Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Frugivory-related traits promote speciation of tropical palms

Nature Ecology & Evolution volume 1, pages 1903–1911 (2017)Cite this article

Subjects

Abstract

Animal-mediated seed dispersal by frugivorous birds and mammals is central to the ecology and functioning of ecosystems, but whether and how frugivory-related traits have affected plant speciation remains little explored. Fruit size is directly linked to plant dispersal capacity and therefore influences gene flow and genetic divergence of plant populations. Using a global species-level phylogeny with comprehensive data on fruit sizes and plant species distributions, we test whether fruit size has affected speciation rates of palms (Arecaceae), a plant family characteristic of tropical rainforests. Globally, the results reveal that palms with small fruit sizes have increased speciation rates compared with those with large (megafaunal) fruits. Speciation of small-fruited palms is particularly high in the understory of tropical rainforests in the New World, and on islands in the Old World. This suggests that frugivory-related traits in combination with geography and the movement behaviour of frugivores can influence the speciation of fleshy-fruited plants.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Global variation in palm fruit size.
Fig. 2: Speciation rate estimates for palm lineages with small (<4 cm) and large (≥4 cm) fruits.
Fig. 3: Understory habitat and its effect on speciation rates for palm lineages with small (<4 cm) fruits.
Fig. 4: Island colonization and its effect on speciation rates for palm lineages with small (<4 cm) fruits.

Similar content being viewed by others

References

  1. Kissling, W. D., Böhning–Gaese, K. & Jetz, W. The global distribution of frugivory in birds. Glob. Ecol. Biogeogr. 18, 150–162 (2009).

    Article  Google Scholar 

  2. Fleming, T. H. & Kress, W. J. The Ornaments of Life: Coevolution and Conservation in the Tropics (Chicago Univ. Press, Chicago, 2013).

  3. Nathan, R. & Muller-Landau, H. C. Spatial patterns of seed dispersal, their determinants and consequences for recruitment. Trends Ecol. Evol. 15, 278–285 (2000).

    Article  CAS  Google Scholar 

  4. Givnish, T. J. Ecology of plant speciation. Taxon 59, 1326–1366 (2010).

    Article  Google Scholar 

  5. Kissling, W. D. Has frugivory influenced the macroecology and diversification of a tropical keystone plant family? Res. Ideas Outcomes 3, e14944 (2017).

    Article  Google Scholar 

  6. Lord, J. M. Frugivore gape size and the evolution of fruit size and shape in Southern Hemisphere floras. Austral Ecol. 29, 430–436 (2004).

    Article  Google Scholar 

  7. Jordano, P. in Seeds: The Ecology of Regeneration in Plant Communities 2nd edn (ed. Fenner, M.) 125–166 (CABI, Wallingford, 2000).

  8. Guimarães, P. R. Jr, Galetti, M. & Jordano, P. Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE 3, e1745 (2008).

    Article  Google Scholar 

  9. Janzen, D. H. & Martin, P. S. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215, 19–27 (1982).

    Article  CAS  Google Scholar 

  10. Haskell, J. P., Ritchie, M. E. & Olff, H. Fractal geometry predicts varying body size scaling relationships for mammal and bird home ranges. Nature 418, 527–530 (2002).

    Article  CAS  Google Scholar 

  11. Milton, K. & May, M. L. Body weight, diet and home range area in primates. Nature 259, 459–462 (1976).

    Article  CAS  Google Scholar 

  12. Shanahan, M., Harrison, R. D., Yamuna, R., Boen, W. & Thornton, I. W. B. Colonization of an island volcano, Long Island, Papua New Guinea, and an emergent island, Motmot, in its caldera lake. V. Colonization by figs (Ficus spp.), their dispersers and pollinators. J. Biogeogr. 28, 1365–1377 (2001).

    Article  Google Scholar 

  13. Burney, C. W. & Brumfield, R. T. Ecology predicts levels of genetic differentiation in neotropical birds. Am. Nat. 174, 358–368 (2009).

    Article  Google Scholar 

  14. Salisbury, C. L., Seddon, N., Cooney, C. R. & Tobias, J. A. The latitudinal gradient in dispersal constraints: ecological specialisation drives diversification in tropical birds. Ecol. Lett. 15, 847–855 (2012).

