Plant Ecology

, Volume 213, Issue 10, pp 1555–1569 | Cite as

Negative evidence of local adaptation to the establishment conditions in a perennial herb

  • José L. GarridoEmail author
  • Pedro J. Rey
  • Carlos M. Herrera
  • José M. Ramírez


The differential adaptation of populations of the same species to their local environmental conditions through divergent selection, known as local adaptation, is a key step in the process of diversification of species. Here, we explore the local adaptation of the perennial mountain herb Helleborus foetidus to variable environmental conditions of seedling emergence and establishment at two different spatial scales (habitats and regions) with special attention to the role of physical and chemical soil properties. The possibility of local adaptation was evaluated under the “local versus foreign” and the “home versus away” criteria. Reciprocal sowing experiments were carried out by cross-sowing seeds among habitats and regions, controlling for maternal effects by means of seed mass, and recording seedling emergence and survival. Several topsoil properties were measured linked to each sowing point. Only partial patterns of local adaptation were found, which were insufficient to eventually state the existence of local adaptation at any spatial scale or under any criteria assessed. Here, we discuss how soil properties and selection on seed size may be related to the non-achievement of local adaptation criteria. Negative evidence of local adaptation seems to be due to a congruency in the selective pressures exerted by the different soil environments on seedling emergence and survival.


Local adaptation Helleborus foetidus Topsoil properties Seedling emergence Seedling establishment Divergent selection 



The authors thank Jorge Garrido and Ester Orive for their invaluable field assistance. The experiments performed in this work comply with all current Spanish law on investigation matters. We also thank the Junta Rectora of the Natural Parks of “Sierra de Cazorla, Segura y Las Villas” and “Sierra Mágina” for providing working facilities. This study was supported by grant PB96-0856 (DGES: Ministerio de Educación y Cultura, Spain).

Supplementary material

11258_2012_111_MOESM1_ESM.pdf (51 kb)
Appendix 1. Relationship between water availability and water retention capacity across the four habitats considered. Contrarily to the rest of habitats, at Dense Oakwood soils, water availability increased with retention capacity. (PDF 50 kb)


