Evolutionary bet-hedging in the real world: empirical evidence and challenges revealed by plants

Understanding the adaptations that allow species to live in temporally variable environments is essential for predicting how they may respond to future environmental change. Variation at the intergenerational scale can allow the evolution of bet-hedging strategies: a novel genotype may be favoured over an alternative with higher arithmetic mean fitness if the new genotype experiences a sufficiently large reduction in temporal fitness variation; the successful genotype is said to have traded off its mean and variance in fitness in order to ‘hedge its evolutionary bets’. We review the evidence for bet-hedging in a range of simple plant systems that have proved particularly tractable for studying bet-hedging under natural conditions. We begin by outlining the essential theory, reiterating the important distinction between conservative and diversified bet-hedging strategies. We then examine the theory and empirical evidence for the canonical example of bet-hedging: diversification via dormant seeds in annual plants. We discuss the complications that arise when moving beyond this simple case to consider more complex life-history traits, such as flowering size in semelparous perennial plants. Finally, we outline a framework for accommodating these complications, emphasizing the central role that model-based approaches can play.

[1]  M. G. Bulmer,et al.  Selection for Iteroparity in a Variable Environment , 1985, The American Naturalist.

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

[3]  S. Tuljapurkar,et al.  Evolution of Delayed Reproduction in Uncertain Environments: A Life‐History Perspective , 2008, The American Naturalist.

[4]  J. P. Grime,et al.  Plant Strategies, Vegetation Processes, and Ecosystem Properties , 2006 .

[5]  J. P. Grime,et al.  A COMPARATIVE STUDY OF GERMINATION CHARACTERISTICS IN A LOCAL FLORA , 1981 .

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

[7]  Mark Rees,et al.  Life‐History Variation in Contrasting Habitats: Flowering Decisions in a Clonal Perennial Herb (Veratrum album) , 2008, The American Naturalist.

[8]  Shripad Tuljapurkar,et al.  Population Dynamics in Variable Environments , 1990 .

[9]  S. Tuljapurkar,et al.  Escape in time : stay young or age gracefully? , 2000 .

[10]  Richard P. Shefferson The evolutionary ecology of vegetative dormancy in mature herbaceous perennial plants , 2009 .

[11]  S. Ellner,et al.  Role of Overlapping Generations in Maintaining Genetic Variation in a Fluctuating Environment , 1994, The American Naturalist.

[12]  M. Rees,et al.  Evolution of size-dependent flowering in a variable environment: partitioning the effects of fluctuating selection , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[13]  R. Ferrière,et al.  Bet Hedging via Seed Banking in Desert Evening Primroses (Oenothera, Onagraceae): Demographic Evidence from Natural Populations , 2006, The American Naturalist.

[14]  D. Doak,et al.  Buffering of Life Histories against Environmental Stochasticity: Accounting for a Spurious Correlation between the Variabilities of Vital Rates and Their Contributions to Fitness , 2004, The American Naturalist.

[15]  Dylan Z Childs,et al.  Bet-hedging as an evolutionary game: the trade-off between egg size and number , 2010, Proceedings of the Royal Society B: Biological Sciences.

[16]  Mark Rees,et al.  Evolutionary demography of monocarpic perennials. , 2003 .

[17]  M. Johnston,et al.  Suboptimal timing of reproduction in Lobelia inflata may be a conservative bet‐hedging strategy , 2003, Journal of evolutionary biology.

[18]  Ken Thompson,et al.  The Ecology of Seeds: Contents , 2005 .

[19]  Lars Gustafsson,et al.  Single‐Generation Estimates of Individual Fitness as Proxies for Long‐Term Genetic Contribution , 2004, The American Naturalist.

[20]  B. Kendall,et al.  Longevity can buffer plant and animal populations against changing climatic variability. , 2008, Ecology.

[21]  S. Ellner,et al.  ESS germination strategies in randomly varying environments. I. Logistic-type models. , 1985, Theoretical population biology.

[22]  Joel s. Brown,et al.  The Selective Interactions of Dispersal, Dormancy, and Seed Size as Adaptations for Reducing Risk in Variable Environments , 1988, The American Naturalist.