    Article  Google Scholar 

  15. Karr, J. R. Geographical variation in the avifaunas of tropical forest undergrowth. Auk 97, 283–298 (1980).

    Google Scholar 

  16. Smith, J. F. High species diversity in fleshy-fruited tropical understory plants. Am. Nat. 157, 646–653 (2001).

    Article  CAS  Google Scholar 

  17. Holbrook, K. M., Smith, T. B. & Hardesty, B. D. Implications of long-distance movements of frugivorous rain forest hornbills. Ecography 25, 745–749 (2002).

    Article  Google Scholar 

  18. Losos, J. B. & Ricklefs, R. E. Adaptation and diversification on islands. Nature 457, 830–836 (2009).

    Article  CAS  Google Scholar 

  19. Dransfield, J. et al. Genera Palmarum: The Evolution and Classification of Palms (Kew Publishing, Kew, 2008).

  20. Couvreur, T. L. P., Forest, F. & Baker, W. J. Origin and global diversification patterns of tropical rain forests: inferences from a complete genus-level phylogeny of palms. BMC Biol. 9, 44 (2011).

    Article  Google Scholar 

  21. Zona, S. & Henderson, A. A review of animal-mediated seed dispersal of palms. Selbyana 11, 6–21 (1989).

    Google Scholar 

  22. Faurby, S., Eiserhardt, W. L., Baker, W. J. & Svenning, J.-C. An all-evidence species-level supertree for the palms (Arecaceae). Mol. Phylogenet. Evol. 100, 57–69 (2016).

    Article  Google Scholar 

  23. Brummitt, R. K., Pando, F., Hollis, S. & Brummitt, N. World Geographical Scheme for Recording Plant Distributions (International Working Group on Taxonomic Databases for Plant Sciences (TDWG), Kew, 2001).

  24. FitzJohn, R. G., Maddison, W. P. & Otto, S. P. Estimating trait-dependent speciation and extinction rates from incompletely resolved phylogenies. Syst. Biol. 58, 595–611 (2009).

    Article  Google Scholar 

  25. FitzJohn, R. G. Diversitree: comparative phylogenetic analyses of diversification in R. Methods Ecol. Evol. 3, 1084–1092 (2012).

    Article  Google Scholar 

  26. Richardson, J. E. & Pennington, R. T. Editorial: Origin of tropical diversity: from clades to communities. Front. Genet. 7, 186 (2016).

    Article  Google Scholar 

  27. Jordano, P., García, C., Godoy, J. A. & García-Castaño, J. L. Differential contribution of frugivores to complex seed dispersal patterns. Proc. Natl Acad. Sci. USA 104, 3278–3282 (2007).

    Article  CAS  Google Scholar 

  28. Lenz, J. et al. Seed-dispersal distributions by trumpeter hornbills in fragmented landscapes. Proc. R. Soc. B 278, 2257–2264 (2011).

    Article  Google Scholar 

  29. Galetti, M. et al. Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340, 1086–1090 (2013).

    Article  CAS  Google Scholar 

  30. Baker, W. J. & Couvreur, T. L. P. Global biogeography and diversification of palms sheds light on the evolution of tropical lineages. II Diversification history and origin of regional assemblages. J. Biogeogr. 40, 286–298 (2013).

    Article  Google Scholar 

  31. Moore, R. P., Robinson, W. D., Lovette, I. J. & Robinson, T. R. Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol. Lett. 11, 960–968 (2008).

    Article  CAS  Google Scholar 

  32. Corlett, R. T. Frugivory and seed dispersal by vertebrates in tropical and subtropical Asia: an update. Glob. Ecol. Conserv. 11, 1–22 (2017).

    Article  Google Scholar 

  33. Fleming, T. H., Breitwisch, R. & Whitesides, G. H. Patterns of tropical vertebrate frugivore diversity. Annu. Rev. Ecol. Syst. 18, 91–109 (1987).

    Article  Google Scholar 

  34. Banin, L. et al. What controls tropical forest architecture? Testing environmental, structural and floristic drivers. Glob. Ecol. Biogeogr. 21, 1179–1190 (2012).

    Article  Google Scholar 

  35. Kissling, W. D. et al. Cenozoic imprints on the phylogenetic structure of palm species assemblages worldwide. Proc. Natl Acad. Sci. USA 109, 7379–7384 (2012).

    Article  CAS  Google Scholar 

  36. Baker, W. J. & Couvreur, T. L. P. in Biotic Evolution and Environmental Cchange in Southeast Asia (eds Gower, D. et al.) 164–190 (Cambridge University Press, Cambridge 2012).