  1. Alcántara JM, Rey PJ (2003) Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird-dispersed tree, Olea europaea. J Evol Biol 16:1168–1176PubMedCrossRefGoogle Scholar
  2. Arp PA (1984) Forest floor variability and factor analysis: a case study. Can J Soil Sci 64:457–461CrossRefGoogle Scholar
  3. Arp PA, Krause HH (1984) The forest floor: lateral variability as revealed by systematic sampling. Can J Soil Sci 64:423–437CrossRefGoogle Scholar
  4. Becker U, Colling G, Dostal P, Jakobsson A, Matthies D (2006) Local adaptation in the monocarpic perennial Carlina vulgaris at different spatial scales across Europe. Oecologia 150:506–518PubMedCrossRefGoogle Scholar
  5. Becker U, Dostal P, LD Jorritsma-Wienk, Matthies D (2008) The spatial scale of adaptive population differentiation in a wide-spread, well-dispersed plant species. Oikos 117:1865–1873CrossRefGoogle Scholar
  6. Bischoff A, Vonlanthen B, Steinger T, Muller-Scharer H (2006) Seed provenance matters—effects on germination of four plant species used for ecological restoration. Basic Appl Ecol 7:347–359CrossRefGoogle Scholar
  7. Burton PJ, Mueller-Dombois D (1984) Response of Metrosideros polymorpha seedlings to experimental canopy opening. Ecology 65:779–791CrossRefGoogle Scholar
  8. Cornelissen JHC, Castro-Diez P, Carnelli AL (1998) Variation in relative growth rate among woody species. In: Lambers H, Pooter H, van Vuuren MMI (eds) Inherent variation in plant growth. Backhuys Publishers, Leiden, pp 363–392Google Scholar
  9. Eriksson O (1995) Seedling recruitment in deciduous forests herbs: the effects of litter, soil chemistry and seed bank. Flora 190:65–70Google Scholar
  10. Evans JR, Etherington CE (1990) The effect of soil water potential on seed germination of some British plants. New Phytol 115:539–548CrossRefGoogle Scholar
  11. Fedriani JM, Rey PJ, Garrido JL, Guitián J, Herrera CM, Medrano M, Sánchez-Lafuente AM, Cerdá X (2004) Geographical variation in the potential of mice to constrain an ant-seed dispersal mutualism. Oikos 105:181–191CrossRefGoogle Scholar
  12. Galloway LF, Fenster CB (2000) Population differentiation in an annual legume: local adaptation. Evolution 54:1173–1181PubMedGoogle Scholar
  13. Garrido JL (2003) Seeds and seedlings of Helleborus foetidus L. (Ranunculaceae): geographic variation, ecology and evolution. PhD, University of Jaén, SpainGoogle Scholar
  14. Garrido JL, Rey PJ, Cerdá X, Herrera CM (2002) Geographical variation in diaspore traits of an ant-dispersed plant (Helleborus foetidus): are ant community composition and diaspore traits correlated? J Ecol 90:446–455CrossRefGoogle Scholar
  15. Garrido JL, Rey PJ, Herrera CM (2005) Pre- and post-germination determinants of spatial variation in recruitment in the perennial herb Helleborus foetidus L. (Ranunculaceae). J Ecol 93:60–66CrossRefGoogle Scholar
  16. Garrido JL, Rey PJ, Herrera CM (2007) Regional and local variation in seedling emergence, mortality and recruitment of a perennial herb in Mediterranean mountain habitats. Plant Ecol 190:109–121CrossRefGoogle Scholar
  17. Godínez-Álvarez H, Valiente-Banuet A (1998) Germination and early seedling growth of Tehuacan Valley cacti species: the role of soils and seed ingestion by dispersers on seedling growth. J Arid Environ 39:21–31CrossRefGoogle Scholar
  18. Gómez JM (2004) Bigger is not always better: conflicting selective pressures on seed size in Quercus ilex. Evolution 58:71–80Google Scholar
  19. Gómez-Aparicio L (2009) The role of plant interactions in the restoration of degraded ecosystems: a meta-analysis across life forms and ecosystems. J Ecol 97:1202–1214CrossRefGoogle Scholar
  20. Gregor JW (1930) Experiments on the genetics of wild populations. I. Plantago maritima. J Gen 22:15–25CrossRefGoogle Scholar
  21. Hammond DS, Brown VK, Zagt R (1999) Spatial and temporal patterns of seed attack and germination in a large-seeded neotropical tree species. Oecologia 119:208–218CrossRefGoogle Scholar
  22. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. Am Nat 173:579–588PubMedCrossRefGoogle Scholar
  23. Herrera CM (2000) Individual differences in progeny viability in Lavandula latifolia: a long-term field study. Ecology 81:3036–3047Google Scholar
  24. Herrera CM (2002) Topsoil properties and seedling recruitment: stage-dependence and spatial decoupling of influential parameters. Oikos 97:260–270CrossRefGoogle Scholar