[23]  C. Baskin,et al.  Seeds: Ecology, Biogeography, and, Evolution of Dormancy and Germination , 1998 .

[24]  J. Baskin,et al.  Studies on the autecology and population biology of the weedy monocarpic perennial, Pastinaca sativa , 1979 .

[25]  T. J. Walker Symposium: Insect Behavioral Ecology--85: Stochastic Polyphenism: Coping with Uncertainty , 1986 .

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

[27]  J. Bakker,et al.  Ecological correlates of seed persistence in soil in the north‐west European flora , 1998 .

[28]  Craig T. Sheldon The behaviour of seeds in soil. 3. The influence of seed morphology and the behaviour of seedlings on the establishment of plants from surface-lying seeds. , 1974 .

[29]  Niclas Jonzén,et al.  What is bet-hedging, really? , 2010, Proceedings of the Royal Society B: Biological Sciences.

[30]  S. Ellner,et al.  Integral Projection Models for Species with Complex Demography , 2006, The American Naturalist.

[31]  M. Rees,et al.  The Analysis and Interpretation of Seedling Recruitment Curves , 1993, The American Naturalist.

[32]  Peter Chesson,et al.  Quantifying and testing coexistence mechanisms arising from recruitment fluctuations. , 2003, Theoretical population biology.

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

[34]  Ken Thompson,et al.  The Ecology of Seeds by Michael Fenner , 2005 .

[35]  M. Rees Delayed Germination of Seeds: A Look at the Effects of Adult Longevity, the Timing of Reproduction, and Population Age/Stage Structure , 1994, The American Naturalist.

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

[37]  B. Kendall,et al.  Correctly Estimating How Environmental Stochasticity Influences Fitness and Population Growth , 2005, The American Naturalist.

[38]  William J. Browne,et al.  Using cross-classified multivariate mixed response models with application to life history traits in great tits (Parus major) , 2007 .

[39]  N. Kachi 21 – Evolution of Size-dependent Reproduction in Biennial Plants: A Demographic Approach , 1990 .

[40]  Jennifer L. Williams Flowering Life‐History Strategies Differ between the Native and Introduced Ranges of a Monocarpic Perennial , 2009, The American Naturalist.

[41]  D. Koons,et al.  Is life-history buffering or lability adaptive in stochastic environments? , 2009 .

[42]  Stephen P. Ellner,et al.  Germination dimorphisms and parent-offspring conflict in seed germination* , 1986 .

[43]  Stephen P. Ellner,et al.  Evolutionary demography of long‐lived monocarpic perennials: a time‐lagged integral projection model , 2008 .

[44]  S. Tuljapurkar,et al.  An uncertain life: demography in random environments. , 1989, Theoretical population biology.

[45]  Stephen P. Ellner,et al.  Stochastic stable population growth in integral projection models: theory and application , 2007, Journal of mathematical biology.

[46]  S. Ellner ESS Germination Strategies in Randomly Varying Environments , 2003 .

[47]  EVOLUTION IN THE REAL WORLD: STOCHASTIC VARIATION AND THE DETERMINANTS OF FITNESS IN CARLINA VULGARIS , 2002, Evolution; international journal of organic evolution.

[48]  Stephen P. Ellner,et al.  Evolution of complex flowering strategies: an age– and size–structured integral projection model , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[49]  J. Jensen Sur les fonctions convexes et les inégalités entre les valeurs moyennes , 1906 .

[50]  C. Pfister,et al.  Patterns of variance in stage-structured populations: evolutionary predictions and ecological implications. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[51]  W. S. Cooper,et al.  The Evolution of Developmental Plasticity in Reproductive Characteristics: An Application of the "Adaptive Coin-Flipping" Principle , 1984, The American Naturalist.

[52]  T. Philippi,et al.  Hedging one's evolutionary bets, revisited. , 1989, Trends in ecology & evolution.

[53]  G. Meszéna,et al.  Life Histories with Lottery Competition in a Stochastic Environment: ESSs which Do Not Prevail , 1995 .

[54]  Stephen P. Ellner,et al.  Integral projection models for populations in temporally varying environments , 2009 .

[55]  P. Krausman Soay Sheep: Dynamics and Selection in an Island Population , 2005 .

