Lessons on Evolution from the Study of Edaphic Specialization

Abstract

Plants adapted to special soil types are ideal for investigating evolutionary processes, including maintenance of intraspecific variation, adaptation, reproductive isolation, ecotypic differentiation, and the tempo and mode of speciation. Common garden and reciprocal transplant approaches show that both local adaptation and phenotypic plasticity contribute to edaphic (soil-related) specialization. Edaphic specialists evolve rapidly and repeatedly in some lineages, offering opportunities to investigate parallel evolution, a process less commonly documented in plants than in animals. Adaptations to soil features are often under the control of major genes and they frequently have direct or indirect effects on genes that contribute to reproductive isolation. Both reduced competitiveness and greater susceptibility to herbivory have been documented among some edaphic specialists when grown in ‘normal’ soils, suggesting that a high physiological cost of tolerance may result in strong divergent selection across soil boundaries. Interactions with microbes, herbivores, and pollinators influence soil specialization either by directly enhancing tolerance to extremes in soil conditions or by reducing gene flow between divergent populations. Climate change may further restrict the distribution of edaphic specialists due to increased competition from other taxa or, expand their ranges, if preadaptations to drought or other abiotic stressors render them more competitive under a novel climate.

This is a preview of subscription content, log in to check access.

Fig. 1

Literature Cited

  1. Abbott, R. J., M. J. Hegarty, S. J. Hiscock & A. C. Brennan. 2010. Homoploid hybrid speciation in action. Taxon 59: 1375–1386.

    Google Scholar 

  2. ———, D. Albach, S. Ansell, J. W. Arntzen, S. J. E. Baird, N. Bierne, J. Boughman, A. Brelsford, C. A. Buerkle, R. Buggs, R. K. Butlin, U. Dieckmann, F. Eroukhmanoff, A. Grill, S. H. Cahan, J. S. Hermansen, G. Hewitt, A. G. Hudson, C. Jiggins, J. Jones, B. Keller, T. Marczewski, J. Mallet, P. Martinez-Rodriguez, M. Möst, S. Mullen, R. Nichols, A. W. Nolte, C. Parisod, K. Pfennig, A. M. Rice, M. G. Ritchie, B. Seifert, C. M. Smadja, R. Stelkens, J. M. Szymura, R. Väinölä, J. B. W. Wolf & D. Zinner. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26: 229–246.

  3. Al-Hiyali, S. A. K., T. McNeilly, A. D. Bradshaw & A. M. Mortimer. 1993. The effect of zinc contamination from electricity pylons. Genetic constraints on selection for zinc tolerance. Heredity 70: 22–32.

    Article  Google Scholar 

  4. Anacker, B. L. 2011. Phylogenetic patterns of endemism and diversity. Pp. 49–79. In: S.P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  5. ———, J. Whittall, E. Goldberg & S. P. Harrison. 2011. Origins and consequences of serpentine endemism in the California flora. Evolution 65: 365–376.

  6. ——— & S. P. Harrison. 2012. Climate and the evolution of serpentine endemism in California. Evolutionary Ecology 26: 1011–1023.

  7. ——— 2014. The nature of serpentine endemism. American Journal of Botany 101: 219–224.

    PubMed  Article  Google Scholar 

  8. ——— & S. Y. Strauss. 2014. The geography and ecology of plant speciation: Range overlap and niche divergence in sister species. Proceedings of the Royal Society B. 281: 20132980.

  9. Andrew, R., K. L. Ostevik, D. P. Ebert & L. H. Rieseberg. 2012. Adaptation with gene flow across the landscape in a dune sunflower. Molecular Ecology 21: 2078–2091.

    PubMed  Article  Google Scholar 

  10. Andrew, R. L. & L. H. Rieseberg. 2013. Divergence is focused on few genomic regions early in speciation: incipient speciation of sunflower ecotypes. Evolution 67: 2468–2482.

    PubMed  Article  Google Scholar 

  11. Antonovics, J. 1968. Evolution in closely adjacent plant populations V. Evolution of self-fertility. Heredity 23: 219–238.

    Article  Google Scholar 

  12. ——— 1976. The nature of limits to natural selection. Annals of the Missouri Botanical Gardens 63: 224–247.

    Article  Google Scholar 

  13. ——— 2006. Evolution in closely adjacent plant populations X: long-term persistence of prereproductive isolation at a mine boundary. Heredity 97: 33–37.

    CAS  PubMed  Article  Google Scholar 

  14. Armbruster, W. S. 2014. Multiple origins of serpentine-soil endemism explained by preexisting tolerance of open habitats. Proceedings of the National Academy of Sciences of the United States of America 111: 14968–14969.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. Arnold, B. J., B. Lahner, J. M. DaCosta, C. M. Weisman, J. D. Hollister, D. E. Salt, K. Bomblies & L. Yant. 2016. Borrowed alleles and convergence in serpentine adaptation. Proceedings of the National Academy of Sciences of the United States of America 113: 8320–8325.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Baack, E., M. C. Melo, L. H. Rieseberg & D. Ortiz-Barrientos. 2015. The origins of reproductive isolation in plants. New Phytologist 207: 968–984.

    PubMed  Article  Google Scholar 

  17. Baker, H. G. 1965. Characteristics and modes of origins of weeds. Pp. 147–172. In: H. G. Baker & G. L. Stebbins (eds.), The genetics of colonizing species. Academic Press, New York.

    Google Scholar 

  18. Baldwin, B. G. 1999. New combinations and new genera in the North American tarweeds (Compositae-Madiinae). Novon 9: 462–471.

    Article  Google Scholar 

  19. ——— 2005. Origin of the serpentine-endemic herb Layia discoidea from the widespread L. glandulosa (Compositae). Evolution 59: 2473– 2479.

    PubMed  Google Scholar 

  20. ——— 2014. Origins of plant diversity in the California Floristic Province. Annual Review of Ecology Evolution and Systematics 45: 347–369.

    Article  Google Scholar 

  21. Barraclough, T. G. & A. P. Vogler. 2000. Detecting the geographical pattern of speciation from species-level phylogenies. American Naturalist 155: 419–434.

    CAS  PubMed  Google Scholar 

  22. Bastida, J. M., P. J. Rey & J. M. Alcántara. 2014. Plant performance and morpho-functional differentiation in response to edaphic variation in Iberian columbines: cues for range distribution? Journal of Plant Ecology-UK 7: 403–412.

    Article  Google Scholar 

  23. Baumbach, H. & F. H. Hellwig. 2007. Genetic differentiation of metallicolous and non-metallicolous Armeria maritima (Mill.) Willd. taxa (Plumbaginaceae) in Central Europe. Plant Systematics and Evolution 269: 245–258.

    Article  Google Scholar 

  24. Bell, G. 2012. Evolutionary rescue and the limits of adaptation. Philosophical Transactions of the Royal Society London B Biological Sciences 368: 20120080.

    Article  Google Scholar 

  25. Bennett, T. H., T. J. Flowers & L. Bromham. 2013. Repeated evolution of salt-tolerance in grasses. Biological Letters 9: 20130029.

    CAS  Article  Google Scholar 

  26. Bolukbasi, A., L. Kurt & S. Palacio. 2016. Unravelling the mechanisms for plant survival on gypsum soils: an analysis of the chemical composition of gypsum plants from Turkey. Plant Biology 18: 271–279.

    CAS  PubMed  Article  Google Scholar 

  27. Borchsenius, F., T. Lozada & J. T. Knudsen. 2016. Reproductive isolation of sympatric forms of the understorey palm Geonoma macrostachys in western Amazonia. Botanical Journal of the Linnean Society 182: 398–410.

    Article  Google Scholar 

  28. Boyd, R. S. 2007. The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant and Soil 293: 153–176.

    CAS  Article  Google Scholar 

  29. ——— & M. A. Wall. 2001. Responses of generalist predators fed high-Ni Melanotrichus boydi (Heteroptera: Miridae): Elemental defense against the third trophic level. American Midland Naturalist 146: 186–198.

  30. ——— 2014. Ecology and evolution of metal-hyperaccumulator plants. Pp. 227–241. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York.

    Google Scholar 

  31. Bradshaw, A. D. 1991. The Croonian Lecture, 1991. Genostasis and the limits to evolution. Philosophical Transactions of the Royal Society London B Biological Sciences 333: 289–305.

    CAS  Article  Google Scholar 

  32. ——— 2006. Unravelling phenotypic plasticity–why should we bother? New Phytologist 170: 644–648.

    PubMed  Article  Google Scholar 

  33. Bradshaw, H. D. 2005. Mutations in CAX1 produce phenotypes characteristic of plants tolerant to serpentine soils. New Phytologist 167: 81–88.

    CAS  PubMed  Article  Google Scholar 

  34. Brady, K. U., A. R. Kruckeberg, H. D. Bradshaw JR. 2005. Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology Evolution and Systematics 36: 243–266.