  25. Herrera CM, Jordano P, López-Soria L, Amat JA (1994) Recruitment of a mast-fruiting, bird-dispersed tree—bridging frugivore activity and seedling establishment. Ecol Monogr 64:315–344CrossRefGoogle Scholar
  26. Herrera CM, Sánchez-Lafuente AM, Medrano M, Guitián J, Cerdá X, Rey P (2001) Geographical variation in autonomous self-pollination levels unrelated to pollinator service in Helleborus Foetidus (Ranunculaceae). Am J Bot 88:1025–1032PubMedCrossRefGoogle Scholar
  27. Horvitz CC, Schemske DW (1986) Seed dispersal and environmental heterogeneity in a neotropical herb: a model of population and patch dynamics. In: Estrada A, Fleming TH (eds) Frugivores and seed dispersal. Junk, Dordrecht, pp 169–186CrossRefGoogle Scholar
  28. Howe HF, Richter W (1982) Effects of seed size on seedling size in Virola surinamensis; a within and between tree analysis. Oecologia 53:347–351CrossRefGoogle Scholar
  29. Hufford KM, Mazer SJ, Camara MD (2008) Local adaptation and effects of grazing among seedlings of two native California bunchgrass species: implications for restoration. Restor Ecol 16:59–69CrossRefGoogle Scholar
  30. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecol Lett 7:1225–1241CrossRefGoogle Scholar
  31. Kikuzawa K, Koyama H (1999) Scaling of soil water absorption by seeds: an experiment using seed analogues. Seed Sci Res 9:171–178Google Scholar
  32. Kitajima K (1992) The importance of cotyledon functional morphology and patterns of seed reserve utilization for the physiological ecology of neotropical tree seedlings. PhD thesis, University of IllinoisGoogle Scholar
  33. Kitajima K, Fenner M (2000) Ecology of seedling regeneration. In: Fenner M (ed) Seeds. Cabi Publishing, Wallingford, pp 331–359Google Scholar
  34. Leimu R, Fischer M (2008) A meta-analysis of local adaptation in plants. PLoS ONE 3:e4010PubMedCrossRefGoogle Scholar
  35. Linhart YB, Grant MC (1996) Evolutionary significance of local genetic differentiation in plants. An Rev Ecol Syst 27:237–277CrossRefGoogle Scholar
  36. Macel M, Lawson CS, Mortimer SR, Smilauerova M, Bischoff A, Cremieux L, Dolezal J, Edwards AR, Lanta V, Bezemer TM, van der Putten WH, Igual JM, Rodríguez-Barrueco C, Muller-Scharer H, Steinger T (2007) Climate vs. soil factors in local adaptation of two common plant species. Ecology 88:424–433Google Scholar
  37. Manzaneda AJ, Rey PJ, Boulay R (2007) Geographic and temporal variation in the ant–seed dispersal assemblage of the perennial herb Helleborus foetidus L. (Ranunculaceae). Biol J Linn Soc 92:135–150CrossRefGoogle Scholar
  38. Manzaneda AJ, Rey PJ, Alcántara JM (2009) Conflicting selection on diaspore traits limits the evolutionary potential of seed dispersal by ants. J Evol Biol 22:1407–1417PubMedCrossRefGoogle Scholar
  39. Molofsky J, Augspurger CK (1992) The effect of leaf litter on early seedling establishment in a tropical forest. Ecology 73:68–77CrossRefGoogle Scholar
  40. Núñez-Farfán J, Dirzo R (1988) Within-gap spatial heterogeneity and seedling performance in a Mexican tropical forest. Oikos 51:274–284CrossRefGoogle Scholar
  41. Núñez-Farfán J, Schlichting CD (2001) Evolution in changing environments: the “synthetic” work of Clausen, Keck and Hiesey. Q Rev Biol 76:433–457PubMedCrossRefGoogle Scholar
  42. Ortegón-Campos I, Abdala-Roberts L, Parra-Tabla V, Carlos Cervera J, Marrufo-Zapata D, Herrera CM (2011) Influence of multiple factors on plant local adaptation: soil type and folivore effects in Ruellia nudiflora (Acanthaceae). Evol Ecol (in press). doi: 10.1007/s10682-011-9507-5
  43. Pabin J, Lipitec J, Wlodek SEA (1998) Critical soil bulk-density and strength for pea seedling root-growth as related to other soil factors. Soil Tillage Res 46:203–208CrossRefGoogle Scholar
  44. Packer A, Clay K (2000) Soil pathogens and spatial patterns of seedling mortality in a temperate tree. Nature 404:278–281PubMedCrossRefGoogle Scholar
  45. Pigliucci M (2001) Phenotypic plasticity. Beyond nature and nurture. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  46. Pugnaire FI, Haase P, Puigdefábregas J (1996a) Facilitation between higher plant species in a semiarid environment. Ecology 77:1420–1426CrossRefGoogle Scholar
  47. Pugnaire FI, Haase P, Puigdefábregas J, Cueto M, Incoll LD, Clark SC (1996b) Facilitation and succession under the canopy of the leguminous shrub, Retama sphaerocarpa, in a semiarid environment in south-east Spain. Oikos 76:455–464CrossRefGoogle Scholar
