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Evolutionary Ecology

, Volume 33, Issue 5, pp 687–700 | Cite as

Is there spatial variation in phenotypic selection on floral traits in a generalist plant–pollinator system?

  • Alejandra V. González
  • Catalina González-Browne
  • Patricia Salinas
  • Maureen MurúaEmail author
Original Paper

Abstract

The selective role of pollinators on the floral phenotype has been identified as the main force behind angiosperm diversification. However, in generalized plant–pollinator interactions this association may not be that evident, since pollinator assemblages vary in composition among populations, possibly influencing the direction and intensity of floral trait selection. In this study we determine whether there was spatial variation in pollinator assemblages and the selective forces they exert in ten populations of Alstroemeria ligtu var. simsii. We characterized the whole pollinator assemblage in ten populations, quantified four floral attraction traits and determined potential selection targets in each of the study populations. Our results revealed that populations differed in the composition of their pollinator assemblages, and the pollinators with the highest visitation rates also differed among populations. Using phenotypic selection analysis we detected significant differentials and selection gradients only in two of the ten populations, for corolla tube length and ratio of the nectar guide. The spatial variation in selection showed that linear selection acting upon these traits differed significantly among the studied populations. Our study indicates that selection can be detected in generalized plant–pollinator systems and brings new evidence of phenotypic selection variation in space for this endemic plant species. Future studies are needed to determine whether the selective patterns described here are consistent over time and whether they produce evolutionary change in the populations under study.

Keywords

Alstroemeria Chile Floral traits Generalist pollination Phenotypic selection 

Notes

Acknowledgements

We are grateful to L. Contreras, D. Lillo, M. Zuñiga, T. Poch, V. Durán and M.J. Ramírez who assisted us in the fieldwork, and I. Sepulveda who helped in the organization of the data and the construction of Fig. 1. We thank V. Duran for providing photographs. This study was supported by the FONDECYT 11110120 Grant awarded to AG. We are grateful to the Corporación Nacional Forestal (CONAF) and the Jardín Botánico Nacional of Chile for granting permits to work on their lands. The authors declare no conflicts of interest.

Supplementary material

10682_2019_10002_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 20 kb)