  35. Bratteler, M., M. Baltisberger & A. Widmer. 2006. QTL analysis of intraspecific differences between two Silene vulgaris ecotypes. Annals of Botany 98:411–419.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. ———, C. Lexer & A. Widmer. 2006. Genetic architecture of traits associated with serpentine adaptation of Silene vulgaris. Journal of Evolutionary Biology 19: 1149–1156.

  37. Bresowar, G. E. & M. E. McGlaughlin. 2015. Morphological and genetic discrepancies in populations of Oreocarya paradoxa and O. revealii: The impact of edaphic selection on recent diversification in the Colorado Plateau. American Journal of Botany 102: 1647–1658.

    CAS  PubMed  Article  Google Scholar 

  38. Brokaw, J. M., T. A. Johnson & C. H. Hofsommer. 2015. Edaphic Specialization in the Cryptic Species Mentzelia monoensis (Loasaceae). Madroño 62: 88–100.

    Article  Google Scholar 

  39. Burge, D. O. & P. S. Manos. 2011. Edaphic ecology and genetics of the gabbro-endemic shrub Ceanothus roderickii (Rhamnaceae). Madroño 58: 1–21.

    Article  Google Scholar 

  40. ———, R. Hopkins, Y.-H. E. Tsai & P. S. Manos. 2013. Limited hybridization across an edaphic disjunction between the gabbro-endemic shrub Ceanothus roderickii (Rhamnaceae) and the soil-generalist Ceanothus cuneatus. American Journal of Botany 100: 1883–1895.

  41. Burrell, A. M., A. K. Hawkins & A. E. Pepper. 2012. Genetic analyses of nickel tolerance in a North American serpentine endemic plant, Caulanthus amplexicaulis var. barbarae (Brassicaceae). American Journal of Botany 99: 1875–1883.

    CAS  PubMed  Article  Google Scholar 

  42. Cacho, N. I. & S. Y. Strauss. 2014. Occupation of bare habitats, an evolutionary precursor to soil specialization in plants. Proceedings of the National Academy of Sciences of the United States of America 111: 15132–15137.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. ———, A. M. Burrell, A. E. Pepper & S. Y. Strauss. 2014. Systematics and the evolution of serpentine tolerance in the California Jewelflowers (Streptanthus) and its allies. Molecular Phylogenetics and Evolution 72: 71–81.

  44. Chaney, R. L., R. D. Reeves, I. A. Baklanov, T. Centofanti, C. L. Broadhurst, A. J. M. Baker, A. van der Ent & R. J. Roseberg. 2014. Phytoremediation and phytomining: using plants to remediate contaminated or mineralized environments. Pp. 365–392. In: N. Rajakaruna, R. S. Boyd, T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, New York.

    Google Scholar 

  45. Cheeseman, J. M. 2015. The evolution of halophytes, glycophytes and crops, and its implications for food security under saline conditions. New Phytologist 206: 557–570.

    PubMed  Article  Google Scholar 

  46. Cheng, N. H., J. K. Pittman, J. B. Bronwyn, T. Shigaki & K. D. Hirchi. 2003. The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15: 347–364.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Cheplick, G. P. 2015. Approaches to Plant Evolutionary Ecology. Oxford University Press, New York.

    Google Scholar 

  48. Christie, P. & M. R. Macnair. 1984. Complementary lethal factors in two North-American populations of the yellow monkey flower. Journal of Heredity 75: 510–511.

    Article  Google Scholar 

  49. ——— & M. R. Macnair. 1987 The distribution of postmating reproductive isolating genes in populations of the yellow monkey flower, Mimulus guttatus. Evolution. 41: 571–578.

  50. Clausen, J., D. D. Keck & W. M. Hiesey. 1940. Experimental studies on the nature of species. I. Effect of varied environment on Western North American plants. Carnegie Institution of Washington, Washington, DC.

    Google Scholar 

  51. Crawford, D. J. 2010. Progenitor-derivative species pairs and plant speciation. Taxon 59: 1413–1423.

    Google Scholar 

  52. ———, R. Ornduff & M. C. Vasey. 1985. Allozyme variation within and between Lasthenia minor and its derivative species, L. maritima (Asteraceae) 72: 1177–1184.

  53. ———, J. J. Doyle, D. E. Soltis, P. S. Soltis & J. F. Wendel. 2014. Contemporary and future studies in plant speciation, morphological/floral evolution and polyploidy: honouring the scientific contributions of Leslie D. Gottlieb to plant evolutionary biology. Philosophical Transactions of the Royal Society London B Biological Sciences 369: 20130341.

  54. Damschen, E. I., S. P. Harrison & J. B. Grace. 2010. Climate change effects on an endemic-rich edaphic flora: resurveying Robert H. Whittaker’s Siskiyou sites (Oregon, USA). Ecology 91: 3609–3619.

    PubMed  Article  Google Scholar 

  55. ———, S. P. Harrison, D. D. Ackerly, B. Fernandez-Going & B. L. Anacker. 2012. Endemic plants on serpentine soils: Early victims or hardy survivors of climate change? Journal of Ecology 100: 1122–1130.

  56. De Storme, N. & A. Mason. 2014. Plant speciation through chromosome instability and ploidy change: Cellular mechanisms, molecular factors and evolutionary relevance. Current Plant Biology 1: 10–33.

    Article  Google Scholar 

  57. Dechamps, C., N. Noret, R. Mozek, J. Escarré, C. Lefèbvre, W. Gruber, P. Meerts. 2008. Cost of adaptation to a metalliferous environment for Thlaspi caerulescens: a field reciprocal transplantation approach. New Phytologist 177: 167–177.

    CAS  PubMed  Google Scholar 

  58. Dillenberger, M. S. & J. W. Kadereit. 2013. The phylogeny of the European high mountain genus Adenostyles (Asteraceae-Senecioneae) reveals that edaphic shifts coincide with dispersal events. American Journal of Botany 100: 1171–1183.

    PubMed  Article  Google Scholar 

  59. Donovan, L. A., D. R. Rosenthal, M. Sanchez-Velenosi, L. H. Rieseberg & F. Ludwig. 2010. Are hybrid species more fit than ancestral parent species in the current hybrid species habitats? Journal of Evolutionary Biology 23: 805–816.

    CAS  PubMed  Article  Google Scholar 

  60. Douglas, N. A., W. A. Wall, Q.-Y. (J) Xiang, W. A. Hoffmann, T. R. Wentworth, J. B. Gray & M. G. Hohmann. 2011. Recent vicariance and the origin of the rare, edaphically specialized Sandhills lily, Lilium pyrophilum (Liliaceae): evidence from phylogenetic and coalescent analyses. Molecular Ecology 20: 2901–2915.

  61. Dubois, S., P.-O. Cheptou, C. Petit, P. Meerts, M. Poncelet, X. Vekemans, C. Lefèbvre & J. Escarré. 2003. Genetic structure and mating systems of metallicolous and nonmetallicolous populations of Thlaspi caerulescens. New Phytologist 157: 633–641.

    Article  Google Scholar 

  62. Dunning, L. T., H. Hipperson, W. J. Baker, R. K. Butlin, C. Devaux, I. Hutton, J. Igea, A. S. T. Papadopulos, X. Quan, C. M. Smadja, C. G. N. Turnbull & V. Savolaine. 2016. Ecological speciation in sympatric palms: 1. Gene expression, selection and pleiotropy. Journal of Evolutionary Biology 29: 1472–1487.

  63. Edelist, C., X. Raffoux, M. Falque, C. Dillmann, D. Sicard, L. H. Rieseberg & S. Karrenberg. 2009. Differential expression of candidate salt-tolerance genes in the halophyte Helianthus paradoxus and its glycophyte progenitors H. annuus and H. petiolaris (Asteraceae). American Journal of Botany 96: 1830–1838.

    CAS  PubMed  Article  Google Scholar 

  64. El Mehdawi, A. F., C. F. Quinn & E. A. Pilon-Smits. 2011. Effects of selenium hyperaccumulation on plant-plant interactions: evidence for elemental allelopathy? New Phytologist 191: 120–131.

    PubMed  Article  CAS  Google Scholar 

  65. ——— & E. A. H. Pilon-Smits. 2012. Ecological aspects of plant selenium hyperaccumulation. Plant Biology 14: 1–10.

  66. Ellis, A. G. & A. E. Weis. 2005. Coexistence and differentiation of ‘flowering stones’: the role of local adaptation to soil microenvironment. Journal of Ecology 94: 322–335.

    Article  CAS  Google Scholar 

  67. ———, A. E. Weis & B. S. Gaut. 2006. Evolutionary radiation of ‘stone plants’ in the genus Argyroderma (Aizoaceae): unraveling the effects of landscape, habitat and flowering time. Evolution 60: 39–55.

  68. Ellstrand, N. C. 2014. Is gene flow the most important evolutionary force in plants? American Journal of Botany 101: 737–753.