  48. Raabová J, Münzbergová Z, Fischer M (2011) The role of spatial scale and soil for local adaptation in Inula hirta. Basic Appl Ecol 12:152–160CrossRefGoogle Scholar
  49. Rendon B, Núñez-Farfán J (2001) Population differentiation and phenotypic plasticity of wild and agrestal populations of the annual Anoda cristata (Malvaceae) growing in two contrasting habitats. Plant Ecol 156:205–213CrossRefGoogle Scholar
  50. Rey PJ, Alcántara JM, Valera F, Sánchez-Lafuente AM, Garrido JL, Ramírez JM, Manzaneda AJ (2004) Seedling establishment in Olea europaea: seed size and microhabitat affect growth and survival. Ecoscience 11:310–320Google Scholar
  51. Sáenz-Romero C, Guries RP (2002) Landscape genetic structure of Pinus banksiana seedling traits. Silvae Genet 51:26–35Google Scholar
  52. SAS Institute (2004) SAS/STAT 9.1. User’s guide. SAS Institute, CaryGoogle Scholar
  53. Saxena NP, Johansen C, Saxena MC, Silim SN (1993) Selection for drought and salinity tolerance in cool-season food legumes. In: Singh KB, Saxena MC (eds) Breeding for tolerance in cool season food legumes. Wiley, Chichester, pp 245–270Google Scholar
  54. Schupp EW (1995) Seed-seedling conflicts, habitat choice, and patterns of plant recruitment. Am J Bot 82:399–409CrossRefGoogle Scholar
  55. Shea KL (1989) Genetic variation between and within populations of Engelmann spruce and subalpine fir. Genome 33:1–8CrossRefGoogle Scholar
  56. Siles G, Rey PJ, Alcántara JM (2010) Post-fire restoration of Mediterranean forests: testing assembly rules mediated by facilitation. Basic Appl Ecol 11:422–431CrossRefGoogle Scholar
  57. Stratton DA, Bennington CC (1998) Fine-grained spatial and temporal variation in selection does not maintain genetic variation in Erigeron annuus. Evolution 52:678–691CrossRefGoogle Scholar
  58. Townend J, Mtakwa PW, Mullins CE, Simmonds LP (1996) Soil physical factors limiting establishment of sorghum and cowpea in two contrasting soil types in the semi-arid tropics. Soil Tillage Res 40:89–106Google Scholar
  59. Turesson G (1922) The genotypical response of the plant species to the habitat. Hereditas 4:171–176CrossRefGoogle Scholar
  60. Valverde T, Silvertown J (1995) Spatial variation in the seed ecology of woodland herb (Primula vulgaris) in relation to light environment. Funct Ecol 9:942–950CrossRefGoogle Scholar
  61. Vander Mijnsbrugge K, De Cock K, Cox K, Breyne P (2010) Conservation measures for Rosa arvensis Huds. in Flanders (Belgium) based on congruent genetic and phenotypic population differentiation. Conserv Genet 11:2243–2253CrossRefGoogle Scholar
  62. Verdú M, García-Fayos P (1996) Postdispersal seed predation in a Mediterranean patchy landscape. A Oecol 17:379–391Google Scholar
  63. Vessal S, Palta JA, Atkins CA, Siddique KHM (2012) Development of an assay to evaluate differences in germination rate among chickpea genotypes under limited water content. Funct Plant Biol 39:60–70CrossRefGoogle Scholar
  64. Vleeshouwers LM (1997) Modelling the effect of temperature, soil penetration resistance, burial depth and seed weight on pre-emergence growth of weeds. Ann Bot 79:553–563Google Scholar
  65. Walters MB, Reich PB (1997) Growth of Acer saccharum seedlings in deeply shaded understories of northern Wisconsin: effects of nitrogen and water availability. Can J Forest Res 27:237–247CrossRefGoogle Scholar
  66. Webster R, Butler BE (1976) Soil classification and survey studies at Ginninderra. Aust J Soil Res 14:1–24CrossRefGoogle Scholar
  67. Werner K, Ebel F (1994) Life-history of the genus Helleborus L (Ranunculaceae). Flora 189:97–130Google Scholar
  68. Whitlock MC (2003) Fixation probability and time in subdivided populations. Genetics 164:767–779PubMedGoogle Scholar
  69. Williams GC (1966) Adaptation and natural selection. Princeton University Press, PrincetonGoogle Scholar
  70. Zamora R (2002) Environmental heterogeneity and the ecology of carnivorous plants: implications for conservation. Rev Chil Hist Nat 75:17–26CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • José L. Garrido
    • 1
    Email author
  • Pedro J. Rey
    • 2
  • Carlos M. Herrera
    • 1
  • José M. Ramírez
    • 2
  1. 1.Estación Biológica de DoñanaConsejo Superior de Investigaciones Científicas (CSIC)SevillaSpain
  2. 2.Departamento de Biología Animal, Biología Vegetal y EcologíaUniversidad de JaénJaénSpain

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