Skip to main content
Log in

Geographic variation in the adaptive landscape for seed size at dispersal in the myrmecochorous Helleborus foetidus

  • Original Paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

Literature on seed dispersal mutualisms suggests that plant populations should hardly adapt to their current dispersers. We address the predictions that selection pressures exerted by ants on dispersal-related diaspore traits of the ant-dispersed Helleborus foetidus are highly variable in space, and that geographic (inter-population) variation in these traits is unrelated to selection by current dispersers. To test these predictions we use the concept of the quantitative adaptive landscape for seed size at dispersal. Such landscape depicts the relationship between the population’s mean trait value (mean seed size in the present study) and the population’s mean fitness (mean dispersal probability in the present study). Adaptive landscapes make it possible to assess whether the mean population’s phenotype agrees with one favored by selection. We first analyse, in 12 populations of H. foetidus from southern Spain, the extent of divergence among populations in seed and elaiosome size, and the abundance, composition, and behavior of the ant communities. Seeds from a fixed set of five of these populations were offered to ants in all the study sites to fit the adaptive landscape for seed size. In addition, seeds from the local population were also offered in each site. Our results show that seed size has undergone a larger divergence among populations than elaiosome size. Despite geographic variation in ant assemblages, the adaptive landscapes for seed size at dispersal were remarkably similar among sites: ants create disruptive selection on seed size in 10 out of 12 study sites. As predicted, the basic features of these adaptive landscapes (curvature and location of the minimum) varied geographically in accordance with variation in the size of seed dispersers. Also as predicted, in most populations, the observed mean seed size does not agree with that expected from the adaptive landscapes at dispersal. However, the relevance of dispersers for seed size evolution should not be neglected since the agreement between observed and optimum seed size was stronger where dispersers were more abundant. Thus, against the general view, our results evidence that, in H. foetidus, the observed geographic variation in dispersal-related plant traits is partly linked to selection exerted by current dispersers. Geographic variation in ant assemblages determines both the existence of a selection mosaic and the degree of adjustment of populations to the patterns of selection in the mosaic.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • 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 16:1168–1176

    Article  PubMed  Google Scholar 

  • Armbruster WS (1990) Estimating and testing the shapes of adaptive surfaces: the morphology and pollination of Dalechampia blossoms. Am Nat 135:14–31

    Article  Google Scholar 

  • Arnold SJ, Pfrender ME, Jones AG (2001) The adaptive landscape as a conceptual bridge between micro- and macroevolution. Genetica 112:9–32

    Article  PubMed  Google Scholar 

  • Auld TD, Denham AJ (1999) The role of ants and mammals in dispersal and post-dispersal seed predation of the shrubs Grevillea (Proteaceae). Plant Ecol 144:201–213

    Article  Google Scholar 

  • Beattie AJ, Culver DC (1981) The guild of myrmecochores in the herbaceous flora of West Virginia forests. Ecology 62:107–115

    Article  Google Scholar 

  • Beattie AJ, Hughes L (2002) Ant–plant interactions. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 211–235

    Google Scholar 

  • Boulay R, Coll-Toledano J, Cerda X (2006) Geographic variations in Helleborus foetidus elaiosome lipid composition: implications for dispersal by ants. Chemoecology 16:1–7

    Article  CAS  Google Scholar 

  • Cerdá X, Retana J, Manzaneda A (1998) The role of competition by dominants and temperatura in the foraging of the subordinate species in Mediterranean ants communities. Oecologia 117:404–412

    Article  Google Scholar 

  • Christian CE (2001) Consequences of a biological invasion reveal the importance of mutualism for plant communities. Nature 413:635–639

    Article  PubMed  CAS  Google Scholar 

  • Cottingham KL, Lennon JT, Brown BL (2005) Knowing when to draw the line: designing more informative ecological experiments. Front Ecol Environ 3:145–152

    Google Scholar 

  • Fenner M (2000) Seeds: the ecology of regeneration in plant communities. CABI Publishing, Wallingford

    Google Scholar 

  • 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 90:446–455

    Article  Google Scholar 

  • Gandon S, Rousset F (1999) Evolution of stepping-stone dispersal rates. Proc R Soc Lond B 266:2507–2513

    Article  CAS  Google Scholar 

  • Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492

    Article  Google Scholar 

  • Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283

    Article  PubMed  CAS  Google Scholar 

  • Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727

    Google Scholar 

  • Herrera CM (1998) Long-term dynamics of Mediterranean frugivorous birds and fleshy fruits: a 12-year study. Ecol Monogr 68:511–538

    Article  Google Scholar 

  • Herrera CM (2002) Seed dispersal by vertebrates. In: Herrera CM, Pellmyr O (eds) Plant–animal interactions: an evolutionary approach. Blackwell Publishing, Oxford, pp 185–208

    Google Scholar 

  • Holt RD, McPeek MA (1996) Chaotic population dynamics favors the evolution of dispersal. Am Nat 148:709–718

    Article  Google Scholar 

  • Howe HF (1984) Constraints in the evolution of mutualisms. Am Nat 123:764–777

    Article  Google Scholar 

  • Hughes L, Westoby M (1992a) Fate of seeds adapted for dispersal by ants in Australian sclerophyll vegetation. Ecology 73:1285–1299