    PubMed  Article  Google Scholar 

  69. Ernst, W. H. O. 2006. Evolution of metal tolerance in higher plants. Forest Snow and Landscape Research 80: 251–274.

    Google Scholar 

  70. Escudero, A., S. Palacio, F. T. Maestre & A. L. Luzuriaga. 2015. Plant life on gypsum: a review of its multiple facets. Biological Reviews 90: 1–18.

    PubMed  Article  Google Scholar 

  71. Faria, R., S. Renaut, J. Galindo, C. Pinho, J. Melo-Ferreira, M. Melo, F. Jones, W. Salzburger, D. Schluter & R. Butlin. 2014. Advances in Ecological Speciation: an integrative approach. Molecular Ecology 23: 513–521.

    PubMed  Article  Google Scholar 

  72. Feliner, G. N., A. Izuzquiza & A.R. Lansac. 1996. Natural and experimental hybridization in Armeria (Plumbaginaceae): A. villosa subsp. carratracensis. Plant Systematics and Evolution 201: 163–177.

    Article  Google Scholar 

  73. Fernandez-Going, B. M., B. L. Anacker & S. P. Harrison. 2012. Temporal variability in California grasslands: Soil type and species functional traits mediate response to precipitation. Ecology 93: 2104–2114.

    CAS  PubMed  Article  Google Scholar 

  74. ——— & S. P. Harrison. 2013. Effects of experimental water addition depend on grassland community characteristics. Plant Ecology 214: 777–786.

  75. ——— 2014. Climate change and the future of edaphic floras. Pp. 297–312. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York.

  76. Ferris, K. G., J. P. Sexton & J. H. Willis. 2014. Speciation on a local geographic scale: the evolution of a rare rock outcrop specialist in Mimulus. Philos. Philosophical Transactions of the Royal Society London B Biological Sciences 369: 20140001.

    Article  Google Scholar 

  77. ———, L. L. Barnett, B. K. Blackman & J. H. Willis. 2016. The genetic architecture of local adaptation and reproductive isolation in sympatry within the Mimulus guttatus species complex. Molecular Ecology 26: 208–224.

  78. Fine, P. V. A., I. Mesones & P. D. Coley. 2004. Herbivores promote habitat specialization by trees in Amazonian forests. Science 305: 663–665.

    CAS  PubMed  Article  Google Scholar 

  79. ———, Z. J. Miller, I. Mesones, S. Irazuzta, H. M. Appel, M. H. H. Stevens, I. Sääksjärvi, J. C. Schultz & P. D. Coley. 2006. The growth-defense trade-off and habitat specialization by plants in Amazonian forests. Ecology 87: S150–S162.

  80. ———, F. Zapata, D. C. Daly, I. Mesones, T. M. Misiewicz, H. F. Cooper & C. E. A. Barbosa. 2013. The importance of environmental heterogeneity and spatial distance in generating phylogeographic structure in edaphic specialist and generalist tree species of Protium (Burseraceae) across the Amazon Basin. Journal of Biogeography 40: 646–661.

  81. Fones, H., C. A. R. Davis, A. Rico, F. Fang, J. A. C. Smith & G.M. Preston. 2010. Metal hyperaccumulation armors plants against disease. PLOS Pathogens 6: e1001093.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  82. Forde, M. B. & D. G. Faris. 1962. Effect of introgression on the serpentine endemism of Quercus durata. Evolution 16: 338–347.

    Article  Google Scholar 

  83. Freeland, J. R., P. Biss, K. F. Conrad & J. Silvertown. 2010. Selection pressures have caused genome-wide population differentiation of Anthoxanthum odoratum despite the potential for high gene flow. Journal of Evolutionary Biology 23: 776–782.

    CAS  PubMed  Article  Google Scholar 

  84. Friedman, J. & J. H. Willis. 2013. Major QTLs for critical photoperiod and vernalization underlie extensive variation in flowering in the Mimulus guttatus species complex. New Phytologist 199: 571–583.

    CAS  PubMed  Article  Google Scholar 

  85. Gardner, M. & M. R. Macnair. 2000. Factors affecting the co-existence of the serpentine endemic Mimulus nudatus Curran and its presumed progenitor, Mimulus guttatus Fischer ex DC. Biological Journal of the Linnean Society 69: 443–459.

    Article  Google Scholar 

  86. Gil-López, M. J., J. G. Segarra-Moragues & F. Ojeda. 2014. Population genetic structure of a sandstone specialist and a generalist heath species at two levels of sandstone patchiness across the Strait of Gibraltar. PLOS One 9: e98602.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  87. Gill, S. S., N. A. Anjum, I. Ahmad, P. Thangavel, G. Sridevi, M. Pacheco, A. C. Duarte, S. Umar, N. A. Khan & M. E. Pereira. 2012. Metal Hyperaccumulation and Tolerance in Alyssum, Arabidopsis and Thlaspi: An Overview. Pp. 99–137. In: N.A. Anjum, I. Ahmad, M.E. Pereira, A.C. Duarte, S. Umar, N.A. Khan (eds.), The plant family Brassicaceae: contribution towards phytoremediation. Springer Science & Business Media, Dordrecht.

    Google Scholar 

  88. Glassmand, S. I. & B. B. Casper. 2012. Biotic contexts alter metal sequestration and AMF effects on plant growth in soils polluted with heavy metals. Ecology 93: 1550–1559.

    Article  Google Scholar 

  89. Going, B. M., J. Hillerislambers & J. M. Levine. 2009. Abiotic and biotic resistance to grass invasion in serpentine annual plant communities. Oecologia 159: 839–847.

    PubMed  Article  Google Scholar 

  90. Gonzalez-Chavez, C., P. J. Harris, J. Dodd & A. A. Meharg. 2002. Arbuscular mycorrhizal fungi confer enhanced arsenate resistance on Holcus lanatus. New Phytologist 155: 163–171.

    CAS  Article  Google Scholar 

  91. Gottlieb, L. D. 1968. Hybridization between Arctostaphylos viscida and A. canescens in Oregon. Brittonia 20: 83–93.

    Article  Google Scholar 

  92. ——— 2004. Rethinking classic examples of recent speciation in plants. New Phytologist 161: 71–82.

    Article  Google Scholar 

  93. Gram, W. L., E. T. Borer, K. L. Cottingham, E. W. Seabloom, V. L. Boucher, L. Goldwasser, F. Micheli, B. E. Kendall & R. S. Burton. 2004. Distribution of plants in a California serpentine grassland: Are rocky hummocks spatial refuges for native species? Plant Ecology 172: 159–171.

    Article  Google Scholar 

  94. Gramlich, S., P. Sagmeister, S. Dullinger, F. Hadacek & E. Hörandl. 2016. Evolution in situ: hybrid origin and establishment of willows (Salix L.) on alpine glacier forefields, Heredity 116: 531–541.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  95. Grossenbacher, D. L., S. D. Veloz & J. P. Sexton. 2014. Niche and range size patterns suggest that speciation begins in small, ecologically diverged populations in North American monkeyflowers (Mimulus spp.). Evolution 68: 1270–1280.

    PubMed  Article  Google Scholar 

  96. Hall, M. C., D. B. Lowry & J. H. Willis. 2010. Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Molecular Ecology 19: 2739–2753.

    CAS  PubMed  Article  Google Scholar 

  97. Harper, F. A., Smith, S. E. & M. R. Macnair. 1997a. Where is the cost in copper tolerance in Mimulus guttatus? Testing the trade-off hypothesis. Functional Ecology 11: 764–774.

    Article  Google Scholar 

  98. ———, Smith, S. E. & M. R. Macnair. 1997b. Can an increased copper requirement in copper-tolerant Mimulus guttatus explain the cost of tolerance? I. Vegetative phase. New Phytologist 136: 455–467

  99. ———, Smith, S. E. & M. R. Macnair. 1998. Can an increased copper requirement in copper-tolerant Mimulus guttatus explain the cost of tolerance? II. Reproductive phase. New Phytologist 140: 637–654.

  100. Harrison, S. P. 1999. Native and alien species diversity at the local and regional scales in a Native and alien species diversity at the local and regional scales in a grazed California grassland. Oecologia 121: 99–106.

    PubMed  Article  Google Scholar 

  101. ——— & N. Rajakaruna (eds.). 2011. Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

  102. ———, E. Damschen, B. Fernandez-Going, A. Eskelinen & S. Copeland. 2015. Plant communities on infertile soils are less sensitive to climate change. Annals of Botany 116: 1017–1022.

  103. Hayward, A. R., K. E. Coates, A. L. Galer, T. C. Hutchinson & R. J. Emery. 2013. Chelator profiling in Deschampsia cespitosa (L.) Beauv. reveals a Ni reaction, which is distinct from the ABA and cytokinin associated response to Cd. Plant Physiology and Biochemistry 64: 84–91.