  37. Bacon, C. D., Baker, W. J. & Simmons, M. P. Miocene dispersal drives island radiations in the palm tribe Trachycarpeae (Arecaceae). Syst. Biol. 61, 426–442 (2012).

    Article  Google Scholar 

  38. Diamond, J. M., Gilpin, M. E. & Mayr, E. Species-distance relation for birds of the Solomon Archipelago, and the paradox of the great speciators. Proc. Natl Acad. Sci. USA 73, 2160–2164 (1976).

    Article  CAS  Google Scholar 

  39. Hughes, C. & Eastwood, R. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proc. Natl Acad. Sci. USA 103, 10334–10339 (2006).

    Article  CAS  Google Scholar 

  40. Kissling, W. D. et al. Quaternary and pre-Quaternary historical legacies in the global distribution of a major tropical plant lineage. Glob. Ecol. Biogeogr. 21, 909–921 (2012).

    Article  Google Scholar 

  41. Morici, C. in Ecologia Insular (eds Fernandez-Palacios, J. M. & Morici, C.) 81–122 (Asociacion Española de Ecología Terrestre, Badajoz, 2004).

  42. Sanín, M. J. et al. The Neogene rise of the tropical Andes facilitated diversification of wax palms (Ceroxylon: Arecaceae) through geographical colonization and climatic niche separation. Bot. J. Linn. Soc. 182, 303–317 (2016).

    Article  Google Scholar 

  43. Svenning, J.-C. On the role of microenvironmental heterogeneity in the ecology and diversification of neotropical rain-forest palms (Arecaceae). Bot. Rev. 67, 1–53 (2001).

    Article  Google Scholar 

  44. Eiserhardt, W. L., Svenning, J.-C., Kissling, W. D. & Balslev, H. Geographical ecology of the palms (Arecaceae): determinants of diversity and distributions across spatial scales. Ann. Bot. 108, 1391–1416 (2011).

    Article  Google Scholar 

  45. Herrera, C. M. Interspecific variation in fruit shape: allometry, phylogeny, and adaptation to dispersal agents. Ecology 73, 1832–1841 (1992).

    Article  Google Scholar 

  46. Lomáscolo, S. B., Levey, D. J., Kimball, R. T., Bolker, B. M. & Alborn, H. T. Dispersers shape fruit diversity in Ficus (Moraceae). Proc. Natl Acad. Sci. USA 107, 14668–14672 (2010).

    Article  Google Scholar 

  47. Voigt, F. A. et al. A comparison of morphological and chemical fruit traits between two sites with different frugivore assemblages. Oecologia 141, 94–104 (2004).

    Article  CAS  Google Scholar 

  48. Dominy, N. J., Svenning, J. C. & Li, W. H. Historical contingency in the evolution of primate color vision. J. Hum. Evol. 44, 25–45 (2003).

    Article  Google Scholar 

  49. Ricklefs, R. E. & Renner, S. S. Species richness within families of flowering plants. Evolution 48, 1619–1636 (1994).

    Article  Google Scholar 

  50. Onstein, R. E. & Linder, H. P. Beyond climate: convergence in fast evolving sclerophylls in Cape and Australian Rhamnaceae predates the Mediterranean climate. J. Ecol. 104, 665–677 (2016).

    Article  Google Scholar 

  51. Baker, W. J. et al. Complete generic-level phylogenetic analyses of palms (Arecaceae) with comparisons of supertree and supermatrix approaches. Syst. Biol. 58, 240–256 (2009).

    Article  Google Scholar 

  52. Govaerts, R. & Dransfield, J. World Checklist of Palms (Royal Botanic Gardens Kew, 2005).

  53. Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008).

    PubMed  Google Scholar 

  54. Weigelt, P., Jetz, W. & Kreft, H. Bioclimatic and physical characterization of the world’s islands. Proc. Natl Acad. Sci. USA 110, 15307–15312 (2013).

    Article  CAS  Google Scholar 

  55. Maddison, W. P., Midford, P. E. & Otto, S. P. Estimating a binary character’s effect on speciation and extinction. Syst. Biol. 56, 701–710 (2007).

    Article  Google Scholar 

  56. Rabosky, D. L. & Goldberg, E. E. Model inadequacy and mistaken inferences of trait-dependent speciation. Syst. Biol. 64, 340–355 (2015).

    Article  CAS  Google Scholar 

  57. Maddison, W. P. & FitzJohn, R. G. The unsolved challenge to phylogenetic correlation tests for categorical characters. Syst. Biol. 64, 127–136 (2015).

