Genetic niche‐hiking: an alternative explanation for the evolution of flammability

In fire-prone ecosystems, many plants possess traits that enhance their relative flammability and ecologists have suggested increased flammability could result from natural selection. To date, theoretical models addressing the evolution of flammable characteristics assume that flammable plants realize some direct fitness advantage. In this paper, we explore the idea that enhanced flammability can increase in frequency in a population without any direct fitness benefit to the flammable type. In our model, flammability evolves due to an association between an allele that promotes flammability and alleles at unlinked loci that give high fitness. In analogy to genetic hitchhiking, in which a deleterious allele can invade due to a genetic linkage, we call this process “genetic niche-hiking,” because the association results from localized niche construction. Specifically, flammable plants sacrifice themselves and their neighbors to produce local fire-cleared gaps (the constructed niche) in which their offspring are able to continually track an ever-changing environment. Niche-hiking requires that mating, dispersal and niche construction all occur locally (i.e. the population is spatially structured), such that offspring are likely to experience the niches their parents construct. Using a spatially-explicit lattice-based simulation, we find that increased flammability can evolve despite the “self-killing” cost of such a trait. Genetic niche-hiking may also be applicable to the evolution of other traits in spatially structured ecological systems such as plant disease susceptibility and forest tree characteristics that influence gap production.

[1]  B. V. Wilgen,et al.  The role of vegetation structure and fuel chemistry in excluding fire from forest patches in the fire prone fynbos shrublands of south africa , 1990 .

[2]  A. Hastings Evolution of Life Histories , 1997 .

[3]  J. Pate,et al.  For everything a season: smoke-induced seed germination and seedling recruitment in a Western Australian Banksia woodland , 1998 .

[4]  Yoh Iwasa,et al.  The Geometry of Ecological Interactions: Pair Approximations for Lattice-based Ecological Models , 2000 .

[5]  N. Enright,et al.  Demography of a non-sprouting and resprouting Hakea species (Proteaceae) in fire-prone Eucalyptus woodlands of southeastern Australia in relation to stand age, drought and disease , 1999, Plant Ecology.

[6]  Ulf Dieckmann,et al.  Moment Approximations of Individual-based Models , 1999 .

[7]  J. Keeley,et al.  Role of allelopathy, heat and charred wood in the germination of chaparral herbs and suffrutescents , 1985 .

[8]  James F. Jackson,et al.  Allometry of Constitutive Defense: A Model and a Comparative Test with Tree Bark and Fire Regime , 1999, The American Naturalist.

[9]  Robert W. Mutch,et al.  Wildland Fires and Ecosystems--A Hypothesis , 1970 .

[10]  A. Troumbis Some questions about fammability in fire ecology , 1989 .

[11]  Peter Kareiva,et al.  Spatial ecology : the role of space in population dynamics and interspecific interactions , 1998 .

[12]  P. Higgs,et al.  Population evolution on a multiplicative single-peak fitness landscape. , 1996, Journal of theoretical biology.

[13]  F. Went,et al.  Fire and Biotic Factors Afecting Germination , 1952 .

[14]  David D. Ackerly,et al.  Flammability and serotiny as strategies: correlated evolution in pines , 2001 .

[15]  N. Christensen,et al.  Relative Importance of Factors Controlling Germination and Seedling Survival in Adenostoma Chaparral , 1975 .

[16]  J. Burdon,et al.  The effect of small-scale environmental changes on disease incidence and severity in a natural plant-pathogen interaction , 1988, Oecologia.

[17]  Yoh Iwasa,et al.  The Geometry of Ecological Interactions: Lattice Models and Pair Approximation in Ecology , 2000 .

[18]  Michael Travisano,et al.  Adaptive radiation in a heterogeneous environment , 1998, Nature.

[19]  J. Keeley,et al.  Role of high fire frequency in destruction of mixed chaparral. , 1993 .

[20]  D. Odion,et al.  FIRE, SOIL HEATING, AND THE FORMATION OF VEGETATION PATTERNS IN CHAPARRAL , 2000 .

[21]  Y. Iwasa,et al.  Allelopathy of bacteria in a lattice population: Competition between colicin-sensitive and colicin-producing strains , 1998, Evolutionary Ecology.

[22]  F. J. Odling-Smee,et al.  Evolutionary consequences of niche construction and their implications for ecology. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Burdon,et al.  The ecological genetics of plant-pathogen interactions in natural communities , 1988 .

[24]  S. K. Rice Vegetation establishment in post-fire Adenostoma chaparral in relation to fine-scale pattern in fire intensity and soil nutrients , 1993 .

[25]  Simon A. Levin,et al.  The Geometry of Ecological Interactions: Moment Methods for Ecological Processes in Continuous Space , 2000 .

[26]  M. C. Heath Evolution of resistance to fungal parasitism in natural ecosystems , 1991 .