    CAS  PubMed  Article  Google Scholar 

  104. Hego, E., S. Vilain, A. Barré, S. Claverol, J.-W. Dupuy, C. Lalanne, M. Bonneu, C. Plomion, M. Mench. 2016. Copper stress-induced changes in leaf soluble proteome of Cu-sensitive and tolerant Agrostis capillaris L. populations. Proteomics 16: 1386–1397.

    CAS  PubMed  Article  Google Scholar 

  105. Henry, L. P., R. H. B. Watson & B. K. Blackman. 2014. Transitions in photoperiodic flowering are common and involve few loci in wild sunflowers (Helianthus; Asteraceae). American Journal of Botany 101: 1748–1758.

    PubMed  Article  Google Scholar 

  106. Hereford, J. 2009. A quantitative survey of local adaptation and fitness trade-offs. American Naturalist 173: 579–588.

    PubMed  Article  Google Scholar 

  107. Hipperson, H., L. T. Dunning, W. J. Baker, R. K. Butlin, I. Hutton, A. S. T. Papadopulos, C. M. Smadja, T. C. Wilson, C. Devaux & V. Savolainen, V. 2016. Ecological speciation in sympatric palms: 2. Pre- and post-zygotic isolation, Journal of Evolutionary Biology 29: 2143–2156.

  108. Hoban, S., J. L. Kelley, K. E. Lotterhos, M. F. Antolin, G. Bradburd, D. B. Lowry, M. L. Poss, L. K. Reed, A. Storfer & M. C. Whitlock. 2016. Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. American Naturalist 188: 379–397.

    PubMed  PubMed Central  Article  Google Scholar 

  109. Hopkins, R. 2013. Reinforcement in plants. New Phytologist 197: 1095–1103.

    PubMed  Article  Google Scholar 

  110. Hörger, A. C., H. N. Fones & G. M. Preston. 2013. The current status of the elemental defense hypothesis in relation to pathogens. Frontiers in Plant Science 4: 1–11.

    Article  Google Scholar 

  111. Huang, X. & D. E. Salt. 2016. Plant ionomics: from elemental profiling to environmental adaptation. Molecular Plant 9: 787–797.

    CAS  PubMed  Article  Google Scholar 

  112. Hunter, B. & K. Bomblies. 2010. Progress and promise in using Arabidopsis to study adaptation, divergence, and speciation. Arabidopsis Book 8: e0138.

  113. Jurjavcic, N. L., S. P. Harrison & A. T. Wolf. 2002. Abiotic stress, competition, and the distribution of the native annual grass Vulpia microstachys in a mosaic environment. Oecologia 130: 555–562.

    CAS  PubMed  Article  Google Scholar 

  114. Kane, N. C. 2009. Comparative genomic and population genetic analyses indicate highly porous genomes and high levels of gene flow between divergent Helianthus species. Evolution 63: 2061–2075.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. Kaplan, Z. 1998. Relict serpentine populations of Knautia arvensis s. l. (Dipsacaceae) in the Czech Republic and an adjacent area of Germany. Preslia 70: 21–31.

    Google Scholar 

  116. Kay, K. M., K. L. Ward, L. R. Watt & D.W. Schemske. 2011. Plant Speciation. Pp. 71–96. In: S. P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  117. Kazakou, E., P.G. Dimitrakopoulos, A.J. Baker, R.D. Reeves & A.Y. Troumbis. 2008. Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biological Reviews 83: 495–508.

    CAS  PubMed  Google Scholar 

  118. Klein, J. T. & J. W. Kadereit. 2015. Phylogeny, biogeography and evolution of edaphic association in the European oreophytes Sempervivum and Jovibarba (Crassulaceae). International Journal of Plant Sciences 176: 44–71.

    Article  Google Scholar 

  119. Kolář, F., T. Fér, M. Štech, P. Trávníček, E. Dušková, P. Schönswetter & J. Suda. 2012. Bringing together evolution on serpentine and polyploidy: spatiotemporal history of the diploid-tetraploid complex of Knautia arvensis (Dipsacaceae). PLoS ONE 7: e39988.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  120. ———, M. Dortová, J. Lepš, M. Pouzar, A. Krejčová & M. Štech. 2014. Serpentine ecotypic differentiation in a polyploid plant complex: shared tolerance to Mg and Ni stress among di- and tetraploid serpentine populations of Knautia arvensis (Dipsacaceae). Plant and Soil 374: 435–447.

  121. Krahulcová, A. & J. Štěpánková. 1998. Serpentine and polyploid differentiation within Galium pumilum agg. (Rubiaceae) in Eastern C. Europe. Folia Geobotanica 33: 87–102.

    Article  Google Scholar 

  122. Kruckeberg, A. R. 1951. Intraspecific variability in the response of certain native plant species to serpentine soil. American Journal of Botany 38: 408–419.

    CAS  Article  Google Scholar 

  123. ——— 1954. The ecology of serpentine soils. III. Plant species in relation to serpentine soils. Ecology 35: 267–274.

    Google Scholar 

  124. ——— 1986. An essay: The stimulus of unusual geologies for plant speciation. Systematic Botany 11: 455–463.

    Article  Google Scholar 

  125. ——— 1992. Plant life of western North American ultramafics. Pp. 31–73. In: B. A. Roberts & J. Proctor (eds.), The ecology of areas with serpentinized rocks. Springer Netherlands. Dordrecht.

    Google Scholar 

  126. Lai, Z., T. Nakazato, M. Salmaso, J. M. Burke, S. Tang, S. J. Knapp & L. H. Rieseberg. 2005. Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics. 171: 291–303.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  127. Lau, J. A., A. C. McCall, K. F. Davies, J. K. McKay & J. W. Wright. 2008. Herbivores and edaphic factors constrain the realized niche of a native plant. Ecology 89: 754–762.

    PubMed  Article  Google Scholar 

  128. Leimu, R. & M. Fischer. 2008. A meta-analysis of local adaptation in plants. PLoS ONE 3(12): e4010.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  129. Leinonen, P. H., D. L. Remington, J. Leppälä & O. Savolainen. 2013. Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Molecular Ecology 22: 709–723.

    CAS  PubMed  Article  Google Scholar 

  130. Levin, D. A. 1993. Local speciation in plants: the rule not the exception. Systematic Botany 18: 197–208.

    Article  Google Scholar 

  131. ——— 2001. The recurrent origin of plant races and species. Systematic Botany 26: 197–204.

    Google Scholar 

  132. ——— 2009. Flowering-time plasticity facilitates niche shifts in adjacent populations. New

  133. Lexer, C., M. E. Welch, J. L. Durphy & L. H. Rieseberg. 2003. Natural selection for salt tolerance quantitative trait loci (QTLs): Implications for the origin of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology 12: 1225–1235.

    CAS  PubMed  Article  Google Scholar 

  134. ———, Z. Lai & L. H. Rieseberg. 2004. Candidate gene polymorphisms associated with salt tolerance in wild sunflower hybrids: implications for the origin of Helianthus paradoxus, a diploid sunflower hybrid species. New Phytologist 161: 225–233.

  135. Loarie, S. R., B. E. Carter, K. Hayhoe, S. McMahon, R. Moe, C. A. Knight & D. D. Ackerly. 2008. Climate Change and the Future of California's Endemic Flora. PLOS One 3: e2502.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  136. Lowry, D. B., R. C. Rockwood & J. H. Willis. 2008. Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62: 2196–2214.

    PubMed  Article  Google Scholar 

  137. ———, M. C. Hall, D. E. Salt, J. H. Willis. 2009. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytologist 183: 776–788.

  138. ——— & J. H. Willis. 2010. A widespread chromosomal inversion polymorphism contributes to a major life history transition, local adaptation, and reproductive isolation. PLOS Biol. 8: e1000500.

  139. ——— 2012. Ecotypes and the controversy over stages in the formation of new species. Biological Journal of the Linnean Society 106: 241–257.

    Article  Google Scholar 

  140. ———, C. C. Sheng, Z. Zhu, T. E. Juenger & B. C. Lahner. 2012. Mapping of ionomic traits in Mimulus guttatus reveals Mo and Cd QTLs that colocalize with MOT1 homologues. PLOS One 7: e30730.

  141. Macnair, M R. 1983. The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity 50: 283–293.

    CAS  Article  Google Scholar 

  142. ——— & P. Christie. 1983. Reproductive isolation as a pleiotropic effect of copper tolerance in Mimulus guttatus? Heredity 50: 295–302.

  143. ———, V. E. Macnair & B. E. Martin. 1989. Adaptive speciation in Mimulus: an ecological comparison of M. cupriphilus with its presumed progenitor, M. guttatus. New Phytologist 112: 269–279.

  144. ———, S. E. Smith & Q. J. Cumbes. 1993. Heritability and distribution of variation in degree of copper tolerance in Mimulus guttatus at Copperopolis, California. Heredity: 71: 445–455.