References

  1. Aigner PA (2005) Variation in pollination performance gradients in a Dudleya species complex: can generalization promote floral divergence? Funct Ecol 19:681–689CrossRefGoogle Scholar
  2. Alexandersson R, Johnson SD (2002) Pollinator-mediated selection of flower-tube length in a hawkmoth-pollinated Gladiolus (Iridaceae). Proc R Soc Lond B 269:631–636CrossRefGoogle Scholar
  3. Anderson B, Alexandersson R, Johnson SD (2009) Evolution and coexistence of pollination ecotypes in an African Gladiolus (Iridaceae). Evolution 64–4:960–972CrossRefGoogle Scholar
  4. Arroyo KM, Uslar P (1993) Breeding systems in a temperate Mediterranean type climate montane sclerophyllous forest in central Chile. Bot J Linn Soc 111:83–102CrossRefGoogle Scholar
  5. Ashman TL, Majestic C (2006) Genetic constraints on floral evolution: a review and evaluation of patterns. Heredity 96:343–352CrossRefGoogle Scholar
  6. Ashman TL, Morgan MT (2004) Explaining phenotypic selection on plant attractive characters: male function, gender balance or ecological context? Proc R Soc Lond B 271:553–559CrossRefGoogle Scholar
  7. Baeza C, Finot V, Ruiz E, Carrasco P, Novoa P, Stuessy T, González AV (2015) Comparative karyotypic analysis and cytotaxonomy in the Alstroemeria ligtu L. (Alstroemeriaceae) complex of Chile. Braz J Bot.  https://doi.org/10.1007/s40415-015-0220-4 Google Scholar
  8. Botto-Mahan C, Ojeda-Camacho M (2000) The importance of floral damage for pollinator visitation in Alstroemeria ligtu L. Rev Chil Entomol 26:73–76Google Scholar
  9. Botto-Mahan C, Ramírez P, Ossa C, Medel R, Ojeda-Camacho M, González A (2011) Floral herbivory affects female reproductive success and pollinator visitation in the perennial herb Alstroemeria ligtu (Alstroemeriaceae). Int J Plant Sci 172:1130–1136CrossRefGoogle Scholar
  10. Caballero P, Ossa CG, González WL, González-Browne C, Astorga G, Murúa MM, Medel R (2013) Testing non-additive effects of nectar-robbing ants and hummingbird pollination on the reproductive success of a parasitic plant. Plant Ecol 214:633–640CrossRefGoogle Scholar
  11. Caruso CM (2000) Competition for pollination influences selection on floral traits of Ipomopsis aggregata. Evolution 54:1546–1557CrossRefGoogle Scholar
  12. Caruso CM (2001) Differential selection on floral traits of Ipomopsis aggregate growing in contrasting environments. Oikos 94:295–302CrossRefGoogle Scholar
  13. Caruso CM, Peterson B, Ridley C (2003) Natural selection on floral traits of Lobelia (Lobeliaceae): spatial and temporal variation. Am J Bot 90:1333–1340CrossRefGoogle Scholar
  14. Caruso CM, Scott SL, Wray JC, Walsh CA (2010) Pollinators, herbivores, and the maintenance of flower color variation: a case study with Lobelia siphilitica. Evol Ecol 31(2):285–304Google Scholar
  15. Darwin CR (1862) On the various contrivances by which British and foreign orchids are fertilized by insects. John Murray, LondonGoogle Scholar
  16. di Castri F, Hajek ER (1976) Bioclimatología de Chile. Ediciones de la Universidad Católica de Chile, Santiago, p 128Google Scholar
  17. Dodd ME, Silvertown J, Chase MW (1999) Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53:732–744CrossRefGoogle Scholar
  18. Emel SL, Franks SJ, Spigler RB (2017) Phenotypic selection varies with pollination intensity across populations of Sabatia angularis. New Phytol 215:813–824CrossRefGoogle Scholar
  19. Faegri K, van der Pijl L (1979) The principles of pollination ecology. Pergamon Press, OxfordGoogle Scholar
  20. Fenster C, Armbruster W, Wilson P, Dudash M, Thomson J (2004) Pollination syndromes and floral specialization. Ecol Evol Syst 35:375–403CrossRefGoogle Scholar
  21. Fishman L, Wills J (2008) Pollen limitation and natural selection on floral characters in the yellow monkeyflower, Mimulus guttatus. New Phytol 177(3):802–810CrossRefGoogle Scholar
  22. Gervasi DDL, Schiestl FP (2017) Real-time divergent evolution in plants driven by pollinators. Nat Commun 8:14691.  https://doi.org/10.1038/ncomms14691 CrossRefGoogle Scholar
  23. Gómez JM, Bosch J, Perfectti F, Fernández J, Abdelaziz M (2007) Pollinator diversity affects plant reproduction and recruitment: the tradeoffs of generalization. Oecologia 153:597–605CrossRefGoogle Scholar
  24. Gómez JM, Bosch J, Perfectti F, Fernández J, Abdelaziz M, Camacho JPM (2008) Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proc R Soc Lond B 275:2241–2249CrossRefGoogle Scholar
  25. Gómez J, Perfectti F, Bosch J, Camacho J (2009) A geographic selection mosaic in a generalized plant–pollinator–herbivore system. Ecol Monogr 79:245–263CrossRefGoogle Scholar
  26. Gómez JM, Perfectti F, Lorite J (2015) The role of pollinators in floral diversification in a clade of generalist flowers. Evolution 69:863–878CrossRefGoogle Scholar
  27. González AV, Murúa M, Ramírez P (2014) Temporal and spatial variation of the pollinator assemblages in Alstroemeria ligtu (Alstroemeriaceae). Rev Chil Hist Nat 1:5Google Scholar
  28. González A, Murúa M, Pérez F (2015) Floral integration is not explained by pollinator diversity in the generalized plant–pollinator system of Alstroemeria ligtu (Alstroemeriaceae). Evol Ecol 29(1):63–75CrossRefGoogle Scholar