[27]  W. Bond,et al.  Convergent seed germination in South African fynbos and Californian chaparral , 1997, Plant Ecology.

[28]  J. Snyder The Role of Fire: Mutch Ado about Nothing? , 1984 .

[29]  C. Tyler,et al.  The effects of neighbors on the growth and survival of shrub seedlings following fire , 1995, Oecologia.

[30]  Thomas M. Smith,et al.  Plant functional types : their relevance to ecosystem properties and global change , 1998 .

[31]  F. J. Odling-Smee,et al.  The evolutionary consequences of niche construction: a theoretical investigation using two‐locus theory , 1996 .

[32]  Marcus W. Feldman,et al.  Rekindling an old flame: A haploid model for the evolution and impact of flammability in resprouting plants , 1999 .

[33]  J. M. Smith,et al.  Selection for recombination in a polygenic model , 1980 .

[34]  W. Bond,et al.  The intermediate disturbance hypothesis does not explain fire and diversity pattern in fynbos , 1997, Plant Ecology.

[35]  P. Rundel Structural and chemical components of flammability [Fire adapted plant species, evolution, canopy structure, includes forest trees, grasses, shrubs] , 1981 .

[36]  J. M. Smith,et al.  Selection for recombination in a polygenic model--the mechanism. , 1988, Genetical research.

[37]  Ulf Dieckmann,et al.  The Geometry of Ecological Interactions: Simplifying Spatial Complexity , 2000 .

[38]  Marcus W. Feldman,et al.  Niche Construction , 2003 .

[39]  C. Castell,et al.  Comparative genet survival after fire in woody Mediterranean species , 1992, Oecologia.

[40]  S. Vaughan Up in smoke? , 1994, British Dental Journal.

[41]  S. Levin,et al.  Theories of Simplification and Scaling of Spatially Distributed Processes , 2011 .

[42]  M. Feldman,et al.  Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors , 2002, Nature.

[43]  R. Whelan,et al.  Variation in bradyspory and seedling recruitment without fire among populations of Banksia serrata (Proteaceae) , 1998 .

[44]  Leslie A. Real,et al.  Spatial pattern and process in plant-pathogen interactions , 1996 .

[45]  M. Andersen Mechanistic Models for the Seed Shadows of Wind-Dispersed Plants , 1991, The American Naturalist.

[46]  P. Wells THE RELATION BETWEEN MODE OF REPRODUCTION AND EXTENT OF SPECIATION IN WOODY GENERA OF THE CALIFORNIA CHAPARRAL , 1969, Evolution; international journal of organic evolution.

[47]  L. Chao,et al.  Structured habitats and the evolution of anticompetitor toxins in bacteria. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[48]  J. Keeley,et al.  Trace gas emissions and smoke-induced seed germination , 1997 .

[49]  J. Pate,et al.  Growth and Fire Response of Selected Epacridaceae of South-Western Australia , 1996 .

[50]  R. D Allelopathy in Spatially Distributed Populations , 1997 .

[51]  R. Lewontin The organism as the subject and object of evolution , 1983 .

[52]  C. Tyler Relative Importance of Factors Contributing to Postfire Seedling Establishment in Maritime Chaparral , 1996 .

[53]  L. Trabaud,et al.  Comparative study of the aerial structure of five shrubs of Mediterranean shrublands , 1991 .

[54]  G. B. Williamson,et al.  High temperature of forest fires under pines as a selective advantage over oaks , 1981, Nature.

[55]  W. Oechel,et al.  Demography of Adenostoma fasciculatum after fires of different intensities in southern California chaparral , 1993, Oecologia.

[56]  C. Benkman Wind dispersal capacity of pine seeds and the evolution of different seed dispersal modes in pines , 1995 .

[57]  J. Keeley Demographic structure of California chaparral in the long-term absence of fire , 1992 .

[58]  J. Mills Herbivory and seedling establishment in post-fire southern California chaparral , 1983, Oecologia.

[59]  W. Bond,et al.  Are Protea populations seed limited? Implications for wildflower harvesting in Cape fynbos , 1996 .

[60]  P. Raven The Evolution of Mediterranean Floras , 1973 .

[61]  William J. Bond,et al.  Kill thy neighbour: an individulalistic argument for the evolution of flammability , 1995 .

[62]  Peter J. Bellingham,et al.  Resprouting as a life history strategy in woody plant communities , 2000 .

[63]  B. Lamont,et al.  A test for lottery recruitment among four Banksia species based on their demography and biological attributes , 1995, Oecologia.

[64]  J. Keeley,et al.  Evolution of life histories in Pinus , 1998 .

[65]  M. Parker Individual variation in pathogen attack and differential reproductive success in the annual legume, Amphicarpaea bracteata , 1986, Oecologia.

[66]  W. Bond,et al.  The costs of leaving home: ants disperse myrmecochorous seeds to low nutrient sites , 1989, Oecologia.