  145. ——— & M. Gardner. 1998. The evolution of edaphic endemics. Pp. 157–171. In: D. J. Howard & S. H. Berlocher (eds.), Endless forms: species and speciation. Oxford University Press, New York.

  146. Maestri, E., M. Marmiroli, G. Visioli & N. Marmiroli. 2010. Metal tolerance and hyperaccumulation: Costs and trade-offs between traits and environment. Environmental and Experimental Botany 68: 1–13.

    CAS  Article  Google Scholar 

  147. Mandáková, T., V.Singh, U. Krämer & M. A. Lysak. 2015. Genome structure of the heavy metal hyperaccumulator Noccaea caerulescens and its stability on metalliferous and nonmetalliferous soils. Plant Physiology 169: 674–689.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  148. Marsden-Jones, E. M. & W. B. Turrill. 1938. Transplant experiments of the British Ecological Society at Potterne, Wiltshire. Summary of results: 1928–1937. Journal of Ecology 26: 380–389.

    Article  Google Scholar 

  149. Martin, N. H., A. C. Bouck & M. L. Arnold. 2006. Detecting adaptive trait introgression between Iris fulva and I. brevicaulis in highly selective field conditions. Genetics 172: 2481–2489.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  150. Mason, H. L. 1946a. The edaphic factor in narrow endemism. I. The nature of environmental influences. Madroño 8: 209–226.

    Google Scholar 

  151. ——— 1946b. The edaphic factor in narrow endemism. II. The geographic occurrence of plants of highly restricted patterns of distribution, Madroño 8: 241–257.

    Google Scholar 

  152. Mayer, M. S. & P. S. Soltis. 1994. The evolution of serpentine endemics: A chloroplast DNA phylogeny of the Streptanthus glandulosus complex (Cruciferae). Systematic Botany 19: 557–574.

    Article  Google Scholar 

  153. ——— & P. S. Soltis. 1999. Intraspecific phylogeny analysis using ITS sequences: Insights from studies of the Streptanthus glandulosus complex (Cruciferae). Systematic Botany 24: 47–61.

  154. Meindl, G. A. & T. -L. Ashman. 2013. The effects of aluminum and nickel in nectar on the foraging behavior of bumblebees. Environmental Pollution 177: 78–81.

  155. ——— & T. -L. Ashman. 2014. Nickel accumulation by Streptanthus polygaloides (Brassicaceae) reduces floral visitation rate. Journal of Chemical Ecology 40: 128–135.

  156. ———, D. J. Bain & T.-L. Ashman. 2014. Nickel accumulation in leaves, floral organs and rewards varies by serpentine soil affinity. AoB PLANTS 6: plu036.

  157. ———& T. -L. Ashman. 2015. Effects of floral metal accumulation on floral visitor communities: Introducing the elemental filter hypothesis. American Journal of Botany 102: 379–389.

  158. Melo, M. C., A. Grealy, B. Brittain, G. M. Walter & D. Ortiz-Barrientos. 2014. Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel. New Phytologist 203: 323–334.

    PubMed  Article  Google Scholar 

  159. Mengoni, A., C. Gonnelli, F. Galardi, R. Gabbrielli & M. Bazzicalupo. 2001. Genetic diversity of heavy metal tolerant populations in Silene paradoxa L. (Caryophyllaceae): a chloroplast microsatellite analysis. Molecular Ecology 10: 1909–1916.

    CAS  PubMed  Article  Google Scholar 

  160. ———, A. J. M. Baker, M. Bazzicalupo, R. D. Reeves, N. Adigüzel, E. Chianni, F. Galardi, R. Gabbrielli & C. Gonnelli. 2003a. Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by its nrDNA analysis. New Phytologist 159: 691–699.

  161. ———, C. Gonnelli, E. Brocchini, F. Galardi, S. Pucci, R. Gabbrielli & M. Bazzicalupo. 2003b. Chloroplast genetic diversity and biogeography in the serpentine endemic Ni-hyperaccumulator Alyssum bertolonii. New Phytologist 157: 349–356.

  162. Miglia, K. J. 2007. Genotype, soil type, and locale effects on reciprocal transplant vigor, endophyte growth, and microbial functional diversity of a narrow sagebrush hybrid zone in Salt Creek Canyon, Utah. American Journal of Botany 94: 425–436.

    PubMed  Article  Google Scholar 

  163. Milla, R., A. Escudero & J. M. Iriondo. 2011. Congruence between geographic range distribution and local competitive ability of two Lupinus species. American Journal of Botany 98: 1456–1464.

    PubMed  Article  Google Scholar 

  164. Moore, A. J. & J. W. Kadereit. 2013. The evolution of substrate differentiation in Minuartia series Laricifoliae (Caryophyllaceae) in the European Alps: In situ origin or repeated colonization? American Journal of Botany 100: 2412–2425.

    PubMed  Article  Google Scholar 

  165. ———, D. Merges & J. W. Kadereit. 2013. The origin of the serpentine endemic Minuartia laricifolia subsp. ophiolitica by vicariance and competitive exclusion, Molecular Ecology 22: 2218–2231.

  166. Moore, K. A. & S. C. Elmendorf. 2011. Plant competition and facilitation in systems with strong environmental gradients. Pp. 223–236. In: S. P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  167. Moore, M. J., J. F. Mota, N. A. Douglas, H. F. Olvera & H. Ochoterena. 2014. The ecology, assembly, and evolution of gypsophile floras. Pp. 97–128. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York.

    Google Scholar 

  168. Moray, C., E. W. Goolsby & L. Bromham. 2016. The phylogenetic association between salt tolerance and heavy metal hyperaccumulation in angiosperms. Evolutionary Biology 43: 119–130.

    Article  Google Scholar 

  169. Mousset, M., P. David, C. Petit, J. Pouzadoux, C. Hatt. E. Flaven, O. Ronce & A. Mignot. 2016. Lower selfing rates in metallicolous populations than in non-metallicolous populations of the pseudometallophyte Noccaea caerulescens (Brassicaceae) in Southern France. Annals of Botany 117: 507–519.

    PubMed  PubMed Central  Article  Google Scholar 

  170. Moyle, L.C., M. Levine, M. L. Stanton & J. W. Wright. 2012. Hybrid sterility over tens of meters between ecotypes adapted to serpentine and non-serpentine soils. Evolutionary Biology 39: 207–218.

    Article  Google Scholar 

  171. Nichols, M.K. & McNeilly, T. 1982. The possible polyphyletic origin of copper tolerance in Agrostis tenuis (Gramineae). Plant Systematics and Evolution 140: 109–117.

    Article  Google Scholar 

  172. Nosil, P. & D. Schluter. 2011. The genes underlying the process of speciation. Trends in Ecology and Evolution 26: 160–167.

    PubMed  Article  Google Scholar 

  173. ——— 2012. Ecological Speciation. Oxford University Press, Oxford.

    Google Scholar 

  174. Nyberg Berglund, A. B., S. Dahlgren & A. Westerbergh. 2004. Evidence for parallel evolution and site-specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytologist 161: 199–209.

    Article  CAS  Google Scholar 

  175. O’Dell, R. E. & N. Rajakaruna. 2011. Intraspecific variation, plant adaptation, and evolution. Pp. 71–96. In: S.P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  176. ——— 2014. Conservation and restoration of chemically extreme edaphic endemic flora in the western US. Pp. 3313–3364. In: N. Rajakaruna, R. S. Boyd, T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, New York.

    Google Scholar 

  177. Olko, A., A. Abratowska, J. Żyłkowska, M. Wierzbicka & A. Tukiendorf. 2008. Armeria maritima from a calamine heap—Initial studies on physiologic–metabolic adaptations to metal-enriched soil. Ecotoxicology and Environmental Safety 69: 209–218.

    CAS  PubMed  Article  Google Scholar 

  178. Ornduff, R. 1965. Ornithocoprophilous endemism in Pacific Basin angiosperms. Ecology 46: 864–867.

    Article  Google Scholar 

  179. Ortiz-Barrientos, D., A. Grealy & P. Nosil. 2009. The genetics and ecology of reinforcement: implications for the evolution of prezygotic isolation in sympatry and beyond. Annals of the New York Academy of Sciences 1168: 156–182.

    CAS  PubMed  Article  Google Scholar 

  180. Ostevik, K. L., B. T. Moyers, G. L. Owens & L. H. Rieseberg. 2012. Parallel Ecological Speciation in Plants? International Journal of Ecology 939862.

    Google Scholar 

  181. ———, R. L. Andrew, S. P. Otto & L. H. Rieseberg. 2016. Multiple reproductive barriers separate recently diverged sunflower ecotypes. Evolution 70: 2322–2335.