  29. González-Browne C, Murúa MM, Navarro L, Medel R (2016) Does plant origin influence the fitness impact of flower damage? A meta-analysis. PLoS ONE 11(1):e0146437.  https://doi.org/10.1371/journal.pone.0146437 CrossRefGoogle Scholar
  30. Gross K, Sun M, Schiestl FP (2016) Why do floral perfumes become different? Region-specific selection on floral scent in a terrestrial orchid. PLoS ONE 11(2):e0147975.  https://doi.org/10.1371/journal.pone.0147975 CrossRefGoogle Scholar
  31. Hammer O, Harper D, Ryan P (2001) PAST: paleontological statistics software for education and data analysis. Paleontol Electrón 4:1–9Google Scholar
  32. Hersch EI, Roy BA (2007) Context-dependent pollinator behavior: an explanation for patterns of hybridization among three species of Indian paintbrush. Evolution 61:111–124CrossRefGoogle Scholar
  33. Irwin RE, Bronstein JL, Manson JS, Richardson L (2010) Nectar robbing: ecological and evolutionary perspectives. Annu Rev Ecol Evol Syst 41:271–292CrossRefGoogle Scholar
  34. Johnson SD, Steiner KE (1997) Long-tongued fly pollination and evolution of floral spur length in the Disa draconis complex (Orchidaceae). Evolution 51:45–53CrossRefGoogle Scholar
  35. Kay K, Sargent R (2009) The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Ecol Evol Syst 40:637–656CrossRefGoogle Scholar
  36. Knauer AC, Schiestl FP (2015) Bees use honest floral signals as indicators of reward when visiting flowers. Ecol Lett 18(2):135–143CrossRefGoogle Scholar
  37. Krupnick GA, Weis AE (1999) The effect of floral herbivory on male and female reproductive success in Isomeris arborea. Ecology 80(1):135–149CrossRefGoogle Scholar
  38. Lillo D (2014) Spatial variation in the pollen limitation of Alstroemeria ligtu var. simsii. Bs. Thesis, Universidad de Chile, Santiago, ChileGoogle Scholar
  39. McCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365CrossRefGoogle Scholar
  40. Medel R, Botto-Mahan C, Kalin-Arroyo M (2003) Pollinator- mediated selection on the nectar guide phenotype in the Andean monkey flower, Mimulus luteus. Ecology 84:1721–1732CrossRefGoogle Scholar
  41. Medel R, González-Browne C, Salazar D, Ferrer P, Ehrenfeld M (2018) The most effective pollinator principle applies to new invasive pollinators. Biol Lett 14:20180132.  https://doi.org/10.1098/rsbl.2018.0132 CrossRefGoogle Scholar
  42. Morrissey MB, Sakrejda K (2013) Unification of regression-based methods for the analysis of natural selection. Evolution 67:2094–2100CrossRefGoogle Scholar
  43. Muñoz M, Moreira MA (2003) Alstroemerias de Chile; diversidad, distribución y conservación. Taller la Era, SantiagoGoogle Scholar
  44. Murúa M, Ramírez MJ, González A (2019) Is the same pollinator species equally effective in different populations of the generalist herb Alstroemeria ligtu var. simsii? Gayana Bot 76(1):109–114CrossRefGoogle Scholar
  45. Navas LE (1973) Flora de la cuenca de Santiago de Chile. Ediciones de la Universidad de Chile, SantiagoGoogle Scholar
  46. Ne’eman G, Jürgens A, Newstrom-Lloyd L, Potts SG, Dafni A (2010) A framework for comparing pollinator performance: effectiveness and efficiency. Biol Rev 85:435–451Google Scholar
  47. Nilsson LA (1988) The evolution of flowers with deep corolla tubes. Nature 334:147–149CrossRefGoogle Scholar
  48. Pohl N, Carvallo G, Botto-Mahan C, Medel R (2006) Nonadditive effects of flower damage and hummingbird pollination on the fecundity of Mimulus luteus. Oecologia 149:648–655CrossRefGoogle Scholar
  49. R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 23 June 2019
  50. Rice W (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  51. Santangelo JS, Thompson KA, Johnson MTJ (2019) Herbivores and plant defences affect selection on plant reproductive traits more strongly than pollinators. J Evol Biol 32(1):4–18CrossRefGoogle Scholar
  52. Schaefer H, Schaefer V, Levey D (2004) How plant–animal interactions signal new insights in communication. TREE 19:577–584Google Scholar
  53. Sekor MR, Franks SJ (2018) An experimentally introduced population of Brassica rapa (Brassicaceae). 1. Phenotypic selection over three years following colonization of a novel environment. Plant Ecol Evol 151(2):209–218CrossRefGoogle Scholar
  54. Souto-Vilarós D, Vuleta A, Manitašević Jovanović S, Budečević S, Wang H, Sapir Y, Imbert E (2018) Are pollinators the agents of selection on flower colour and size in irises? Oikos 127(3):834–846CrossRefGoogle Scholar
  55. Totland Ø (2001) Environment-dependent pollen limitation and selection on floral traits in an Alpine species. Ecology 82(8):2233–2244CrossRefGoogle Scholar
  56. Zhao Z-G, Wang Y-K (2015) Selection by pollinators on floral traits in generalized Trollius ranunculoides (Ranunculaceae) along altitudinal gradients. PLoS ONE 10(2):e0118299.  https://doi.org/10.1371/journal.pone.0118299 CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Alejandra V. González
    • 1
  • Catalina González-Browne
    • 1
  • Patricia Salinas
    • 1
  • Maureen Murúa
    • 2
    • 3
    Email author
  1. 1.Departamento de Ciencias Ecológicas, Facultad de CienciasUniversidad de ChileSantiagoChile
  2. 2.Centro GEMA-Genómica, Ecología y Medio Ambiente, Facultad de CienciasUniversidad MayorSantiagoChile
  3. 3.Fundación FloresProvidencia, SantiagoChile

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