[56]  Lindsay A. Turnbull,et al.  The costs and benefits of fast living. , 2009, Ecology letters.

[57]  Stephen P. Ellner,et al.  Evolution of size–dependent flowering in a variable environment: construction and analysis of a stochastic integral projection model , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[58]  H. Michaels,et al.  Seed size variation: magnitude, distribution, and ecological correlates , 1988, Evolutionary Ecology.

[59]  C Jessica E Metcalf,et al.  Why evolutionary biologists should be demographers. , 2007, Trends in ecology & evolution.

[60]  J. Metz,et al.  Plant survival in relation to seed size along environmental gradients: a long‐term study from semi‐arid and Mediterranean annual plant communities , 2010, Journal of Ecology.

[61]  A. Sugden ECOLOGY/EVOLUTION: Phenotypic Plasticity , 2004 .

[62]  S. Tuljapurkar,et al.  Delayed reproduction and fitness in variable environments. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[63]  R. Lande,et al.  GENOTYPE‐ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY , 1985, Evolution; international journal of organic evolution.

[64]  REPRODUCTIVE EFFORT IN VARIABLE ENVIRONMENTS, OR ENVIRONMENTAL VARIATION IS FOR THE BIRDS , 2001 .

[65]  M. Rees Evolutionary ecology of seed dormancy and seed size , 1996 .

[66]  F. Menu,et al.  Adaptive Dynamics of Dormancy Duration Variability: Evolutionary Trade-Off and Priority Effect Lead to Suboptimal Adaptation , 2009, Evolution; international journal of organic evolution.

[67]  M. McPeek,et al.  Extinction dynamics, population growth and seed banks , 1993, Oecologia.

[68]  J. Ripa,et al.  Bet-hedging as an evolutionary game: the trade-off between egg size and number , 2009, Proceedings of the Royal Society B: Biological Sciences.

[69]  K. Trenberth,et al.  Modern Global Climate Change , 2003, Science.

[70]  C. Jessica E. Metcalf,et al.  Using Bayesian inference to understand the allocation of resources between sexual and asexual reproduction , 2009 .

[71]  H. Wilbur,et al.  Life‐History Evolution in Uncertain Environments: Bet Hedging in Time , 2006, The American Naturalist.

[72]  J. P. Grime,et al.  SEASONAL VARIATION IN THE SEED BANKS OF HERBACEOUS SPECIES IN TEN CONTRASTING HABITATS , 1979 .

[73]  M. Rees Trade-offs among dispersal strategies in British plants , 1993, Nature.

[74]  Mark Rees,et al.  Seed Dormancy and Delayed Flowering in Monocarpic Plants: Selective Interactions in a Stochastic Environment , 2006, The American Naturalist.

[75]  M. Johnston,et al.  ENVIRONMENTAL AND GENETIC SOURCES OF DIVERSIFICATION IN THE TIMING OF SEED GERMINATION: IMPLICATIONS FOR THE EVOLUTION OF BET HEDGING , 2006, Evolution; international journal of organic evolution.

[76]  Shripad Tuljapurkar,et al.  Structured-Population Models in Marine, Terrestrial, and Freshwater Systems , 1997, Population and Community Biology Series.

[77]  W. Elberse,et al.  Germination of Six Grassland Herbs in Microsites with Different Water Contents , 1976 .

[78]  M. Slatkin Hedging one's evolutionary bets , 1974, Nature.

[79]  Y. Buckley,et al.  Are invasives bigger? a global study of seed size variation in two invasive shrubs , 2003 .

[80]  On the Evolution of Coin-Flipping Plasticity: A Response to McGinley, Temme, and Geber , 1988, The American Naturalist.

[81]  Ken Thompson,et al.  The Ecology of Seeds: Seedling establishment , 2005 .

[82]  J. Gillespie Natural selection for within-generation variance in offspring number II. Discrite haploid models. , 1975, Genetics.

[83]  J H Gillespie,et al.  Nautural selection for within-generation variance in offspring number. , 1974, Genetics.

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

[85]  J. Lovett-Doust,et al.  Plant strategies, vegetation processes, and ecosystem properties , 2002 .