  182. Palacio, S., A. Escudero, G. Montserrat-Martí, M. Maestro, R. Milla & M. J. Albert. 2007. Plants living on gypsum: beyond the specialist model. Annals of Botany 99: 333–343.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  183. ———, D. Johnson, A. Escudero & G. Montserrat-Martí. 2012. Root colonisation by AM fungi differs between gypsum specialist and non-specialist plants: Links to the gypsophile behavior. Journal of Arid Environments 76: 128–132.

  184. ———, J. Azorín, G. Montserrat-Martí & J. P. Ferrio. 2014. The crystallization water of gypsum rocks is a relevant water source for plants. Nature Communications 5: 4660; doi:https://doi.org/10.1038/ncomms5660.

  185. Palacio-López, K., B. Beckage, S. Scheiner & J. Molofsky. 2015. The ubiquity of phenotypic plasticity in plants: a synthesis. Ecology and Evolution 5: 3389–3400.

    PubMed  PubMed Central  Article  Google Scholar 

  186. Palm, E., K. Brady & E. Van Volkenburgh. 2012. Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Functional Plant Biology 39: 679–688.

    CAS  Article  Google Scholar 

  187. ——— & E. Van Volkenburgh. 2014. Physiological adaptations of plants to serpentine soil. Pp. 129–148. In: N. Rajakaruna, R. S. Boyd, T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York.

  188. Papadopulos, A. S. T., W. J. Baker, D. Crayn, R. K. Butlin, R. G. Kynast, I. Hutton & V. Savolainen. 2011. Speciation with gene flow on Lord Howe Island. Proceedings of the National Academy of Sciences of the United States of America 108: 13188–13193.

  189. Parejo-Farnés, C., R. G. Albaladejo, J. Arroyo & A. Aparicio. 2013. A phylogenetic hypothesis for Helianthemum (Cistaceae) in the Iberian Peninsula. Botanica Complutensis 37: 83−92.

    Google Scholar 

  190. Paris, C. A. & M. D. Windham. 1988. A biosystematic investigation of the Adiantum pedatum complex in eastern North America. Systematic Botany 13: 240–255.

    Article  Google Scholar 

  191. ——— 1991. Adiantum viridimontanum, a new maidenhair fern in eastern North America. Rhodora 93: 105–122.

    Google Scholar 

  192. Partridge, L. & R. Sibly. 1991. Constraints in the evolution of life histories. Philosophical Transactions of the Royal Society London, B 332: 3–13.

    Article  Google Scholar 

  193. Parys, E., W. Wasilewska, M. Siedlecka, M. Zienkiewicz, A. Drożak & E. Romanowska. 2014. Metabolic responses to lead of metallicolous and nonmetallicolous populations of Armeria maritima. Archives of Environmental Contamination and Toxicology 67: 565–577.

    CAS  PubMed  Article  Google Scholar 

  194. Paule, J., F. Kolář & C. Dobeš. 2015. Arctic-alpine and serpentine differentiation in polyploid Potentilla crantzii. Preslia 87: 195–215.

    Google Scholar 

  195. Paun, O., B. Turner, E. Trucchi, J. Munzinger, M. W. Chase & R. Samuel. 2016. Processes Driving the Adaptive Radiation of a Tropical Tree (Diospyros, Ebenaceae) in New Caledonia, a Biodiversity Hotspot. Systematic Biology 65: 212–227.

    PubMed  Article  Google Scholar 

  196. Pauwels, M., P. Saumitou-Laprade, A.C. Holl, D. Petit & I. Bonnin. 2005. Multiple origin of metallicolous populations of the pseudometallophyte Arabidopsis halleri (Brassicaceae) in central Europe: the cpDNA testimony. Molecular Ecology 14: 4403–4414.

    CAS  PubMed  Article  Google Scholar 

  197. Pepper, A. E. & L. E. Norwood. 2001. Evolution of Caulanthus amplexicaulis var. barbarae (Brassicaceae), a rare serpentine endemic plant: a molecular phylogenetic perspective. American Journal of Botany 88: 1479–1489.

    CAS  PubMed  Article  Google Scholar 

  198. Peterson, M. L., K. J. Rice & J. P Sexton. 2013. Niche partitioning between close relatives suggests trade-offs between adaptation to local environments and competition. Ecology and Evolution 3: 512–522.

    PubMed  PubMed Central  Article  Google Scholar 

  199. Pettengill, J. B. & D. A. Moeller. 2012. Phylogeography of speciation: allopatric divergence and secondary contact between outcrossing and selfing Clarkia. Molecular Ecology 21: 4578–4592.

    PubMed  Article  Google Scholar 

  200. Pfennig, K. S. & D. W. Pfennig. 2009. Character displacement: ecological and reproductive responses to a common evolutionary problem. The Quarterly Review of Biology 84: 253–276.

    PubMed  PubMed Central  Article  Google Scholar 

  201. Pope, N., M. Fong, R. S. Boyd & N. Rajakaruna. 2014. The role of elevation and soil chemistry in the distribution and ion accumulation of floral morphs of Streptanthus polygaloides Gray (Brassicaceae), a Californian nickel hyperaccumulator. Plant Ecology and Diversity 7: 1–39.

    Article  Google Scholar 

  202. Porter, S. S., P. L. Chang, C. A. Conow, J. P. Dunham, M. L. Friesen. 2017. Association mapping reveals novel serpentine adaptation gene clusters in a population of symbiotic Mesorhizobium. The ISME Journal 11: 248–262

    CAS  PubMed  Article  Google Scholar 

  203. Powell, K. I. & T. M. Knight. 2009. Effects of nutrient addition and competition on biomass of five Cirsium species (Asteraceae), including a serpentine endemic. International Journal of Plant Sciences 170: 918–925.

    Article  Google Scholar 

  204. Quinn, C. F., J. L. Freeman, R. J. B. Reynolds, J. J. Cappa, S. C. Fakra, M. A. Marcus, S. D. Lindblom, E. K. Quinn, L. E. Bennett & E. A. H Pilon-Smits. 2010. Selenium hyperaccumulation offers protection from cell disruptor herbivores. BMC Ecology 10: 1–11.

    Article  CAS  Google Scholar 

  205. ———, C. N. Prins, J. L. Freeman, A. M. Gross, L. J. Hantzis, R. J. B. Reynolds, S.Yang, P. A. Covey, G. S. Bañuelos, I. J. Pickering, S. C. Fakra, M. A. Marcus, H. S. Arathi, & E. A. H. Pilon-Smits. 2011a. Selenium accumulation in flowers and its effects on pollination. New Phytologist 192: 727–737.

  206. ———, K. A. Wyant, A. L. Wangeline, J. Shulman, M. L. Galeas, J. R. Valdez, J. R. Self, M. W. Paschke & E. A. H. Pilon-Smits. 2011b. Enhanced decomposition of selenium hyperaccumulator litter in a seleniferous habitat—evidence for specialist decomposers? Plant and Soil 341: 51–61.

  207. Qureshi, J. A., D. A. Thurman, K. Hardwick, H. A. Collin. 1985. Uptake and accumulation of zinc, lead and copper in zinc and lead tolerant Anthoxanthum odoratum L. New Phytologist 100: 429–434.

    CAS  Article  Google Scholar 

  208. Rajakaruna, N. 2003. Edaphic differentiation in Lasthenia: A model for studies in evolutionary ecology. Madrono 50: 34–40.

    Google Scholar 

  209. ——— 2004. The edaphic factor in the origin of species. International Geology Review 46: 471–478.

    Article  Google Scholar 

  210. ———, M. Y. Siddiqi, J. Whitton, B. A. Bohm & A. D. M. Glass. 2003a. Differential responses to Na+/K+ and Ca2+/Mg2+ in two edaphic races of the Lasthenia californica (Asteraceae) complex: A case for parallel evolution of physiological traits. New Phytologist 157: 93–103.

  211. ———, G. E. Bradfield, B. A. Bohm & J. Whitton. 2003b. Adaptive differentiation in response to water stress by edaphic races of Lasthenia californica (Asteraceae). International Journal of Plant Sciences 164: 371–376.

  212. ———, Baldwin, B. G., R. Chan, A. M. Desrochers, B. A. Bohm, & J. Whitton. 2003c. Edaphic races and phylogenetic taxa in the Lasthenia californica complex (Asteraceae: Heliantheae): An hypothesis of parallel evolution. Molecular Ecology 12: 1675–1679.

  213. ——— & J. Whitton. 2004. Trends in the evolution of edaphic specialists with an example of parallel evolution in the Lasthenia californica complex. Pp. 103–110. In: Q. C. B. Cronk, J. Whitton, R. Ree & I. E. P. Taylor (eds.), Plant adaptation: molecular genetics and ecology. NRC Research Press, Ottawa.

  214. ———, R. S. Boyd & T. B. Harris. 2014. Synthesis and future directions: What have harsh environments taught us about ecology, evolution, conservation and restoration. Pp. 393–409. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Inc., NY.