    Article  Google Scholar 

  58. Davis, M. P., Midford, P. E. & Maddison, W. Exploring power and parameter estimation of the BiSSE method for analyzing species diversification. BMC Evol. Biol. 13, 1–11 (2013).

    Article  Google Scholar 

  59. R Development Core Team R: A Language and Environment for Statistical Computing, Version 3.1.0 (R Foundation for Statistical Computing, Vienna, 2014); http://www.R-project.org

  60. Bruggeman, J., Heringa, J. & Brandt, B. W. PhyloPars: estimation of missing parameter values using phylogeny. Nucleic Acids Res. 37, W179–W184 (2009).

    Article  CAS  Google Scholar 

  61. Baker, W. J. & Couvreur, T. L. P. Global biogeography and diversification of palms sheds light on the evolution of tropical lineages. I. Historical biogeography. J. Biogeogr. 40, 274–285 (2013).

    Article  Google Scholar 

  62. FitzJohn, R. G. Quantitative traits and diversification. Syst. Biol. 59, 619–633 (2010).

    Article  Google Scholar 

  63. Rabosky, D. L. Automatic detection of key innovations, rate shifts, and diversity-dependence on phylogenetic trees. PLoS ONE 9, e89543 (2014).

    Article  Google Scholar 

  64. Rabosky, D. L. & Huang, H. A robust semi-parametric test for detecting trait-dependent diversification. Syst. Biol. 65, 181–193 (2016).

    Article  Google Scholar 

Download references

Acknowledgements

We thank H. Balslev, A. Barfod, A. Blach-Overgaard, F. Borchsenius, J. Dransfield, W. Eiserhardt and M. J. Sanín for discussions about palm biology and J. Dransfield,A. Barfod and A. J. Henderson for the use of pictures for Fig. 1. We thank J. Ollerton for constructive comments on an earlier version of the manuscript. W.D.K. was supported by the University of Amsterdam (starting grant), the Danish Council for Independent Research–Natural Sciences (grant 11-106163) and the Netherlands Organisation for Scientific Research (grant 824.15.007). W.J.B. was supported by a grant from the Garfield Weston Foundation to the Global Tree Seed Bank Project at the Royal Botanic Gardens, Kew. J.C.S. was supported by the European Research Council (ERC-2012-StG-310886-HISTFUNC), and also considers this work a contribution to his VILLUM Investigator project 'Biodiversity Dynamics in a Changing World' funded by VILLUM FONDEN.

Author information

Authors and Affiliations

  1. Institute for Biodiversity and Ecosystem Dynamics (IBED), University of Amsterdam, PO Box 94248, Amsterdam, 1090 GE, The Netherlands

    Renske E. Onstein & W. Daniel Kissling

  2. Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, UK

    William J. Baker

  3. IRD, DIADE, Univ Montpellier, Montpellier, 34394, France

    Thomas L. P. Couvreur

  4. Department of Biological and Environmental Sciences, University of Gothenburg, Box 461, SE 405 30, Göteborg, Sweden

    Søren Faurby

  5. Gothenburg Global Biodiversity Centre, Box 461, SE 405 30, Göteborg, Sweden

    Søren Faurby

  6. Section for Ecoinformatics and Biodiversity, Department of Bioscience, Aarhus University, Ny Munkegade 114, Aarhus C, DK-8000, Denmark

    Jens-Christian Svenning

Authors
  1. Renske E. Onstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. William J. Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas L. P. Couvreur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Søren Faurby
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jens-Christian Svenning
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. W. Daniel Kissling
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

W.D.K. conceived the idea; W.D.K. and R.E.O. designed the study; W.D.K. and R.E.O. collected data; R.E.O. analysed the data; R.E.O. and W.D.K. wrote the manuscript; all authors discussed the results and commented on the manuscript.

Corresponding authors

Correspondence to Renske E. Onstein or W. Daniel Kissling.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Supplementary Information

Supplementary notes, figures, tables, data sources and references

Life sciences reporting summary

Supplementary Table 1

Summary statistics of fruit sizes for each palm genus

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Onstein, R.E., Baker, W.J., Couvreur, T.L.P. et al. Frugivory-related traits promote speciation of tropical palms. Nat Ecol Evol 1, 1903–1911 (2017). https://doi.org/10.1038/s41559-017-0348-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-017-0348-7

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing