The fitness value of information

Communication and information are central concepts in evolutionary biology. In fact, it is hard to find an area of biology where these concepts are not used. However, quantifying the information transferred in biological interactions has been difficult. How much information is transferred when the first spring rainfall hits a dormant seed, or when a chick begs for food from its parent? One measure that is commonly used in such cases is fitness value: by how much, on average, an individual's fitness would increase if it behaved optimally with the new information, compared to its average fitness without the information. Another measure, often used to describe neural responses to sensory stimuli, is the mutual information-a measure of reduction in uncertainty, as introduced by Shannon in communication theory. However, mutual information has generally not been considered to be an appropriate measure for describing developmental or behavioral responses at the organismal level, because it is blind to function; it does not distinguish between relevant and irrelevant information. In this paper we show that there is in fact a surprisingly tight connection between these two measures in the important context of evolution in an uncertain environment. In this case, a useful measure of fitness benefit is the increase in the long-term growth rate, or the fold increase in number of surviving lineages. We show that in many cases the fitness value of a developmental cue, when measured this way, is exactly equal to the reduction in uncertainty about the environment, as described by the mutual information.

[1]  Thomas M. Cover,et al.  Elements of Information Theory (Wiley Series in Telecommunications and Signal Processing) , 2006 .

[2]  John Maynard Smith,et al.  The Idea of Information in Biology , 1999, The Quarterly Review of Biology.

[3]  M. L. Crump Variation in Propagule Size as a Function of Environmental Uncertainty for Tree Frogs , 1981, The American Naturalist.

[4]  E. Dempster Maintenance of genetic heterogeneity. , 1955, Cold Spring Harbor symposia on quantitative biology.

[5]  J. B. S. Haldane,et al.  The cost of natural selection , 1957, Journal of Genetics.

[6]  Lloyd Demetrius,et al.  Statistical mechanics and population biology , 1983 .

[7]  Joel P. Brockman,et al.  What is Bet-Hedging , 1987 .

[8]  G. Llorente,et al.  A comparative analysis of the adaptive developmental plasticity hypothesis in six Mediterranean anuran species along a pond permanency gradient , 2006 .

[9]  Andreas Wagner,et al.  Faculty Opinions recommendation of Bacterial persistence: a model of survival in changing environments. , 2005 .

[10]  D. Stephens Variance and the Value of Information , 1989, The American Naturalist.

[11]  J. Haldane,et al.  Polymorphism due to selection of varying direction , 1963, Journal of Genetics.

[12]  Carl T. Bergstrom,et al.  Phenotypic diversity as an adaptation to environmental uncertainty , 2008 .

[13]  Mill Johannes G.A. Van,et al.  Transmission Of Information , 1961 .

[14]  D. Cohen Optimizing reproduction in a randomly varying environment. , 1966, Journal of theoretical biology.

[15]  Dennis V. Lindley,et al.  An Introduction to Bayesian Inference and Decision , 1974 .

[16]  R. Lewontin,et al.  On population growth in a randomly varying environment. , 1969, Proceedings of the National Academy of Sciences of the United States of America.

[17]  S. Leibler,et al.  Bacterial Persistence , 2005, Genetics.

[18]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[19]  D. L. Venable,et al.  Seed Germination in Desert Annuals: An Empirical Test of Adaptive Bet Hedging , 2000, The American Naturalist.

[20]  A. Simons Fluctuating natural selection accounts for the evolution of diversification bet hedging , 2009, Proceedings of the Royal Society B: Biological Sciences.

[21]  Joseph Felsenstein,et al.  Macroevolution in a Model Ecosystem , 1978, The American Naturalist.

[22]  John L. Kelly,et al.  A new interpretation of information rate , 1956, IRE Trans. Inf. Theory.

[23]  M. Mead,et al.  Cybernetics , 1953, The Yale Journal of Biology and Medicine.

[24]  M. Lachmann,et al.  The inheritance of phenotypes: an adaptation to fluctuating environments. , 1996, Journal of theoretical biology.

[25]  V. Jansen,et al.  Evolution and population dynamics in stochastic environments , 1996, Researches on Population Ecology.

[26]  Carl T. Bergstrom,et al.  Shannon information and biological fitness , 2004, Information Theory Workshop.

[27]  I. Good On the Principle of Total Evidence , 1967 .

[28]  P. Kindlmann,et al.  Dynamics of Production of Sexual Forms in Aphids: Theoretical and Experimental Evidence for Adaptive “Coin‐Flipping” Plasticity , 2004, The American Naturalist.

[29]  Y. Iwasa,et al.  Optimal Mixed Strategies in Stochastic Environments , 1995 .

[30]  T. Philippi Bet-Hedging Germination of Desert Annuals: Variation Among Populations and Maternal Effects in Lepidium lasiocarpum , 1993, The American Naturalist.

[31]  P. Redbo-Torstensson,et al.  Cleistogamy as a bet‐hedging strategy in Oxalis acetosella, a perennial herb , 1998 .

[32]  Robert L. Winkler,et al.  An Introduction to Bayesian Inference and Decision , 1972 .

[33]  T. Philippi Bet-Hedging Germination of Desert Annuals: Beyond the First Year , 1993, The American Naturalist.

[34]  N. Sahlin Weight of the Value of Knowledge , 1990 .

[35]  D. Cohen,et al.  Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. , 1967, Journal of theoretical biology.

[36]  D. L. Venable,et al.  DORMANCY AND GERMINATION IN A GUILD OF SONORAN DESERT ANNUALS , 2004 .

[37]  J. Crow,et al.  Shannon's brief foray into genetics. , 2001, Genetics.

[38]  M. Mahony,et al.  Larval anurans with synchronous and asynchronous development periods: contrasting responses to water reduction and predator presence , 2002 .

[39]  M. Kimura Natural selection as the process of accumulating genetic information in adaptive evolution , 1961 .

[40]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[41]  J. P. Gould Risk, stochastic preference, and the value of information , 1974 .

[42]  J. Gillespie Polymorphism in random environments , 1973 .

[43]  T. Philippi,et al.  HABITAT EPHEMERALITY AND HATCHING FRACTIONS OF A DIAPAUSING ANOSTRACAN (CRUSTACEA: BRANCHIOPODA) , 2001 .

[44]  S. Leibler,et al.  Phenotypic Diversity, Population Growth, and Information in Fluctuating Environments , 2005, Science.

[45]  George Schlesinger Location and Range , 1990 .

[46]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

[48]  Carl T. Bergstrom,et al.  The disadvantage of combinatorial communication , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  Joseph Felsenstein,et al.  On the Biological Significance of the Cost of Gene Substitution , 1971, The American Naturalist.

[50]  C. Shannon,et al.  An algebra for theoretical genetics , 1940 .

[51]  A. R.,et al.  Risky Business : Sexual and Asexual Reproduction in Variable Environments , 1999 .

[52]  H. Nyquist,et al.  Certain factors affecting telegraph speed , 1924, Journal of the A.I.E.E..

[53]  M. Koops,et al.  Environmental predictability and the cost of imperfect information: influences on offspring size variability , 2003 .

[54]  D. L. Venable Bet hedging in a guild of desert annuals. , 2007, Ecology.

[55]  D. Reznick,et al.  The relationship between habitat permanence and larval development in California spadefoot toads: field and laboratory comparisons of developmental plasticity , 2004 .

[56]  B. Danforth Emergence dynamics and bet hedging in a desert bee, Perdita portalis , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[57]  W. S. Cooper,et al.  Adaptive "coin-flipping": a decision-theoretic examination of natural selection for random individual variation. , 1982, Journal of theoretical biology.