  215. Rascio, N. & F. Navari-Izzo. 2011. Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Science 180: 169–181.

    CAS  PubMed  Article  Google Scholar 

  216. Raven, P. H. 1964. Catastrophic selection and edaphic endemism. Evolution 18: 336–338.

    Article  Google Scholar 

  217. Renaut, S., C. J. Grassa, S. Yeaman, Z. Lai, N. K. Kane, B. T. Moyers, J. E. Bowers, J. M. Burke & L. H. Rieseberg. 2013. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nature Communications 1827: doi:https://doi.org/10.1038/ncomms2833.

  218. Rice, K. 1989. Competitive interactions in California annual grasslands. Pp. 59–72. In: L. F. Huenneke & H. A. Mooney (eds.), Grassland structure and function: California annual grassland. Kluwer, Dordrecht.

    Google Scholar 

  219. Roda, F., L. Ambrose, G. M. Walter, G,. H. L. Liu, L. Schaul, A. Lowe, P. B. Pelser, P. Prentis, L. H. Rieseberg & D. Ortiz-Barrientos. 2013. Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex. Molecular Ecology 22: 2941–2952.

    CAS  PubMed  Article  Google Scholar 

  220. Roux, C., V. Castric, M. Pauwels, S. I. Wright, P. Saumitou-Laprade & X. Vekemans. 2011. Does speciation between Arabidopsis halleri and Arabidopsis lyrata coincide with major changes in a molecular target of adaptation? PLoS ONE 6: e26872.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  221. Roy, S. J., E. J. Tucker & M. Tester. 2011. Genetic analysis of abiotic stress tolerance in crops. Current Opinion in Plant Biology 14: 232–239.

    CAS  PubMed  Article  Google Scholar 

  222. Rozema, J. & H. Schat. 2013. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environmental and Experimental Botany 92: 83–95.

    CAS  Article  Google Scholar 

  223. Sambatti, J. B. & K. J. Rice. 2007. Functional ecology of ecotypic differentiation in the Californian serpentine sunflower (Helianthus exilis). New Phytologist 175: 107–119.

    CAS  PubMed  Article  Google Scholar 

  224. Sánchez, A. M., P. Alonso-Valiente, M. J. Albert & A. Escudero. 2017. How might edaphic specialists in gypsum islands respond to climate change? Reciprocal sowing experiment to infer local adaptation and phenotypic plasticity. Annals of Botany 120: 135–146.

    PubMed  Article  Google Scholar 

  225. Saslis-Lagoudakis, C. H., C. Moray & L. Bromham. 2014. Evolution of salt tolerance in angiosperms: a phylogenetic approach. Pp. 77–95. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, Hauppauge, New York.

    Google Scholar 

  226. Savolainen, V., M.-C. Anstett, C. Lexer, I. Hutton, J. J. Clarkson, M. V. Norup, M. P. Powell, D. Springate, N. Salamin & W. J. Baker. 2006. Sympatric speciation in palms on an oceanic island. Nature 441: 210–213.

    CAS  PubMed  Article  Google Scholar 

  227. Schechter, S. P. & T. D. Bruns. 2008. Serpentine and non-serpentine ecotypes of Collinsia sparsiflora associate with distinct arbuscular mycorrhizal fungal assemblages. Molecular Ecology 17: 3198–3210.

    CAS  PubMed  Article  Google Scholar 

  228. ——— & T. D. Bruns. 2013. A common garden test of host-symbiont specificity supports a dominant role for soil type in determining AMF assemblage structure in Collinsia sparsiflora. PLOS One 8: e55507.

  229. ——— & S. Branco. 2014. The ecology and evolution of mycorrhizal fungi in extreme soils. Pp. 33–52. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, New York.

  230. Schemske, D. W. 2010. Adaptation and the origin of species. American Naturalist 176: S4–S25.

    PubMed  Article  Google Scholar 

  231. Schiavon, M. & E. A. H. Pilon-Smits. 2017. The fascinating facets of plant selenium accumulation – biochemistry, physiology, evolution and ecology. New Phytologist 213: 1582–1596.

  232. Schmickl, R. & M. A. Koch. 2011. Arabidopsis hybrid speciation processes. Proceedings of the National Academy of Sciences of the United States of America 108: 14192–14197.

    PubMed  PubMed Central  Article  Google Scholar 

  233. Schneider, A. C., W. A. Freyman, C. M. Guilliams, Y. P. Springer & B. G. Baldwin. 2016. Pleistocene radiation of the serpentine-adapted genus Hesperolinon and other divergence times in Linaceae (Malpighiales). American Journal of Botany 103: 221–232.

    PubMed  Article  Google Scholar 

  234. Searcy, K. B. & D. L. Mulcahy. 1985. Pollen selection and the gametophytic expression of metal tolerance in Silene dioica (caryophyllaceae) and Mimulus guttatus (Scrophulariaceae). American Journal of Botany 72: 1700–1706.

    Article  Google Scholar 

  235. ——— & M. R. Macnair. 1990. Differential seed production in Mimulus guttatus Fisch, ex DC in response to increasing concentrations of copper in the pistil by pollen from copper tolerant and sensitive sources. Evolution 44: 1424–1435.

  236. ——— & M. R. Macnair. 1993. Developmental selection in response to environmental conditions of the maternal parent in Mimulus guttatus. Evolution 47: 13–24.

  237. Selby, J. P., A. L. Jeong, K. Toll, K. M. Wright, D. B. Lowry. 2014. Methods and discoveries in the pursuit of understanding the genetic basis of adaptation to harsh environments in Mimulus. Pp. 243–265. In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, New York.

    Google Scholar 

  238. Shimizu-Inatsugi, R., A. Terada, K. Hirose, H. Kudoh, J. Sese & K. K. Shimizu. 2016. Plant adaptive radiation mediated by polyploid plasticity in transcriptomes. Molecular Ecology 26: 193–207.

    PubMed  Article  CAS  Google Scholar 

  239. Silvertown, J., C. Servaes, P. Biss & D. Macleod. 2005. Reinforcement of reproductive isolation between adjacent populations in the Park Grass Experiment. Heredity 95: 198–205.

    CAS  PubMed  Article  Google Scholar 

  240. ———, P. Poulton, E. Johnston, G. Edwards, M. Heard & P. M. Biss. 2006. The Park Grass Experiment 1856–2006: its contribution to ecology. Journal of Ecology 94: 801–814.

  241. Slovák, M., J. Kučera, P. Turis & J. Zozomová-Lihová. 2012. Multiple glacial refugia and postglacial colonization routes inferred for a woodland geophyte, Cyclamen purpurascens: patterns concordant with the Pleistocene history of broadleaved and coniferous tree species. Biological Journal of the Linnean Society: 105: 741–760.

    Article  Google Scholar 

  242. Smith, S. E. & M. R. Macnair. 1998. Hypostatic modifiers cause variation in degree of copper tolerance in Mimulus guttatus. Heredity 80: 760–768.

    CAS  Article  Google Scholar 

  243. Sobel, J. M. 2014. Ecogeographic isolation and speciation in the genus Mimulus. American Naturalist 184: 565–579.

    PubMed  Article  Google Scholar 

  244. Sobczyk, M. K., J. A. C. Smith, A. J. Pollard & D. A. Filatov. 2017. Evolution of nickel hyperaccumulation and serpentine adaptation in the Alyssum serpyllifolium species complex. Heredity 118: 31–41.

    CAS  PubMed  Article  Google Scholar 

  245. Soltis, D. E., P. S. Soltis & J. A. Tate. 2004. Advances in the study of polyploidy since plant speciation. New Phytologist 161: 173–191.

    CAS  Article  Google Scholar 

  246. Southworth, D., L. E. Tackaberry & H. B. Massicotte. 2014. Mycorrhizal ecology on serpentine soils. Plant Ecology and Diversity 7: 445–455.

    Article  Google Scholar 

  247. Spasojevic, M. J., E. I. Damschen & S. P. Harrison. 2014. Patterns of seed dispersal syndromes on serpentine soils: examining the roles of habitat patchiness, soil infertility and correlated functional traits. Plant Ecology and Diversity 7: 401–410.

    Article  Google Scholar 

  248. Springer, Y. P. 2007. Clinal resistance structure and pathogen local adaptation in a serpentine flax-flax rust interaction. Evolution 61: 1812–1822.

    PubMed  Article  Google Scholar 

  249. ——— 2009. Edaphic quality and plant-pathogen interactions: Effects of soil calcium on fungal infection of a serpentine flax. Ecology 90: 1852–1862.

    PubMed  Article  Google Scholar 

  250. Strasburg, J. L., N. A. Sherman, K. M. Wright, L. C. Moyle, J. H. Willis & L. H. Rieseberg. 2012. What can patterns of differentiation across plant genomes tell us about adaptation and speciation? Philosophical Transactions of the Royal Society London B Biological Sciences 367: 364–373.

