Pleiotropic mutation, modularity and evolvability

The relationship between pleiotropy and the rate of evolution of a phenotypic character (evolvability) in a population is explored using computer simulations. I present results that suggest the rate of evolution of a phenotypic character may not decline when that character is pleiotropically associated to an increasing number of other characters, provided that the characters are under pure directional selection such that they are far from their optima relative to the average magnitude of a mutation. These conditions may be relevant during adaptive radiations. Adding pleiotropic associations to a set of characters in which one is under directional selection and the other is under stabilizing selection increases the rate of adaptation of the character under directional selection provided that the new characters that come to be pleiotropically associated are under directional selection. Thus, increasing the number of pleiotropic associations under these conditions increases the rate of adaptation of a character.

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

[2]  Günter P. Wagner,et al.  Complex Adaptations and the Evolution of Evolvability , 2005 .

[3]  J. B. S. Haldane,et al.  A mathematical theory of natural and artificial selection—I , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[4]  R. Bürger.  CONSTRAINTS FOR THE EVOLUTION OF FUNCTIONALLY COUPLED CHARACTERS: A NONLINEAR ANALYSIS OF A PHENOTYPIC MODEL , 1986, Evolution; international journal of organic evolution.

[5]  MULTIVARIATE STABILIZING SELECTION AND PLEIOTROPY IN THE MAINTENANCE OF QUANTITATIVE GENETIC VARIATION , 2003, Evolution; international journal of organic evolution.

[6]  D. Thieffry,et al.  Modularity in development and evolution. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[7]  J. Bonner.  Cells, embryos, and evolution: Toward a cellular and developmental understanding of phenotypic variation and evolutionary adaptability , 1998 .

[8]  M. Whitlock,et al.  The genetics of adaptation: the roles of pleiotropy, stabilizing selection and drift in shaping the distribution of bidirectional fixed mutational effects. , 2003, Genetics.

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

[10]  J. Welch,et al.  Nonequivalent Loci and the distribution of mutant effects. , 2002, Genetics.

[11]  T. D. Iles,et al.  The cichlid fishes of the great lakes of Africa: their biology and evolution, , 1972 .

[12]  Günter P. Wagner,et al.  The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution , 1988 .

[13]  G. Wagner.  Coevolution of functionally constrained characters: prerequisites for adaptive versatility. , 1984, Bio Systems.

[14]  G. Wagner,et al.  Multivariate mutation-selection balance with constrained pleiotropic effects. , 1989, Genetics.

[15]  Mandy J. Haldane,et al.  A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation , 1927, Mathematical Proceedings of the Cambridge Philosophical Society.

[16]  G. von Dassow,et al.  Modularity in animal development and evolution: elements of a conceptual framework for EvoDevo. , 1999, The Journal of experimental zoology.

[17]  G. Wagner,et al.  Adaptive Inertia Caused by Hidden Pleiotropic Effects , 1997 .

[18]  Charles R. Brown,et al.  Ecology and Evolution of Darwin’s Finches , 2001, Heredity.

[19]  T. Mackay,et al.  Effects of single P-element insertions on bristle number and viability in Drosophila melanogaster. , 1996, Genetics.

[20]  A. Agresti,et al.  Approximate is Better than “Exact” for Interval Estimation of Binomial Proportions , 1998 .

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

[22]  Bret J. Pearson,et al.  Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. , 1999, Science.

[23]  J. S. Gale,et al.  Theoretical Population Genetics , 1990, Springer Netherlands.

[24]  S. Otto,et al.  Two steps forward, one step back: the pleiotropic effects of favoured alleles , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[25]  A. Yang,et al.  Modularity, evolvability, and adaptive radiations: a comparison of the hemi‐ and holometabolous insects , 2001, Evolution & development.

[26]  T. F. Hansen.  Is modularity necessary for evolvability? Remarks on the relationship between pleiotropy and evolvability. , 2003, Bio Systems.

[27]  L. Altenberg,et al.  PERSPECTIVE: COMPLEX ADAPTATIONS AND THE EVOLUTION OF EVOLVABILITY , 1996, Evolution; international journal of organic evolution.

[28]  T. Mackay,et al.  Effects of P element insertions on quantitative traits in Drosophila melanogaster. , 1992, Genetics.

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

[30]  D. Wake,et al.  Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes , 2003, Proceedings of the National Academy of Sciences of the United States of America.