    Article  Google Scholar 

  • Hughes L, Westoby M (1992b) Effects of diaspore characteristics on removal of seeds adapted for dispersal by ants. Ecology 73:1300–1312

    Article  Google Scholar 

  • Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence, asymmetries, and coevolution. Am Nat 129:657–677

    Article  Google Scholar 

  • Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant–animal interactions. Am Nat 145:163–191

    Article  Google Scholar 

  • Kalisz S, Hanzawa FM, Tensor SJ, Thiede DA, Voigt S (1999) Ant-mediated seed dispersal alters patterns of relatedness in a population of Trillium grandiflorum. Ecology 80:2620–2634

    Article  Google Scholar 

  • Kaspari M (1996) Worker size and seed size selection by harvester ants in a Neotropical forest. Oecologia 105:397–404

    Article  Google Scholar 

  • Kingsolver JG, Hoekstra HE, Hoekstra JM, Berrigan D, Vignieri SN, Hill CE, Hoang A, Gibert P, Beerli P (2001) The strength of phenotypic selection in natural populations. Am Nat 157:245–261

    Article  Google Scholar 

  • Lande R (1976) Natural selection and random genetic drift in phenotypic evolution. Evolution 30:314–334

    Article  Google Scholar 

  • Lande R, Arnold SJ (1983) Measurement of selection on correlated characters. Evolution 37:1210–1226

    Article  Google Scholar 

  • Levin SA, Muller-Landau HC, Nathan R, Chave J (2003) The ecology and evolution of seed dispersal: a theoretical perspective. Annu Rev Ecol Evol Syst 34:575–604

    Article  Google Scholar 

  • Manzaneda AJ (2005) Ecología y Evolución de la dispersión de semillas en Helleborus foetidus (Ranunculaceae). Variación geográfica en las interacciones planta–animal. PhD thesis, University of Sevilla, Spain

  • Manzaneda AJ, Fedriani JM, Rey PJ (2005) Adaptive advantages of myrmecochory: the predator-avoidance hypothesis tested over a wide geographic range. Ecography 28:583–592

    Article  Google Scholar 

  • Mark S, Olesen JM (1996) Importance of elaiosome size to removal of ant-dispersed seeds. Oecologia 107:95–101

    Article  Google Scholar 

  • McKey D (1975) The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 159–191

    Google Scholar 

  • Mitchell-Olds T, Shaw RG (1987) Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161

    Article  Google Scholar 

  • Moles AT, Westoby M (2006) Seed size and plant strategy across the whole life cycle. Oikos 113:91–105

    Article  Google Scholar 

  • Møller AP, Jennions MD (2002) How much variance can be explained by ecologists and evolutionary biologists? Oecologia 132:492–500

    Article  Google Scholar 

  • Peters M, Oberrath R, Böhning-Gaese K (2003) Seed dispersal by ants: are seed preferences influenced by foraging strategies or historical constraints? Flora 198:413–420

    Google Scholar 

  • Rey PJ, Ramírez JM, Sánchez-Lafuente AM (2006) Seed- vs. microsite-limited recruitment in a myrmecochorous herb. Plant Ecol 184:213–222

    Google Scholar 

  • SAS Institute (1998) SAS System for Windows. Version 8.0. Cary, North Carolina, USA

  • Schluter D (2000) The ecology of adaptive radiation. Oxford University Press, Oxford

    Google Scholar 

  • Snow DW (1971) Evolutionary aspects of fruit-eating by birds. Ibis 113:194–202

    Google Scholar 

  • Stanton ML (2003) Interacting guilds: moving beyond the pairwise perspective on mutualisms. Am Nat 162:S10–S23

    Article  PubMed  Google Scholar 

  • StatSoft (2001) Statistica for Windows. StatSoft Inc., Tulsa

  • Steury TD, Murray DL (2005) Regression versus ANOVA. Front Ecol Environ 3, 356–357

    Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Whitlock MC, Phillips PC, Moore FB-G, Tonsor SJ (1995) Multiple fitness peaks and epistasis. Annu Rev Ecol Sys 26:601–629

    Article  Google Scholar 

  • Willson MF, Traveset A (2000) The ecology of seed dispersal. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, 2nd edn. CABI Publishing, Wallingford, pp 85–110

    Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by Ministerio de Ciencia y Tecnología (Spain) Grant BOS2000-1122-C03. R.B. was funded by the European Commission (Marie Curie Individual Fellowship number HPMF-CT-2002-01565). Ant species were determined by Alberto Tinaut. José A. Dorante and Ibama Pineda helped during field work. Jonathan B. Losos and Mark W. Blows provided helpful comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julio M. Alcántara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alcántara, J.M., Rey, P.J., Manzaneda, A.J. et al. Geographic variation in the adaptive landscape for seed size at dispersal in the myrmecochorous Helleborus foetidus . Evol Ecol 21, 411–430 (2007). https://doi.org/10.1007/s10682-006-9110-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-006-9110-3

Keywords

Navigation