    Article  Google Scholar 

  251. Strauss, S. Y. & R. S. Boyd. 2011. Herbivory and other cross-kingdom interactions on harsh soils. Pp. 181–199. In: S. P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  252. ——— & N. I. Cacho. 2013. Nowhere to run, nowhere to hide: The importance of enemies and apparency in adaptation to harsh soil environments. American Naturalist 182: E1–E14.

  253. Sun, G. & P. Schliekelman. 2011. A genetical genomics approach to genome scans increases power for QTL mapping, Genetics 187: 939–953.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  254. Thrall, P. H., M. E. Hochberg, J. J. Burdon & J. D. Bever. 2007. Coevolution of symbiotic mutualists and parasites in a community context. Trends in Ecology & Evolution 22: 120–126.

    Article  Google Scholar 

  255. ———, J. D. Bever & J. F. Slattery. 2008. Rhizobial mediation of Acacia adaptation to soil salinity: evidence of underlying trade-offs and tests of expected patterns. Journal of Ecology 96: 746–755.

  256. Tiffin, P. & J Ross-Ibarra. 2014. Advances and limits of using population genetics to understand local adaptation. Trends in Ecology & Evolution 29: 673–680.

    Article  Google Scholar 

  257. Turesson, G. 1922. The species and the variety as ecological units. Hereditas 3: 100–113.

    Article  Google Scholar 

  258. Turner, T. L., E. J. von Wettberg, S. V. Nuzhdin. 2008. Genomic analysis of differentiation between soil types reveals candidate genes for local adaptation in Arabidopsis lyrata. PLOS One 3: e3183.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  259. ———, E. C. Bourne, E. J. Von Wettberg, T. T. Hu, S. V. Nuzhdin. 2010. Population resequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nature Genetics 42: 260–263.

  260. Twyford, A.D. & J. Friedman. 2015. Adaptive divergence in the monkey flower Mimulus guttatus is maintained by a chromosomal inversion. Evolution 69: 1476–1486.

    PubMed  PubMed Central  Article  Google Scholar 

  261. Valladares, F., S. Matesanz, F. Guilhaumon, M. B. Araújo, L. Balaguer, M. Benito-Garzón, W. Cornwell, E. Gianoli, M. van Kleunen, D. E. Naya, A. B. Nicotra, H. Poorter & M. A. Zavala. 2014. The effects of phenotypic plasticity and local adaptation on forecasts of species range shifts under climate change. Ecology Letters 17: 1351–1364.

    PubMed  Article  Google Scholar 

  262. Vallano, D. M., P. C. Selmants & E. S. Zavaleta. 2012. Simulated nitrogen deposition enhances the performance of an exotic grass relative to native serpentine grassland competitors. Plant Ecology 213: 1015–1026.

    Article  Google Scholar 

  263. Vamosi, J. C., W. S. Armbruster & S. S. Renner. 2014. Evolutionary ecology of specialization: insights from phylogenetic analysis. Proceedings of the Royal Society B: Biological Sciences 281: 20142004.

    PubMed  PubMed Central  Article  Google Scholar 

  264. van der Niet, T. & S. D. Johnson. 2009. Patterns of plant speciation in the Cape floristic region, Molecular Phylogenetics and Evolution 51: 85–93.

    PubMed  Article  Google Scholar 

  265. van Hoof, N. A. L. M., V. H. Hassinen, H. W. J. Hakvoort, K. F. Ballintijn, H. Schat, J. A.C. Verkleij, W. H.O. Ernst, S. O. Karenlampi & A. I. Tervahauta. 2001. Enhanced copper tolerance in Silene vulgaris (Moench) Garcke populations from copper mines is associated with increased transcript levels of a 2b-type metallothionein gene. Plant Physiology 126: 1519–1526.

    PubMed  PubMed Central  Article  Google Scholar 

  266. Van Nuland, M. E. 2016. Plant–soil feedbacks: connecting ecosystem ecology and evolution. Functional Ecology 30: 1032–1042.

    Article  Google Scholar 

  267. Van Zandt, P. A. 2007. Plant defense, growth, and habitat: a comparative assessment of constitutive and induced resistance. Ecology 88: 1984–1993.

    PubMed  Article  Google Scholar 

  268. Vekemans, X. & C. Lefèbvre. 1997. On the evolution of heavy-metal tolerant populations in Armeria maritima: evidence from allozyme variation and reproductive barriers. Journal of Evolutionary Biology 10: 175–191.

    Article  Google Scholar 

  269. Venables, A. V. & D. A. Wilkins. 1978. Salt tolerance in pasture grasses. New Phytologist 80: 613–622.

    CAS  Article  Google Scholar 

  270. Verbruggen, N., C. Hermans & H. Schat. 2009. Molecular mechanisms of metal hyperaccumulation in plants. New Phytologist 181: 759–776.

    CAS  PubMed  Article  Google Scholar 

  271. Via, S. 2009. Natural selection in action during speciation. Proceedings of the National Academy of Sciences of the United States of America 106: 9939–9946.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  272. von Wettberg, E. J. & J. W. Wright. 2011. Genomic approaches to understanding adaptation. Pp. 139–153. In: S.P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

    Google Scholar 

  273. ———, J. Ray-Mukherjee, N. D’Adesky, D. Nesbeth & S. Sistla. 2014. The evolutionary ecology and genetics of stress resistance syndrome (SRS) traits: revisiting Chapin, Autumn and Pugnaire (1993). Pp.201–226.In: N. Rajakaruna, R. S. Boyd & T. B. Harris (eds.), Plant ecology and evolution in harsh environments. Nova Science Publishers, New York.

  274. Wallace, D. R. 1983. The Klamath Knot. University of California Press, Berkeley.

    Google Scholar 

  275. Westerbergh, A. & A. Saura. 1992. The effect of serpentine on the population structure of Silene dioica (Caryophyllaceae). Evolution 46: 1537–1548.

    CAS  PubMed  Article  Google Scholar 

  276. Widmer, A., C. Lexer & S. Cozzolino. 2009. Evolution of reproductive isolation in plants. Heredity 102: 31–38.

    CAS  PubMed  Article  Google Scholar 

  277. Williams, J. L., R. E. Snyder & J. M. Levine. 2016. The influence of evolution on population spread through patchy landscapes. American Naturalist 188: 15–26.

    PubMed  Article  Google Scholar 

  278. Wright, J. W. & M. L. Stanton. 2007. Collinsia sparsiflora in serpentine and nonserpentine habitats: Using F2 hybrids to detect the potential role of selection in ecotypic differentiation. New Phytologist 173: 354–366.

    PubMed  Article  Google Scholar 

  279. ——— & M. L. Stanton. 2011. Local adaptation in heterogeneous landscapes–reciprocal transplant experiments and beyond. Pp. 155–180. In: S.P. Harrison & N. Rajakaruna (eds.), Serpentine: the evolution and ecology of a model system. University of California Press, Berkeley.

  280. Wright, K. M., D. Lloyd, D. B. Lowry, M. R. Macnair & J.H. Willis. 2013. Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLOS Biology 11: e1001497.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  281. Wu, C. A., D. B. Lowry, L. I. Nutter & J. H. Willis. 2010. Natural variation for drought-response traits in the Mimulus guttatus species complex. Oecologia, 162: 23–33.

    PubMed  Article  Google Scholar 

  282. Wu, L., A. D. Bradshaw & D. A. Thurman. 1975. The potential for evolution of heavy metal tolerance in plants. I. The rapid evolution of copper tolerance in Agrostis stolonifera. Heredity 34: 165–178.

    Article  Google Scholar 

  283. Yakimowski, S.B. & L.H. Rieseberg. 2014. The role of homoploid hybridization in evolution: A century of studies synthesizing genetics and ecology. American Journal of Botany 101: 1247–1258.

    PubMed  Article  Google Scholar 

  284. Yost, J. M., T. M. Barry, K. M. Kay & N. Rajakaruna. 2012. Edaphic adaptation maintains the coexistence of two cryptic species on serpentine soils. American Journal of Botany 99: 890–897.

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgments

I would like to thank Bob Boyd, Ian Medeiros, Elizabeth Farnsworth, Susan Harrison, Tanner Harris, and Jonathan Gressel for constructive comments on earlier drafts of the manuscript. Additional comments from Mark R. Macnair and an anonymous reviewer greatly improved the manuscript. Funding from the US-Sri Lanka Fulbright Commission during the writing of this review is gratefully acknowledged.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Nishanta Rajakaruna.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rajakaruna, N. Lessons on Evolution from the Study of Edaphic Specialization. Bot. Rev. 84, 39–78 (2018). https://doi.org/10.1007/s12229-017-9193-2

Download citation

Keywords

  • Ecological Speciation
  • Edaphic Endemism
  • Harsh Environments
  • Cost of Tolerance
  • Serpentine
  • Metal Tolerance
  • Parallel Speciation
  • Geobotany
  • Plant-Soil Relations
  • Local Adaptation