheritance, genetic assimilation and speciation. , 1999, Journal of theoretical biology.

[82]  S. Tonsor,et al.  A SIMULATION OF WRIGHT'S SHIFTING‐BALANCE PROCESS: MIGRATION AND THE THREE PHASES , 1994, Evolution; international journal of organic evolution.

[83]  Larry Bull,et al.  On the Baldwin Effect , 1999, Artificial Life.

[84]  M. Pigliucci,et al.  Developmental phenotypic plasticity: where ecology and evolution meet molecular biology. , 1997, BioEssays : news and reviews in molecular, cellular and developmental biology.

[85]  M. C. Grant,et al.  Associations Among Protein Heterozygosity, Growth Rate, and Developmental Homeostasis , 1984 .

[86]  C. Hubbs Experimental Studies on the Nature of Species. I. Effect of Varied Environments on Western North American Plants.Jens Clausen , David D. Keck , William M. Hiesey , 1941 .

[87]  C H WADDINGTON,et al.  Genetic assimilation. , 1961, Advances in genetics.

[88]  J. Buskirk THE COSTS OF AN INDUCIBLE DEFENSE IN ANURAN LARVAE , 2000 .

[89]  A. Bleecker,et al.  A Mutation Altering Auxin Homeostasis and Plant Morphology in Arabidopsis. , 1995, The Plant cell.

[90]  Takahiro Sasaki,et al.  Evolving Learnable Neural Networks Under Changing Environments with Various Rates of Inheritance of Acquired Characters: Comparison of Darwinian and Lamarckian Evolution , 1999, Artificial Life.

[91]  G. Sword Density-dependent warning coloration , 1999, Nature.

[92]  Michael Fisher,et al.  Evolutionary synthesis of analog networks , 2005 .

[93]  M. Whitlock,et al.  VARIANCE‐INDUCED PEAK SHIFTS , 1995, Evolution; international journal of organic evolution.

[94]  M. Slatkin,et al.  PEAK SHIFTS PRODUCED BY CORRELATED RESPONSE TO SELECTION , 1993, Evolution; international journal of organic evolution.

[95]  Harry Smith,et al.  Phytochromes and light signal perception by plants—an emerging synthesis , 2000, Nature.

[96]  M. Whitlock FOUNDER EFFECTS AND PEAK SHIFTS WITHOUT GENETIC DRIFT: ADAPTIVE PEAK SHIFTS OCCUR EASILY WHEN ENVIRONMENTS FLUCTUATE SLIGHTLY , 1997, Evolution; international journal of organic evolution.

[97]  R. Emery,et al.  Phenotypic plasticity of stem elongation in two ecotypes of Stellaria longipes: the role of ethylene and response to wind , 1994 .

[98]  Hepsa Ely,et al.  The Material Basis of Evolution , 1915, Nature.

[99]  Geoffrey E. Hinton,et al.  How Learning Can Guide Evolution , 1996, Complex Syst..

[100]  M. Pigliucci,et al.  Manipulative Approaches to Testing Adaptive Plasticity: Phytochrome‐Mediated Shade‐Avoidance Responses in Plants , 1999, The American Naturalist.

[101]  D. Wilson,et al.  Costs and limits of phenotypic plasticity. , 1998, Trends in ecology & evolution.