Immigration history controls diversification in experimental adaptive radiation

Abstract

Diversity in biological communities is a historical product of immigration, diversification and extinction1,2,3,4, but the combined effect of these processes is poorly understood. Here we show that the order and timing of immigration controls the extent of diversification. When an ancestral bacterial genotype was introduced into a spatially structured habitat, it rapidly diversified into multiple niche-specialist types5. However, diversification was suppressed when a niche-specialist type was introduced before, or shortly after, introduction of the ancestral genotype. In contrast, little suppression occurred when the same niche specialist was introduced relatively late. The negative impact of early arriving immigrants was attributable to the historically sensitive outcome of interactions involving neutral competition3 and indirect facilitation. Ultimately, the entire boom-and-bust dynamics of adaptive radiation were altered. These results demonstrate that immigration and diversification are tightly linked processes, with small differences in immigration history greatly affecting the evolutionary emergence of diversity.

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Figure 1: Diversification of the ancestral SM genotype in spatially structured microcosms.
Figure 2: Effects of immigration history.
Figure 3: Long-term changes in diversity.
Figure 4: Effect of the founding density of WS genotypes on the outcome of competition.

References

  1. 1

    Ricklefs, R. E. & Schluter, D. .Species Diversity in Ecological Communities: Historical and Geographical Perspectives (Univ. Chicago Press, Chicago, 1993)

    Google Scholar 

  2. 2

    Losos, J. B. & Schluter, D. Analysis of an evolutionary species-area relationship. Nature 408, 847–850 (2000)

    ADS  CAS  Article  Google Scholar 

  3. 3

    Hubbell, S. P. The Unified Neutral Theory of Biodiversity and Biogeography (Princeton Univ. Press, Princeton, 2001)

    Google Scholar 

  4. 4

    Gillespie, R. G. Community assembly through adaptive radiation in Hawaiian spiders. Science 303, 356–359 (2004)

    ADS  CAS  Article  Google Scholar 

  5. 5

    Rainey, P. B. & Travisano, M. Adaptive radiation in a heterogeneous environment. Nature 394, 69–72 (1998)

    ADS  CAS  Article  Google Scholar 

  6. 6

    MacArthur, R. H. & Wilson, E. O. The Theory of Island Biogeography (Princeton Univ. Press, Princeton, 1967)

    Google Scholar 

  7. 7

    Connor, E. F. & McCoy, E. D. The statistics and biology of the species-area relationship. Am. Nat. 113, 791–833 (1979)

    MathSciNet  Article  Google Scholar 

  8. 8

    Drake, J. A. Community-assembly mechanics and the structure of an experimental species ensemble. Am. Nat. 137, 1–26 (1991)

    Article  Google Scholar 

  9. 9

    Weiher, E. & Keddy, P. A. Ecological Assembly Rules: Perspectives, Advances, Retreats (Cambridge Univ. Press, Cambridge, 1999)

    Google Scholar 

  10. 10

    Chase, J. M. Community assembly: when should history matter?. Oecologia 136, 489–498 (2003)

    ADS  Article  Google Scholar 

  11. 11

    Fukami, T. & Morin, P. J. Productivity-biodiversity relationships depend on the history of community assembly. Nature 424, 423–426 (2003)

    ADS  CAS  Article  Google Scholar 

  12. 12

    Emerson, B. C. & Kolm, N. Species diversity can drive speciation. Nature 434, 1015–1017 (2005)

    ADS  CAS  Article  Google Scholar 

  13. 13

    Travisano, M., Mongold, J. A., Bennett, A. F. & Lenski, R. E. Experimental tests of the roles of adaptation, chance, and history in evolution. Science 267, 87–90 (1995)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Losos, J. B., Jackman, T. R., Larson, A., de Queiroz, K. & Rodriguez-Schettino, L. Contingency and determinism in replicated adaptive radiations of island lizards. Science 279, 2115–2118 (1998)

    ADS  CAS  Article  Google Scholar 

  15. 15

    Taylor, E. B. & McPhail, J. D. Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus.. Proc. R. Soc. B 267, 2375–2384 (2000)

    CAS  Article  Google Scholar 

  16. 16

    Schluter, D. The Ecology of Adaptive Radiation (Oxford Univ. Press, Oxford, 2000)

    Google Scholar 

  17. 17

    Gillespie, R. G., Palumbi, S. R. & Croom, H. B. Multiple origins of a spider radiation in Hawaii. Proc. Natl Acad. Sci. USA 91, 2290–2294 (1994)

    ADS  CAS  Article  Google Scholar 

  18. 18

    Emerson, B. C. Evolution on oceanic islands: molecular phylogenetic approaches to understanding pattern and process. Mol. Ecol. 11, 951–966 (2002)

    CAS  Article  Google Scholar 

  19. 19

    Webb, C. O., Ackerly, D. D., McPeeck, M. A. & Donoghue, M. J. Phylogenies and community ecology. Annu. Rev. Ecol. Syst. 33, 475–505 (2002)

    Article  Google Scholar 

  20. 20

    Emerson, B. C. & Oromí, P. Diversification of the forest beetle genus Tarphius in the Canary Islands, and the evolutionary origins of island endemics. Evolution 59, 586–598 (2005)

    PubMed  PubMed Central  Google Scholar 

  21. 21

    Losos, J. B. & Glor, R. E. Phylogenetic comparative methods and the geography of speciation. Trends Ecol. Evol. 18, 220–227 (2003)

    Article  Google Scholar 

  22. 22

    Kassen, R., Llewellyn, M. & Rainey, P. B. Ecological constraints on diversification in a model adaptive radiation. Nature 451, 984–988 (2004)

    ADS  Article  Google Scholar 

  23. 23

    Rainey, P. B. in The Influence of Cooperative Bacteria on Animal Host Biology (eds McFall-Ngai, M. J., Henderson, B. & Ruby, E. G.) 83–100 (Cambridge Univ. Press, Cambridge, 2005)

    Google Scholar 

  24. 24

    Goymer, P. et al. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 173, 515–526 (2006)

    CAS  Article  Google Scholar 

  25. 25

    Doebeli, M. & Dieckmann, U. Speciation along environmental gradients. Nature 421, 259–264 (2003)

    ADS  CAS  Article  Google Scholar 

  26. 26

    Gavrilets, S. & Vose, A. Dynamic patterns of adaptive radiation. Proc. Natl Acad. Sci. USA 102, 18040–18045 (2005)

    ADS  CAS  Article  Google Scholar 

  27. 27

    Seehausen, O. African cichlid fish: a model system in adaptive radiation research. Proc. R. Soc. Lond. B 273, 1987–1998 (2006)

    Article  Google Scholar 

  28. 28

    Cowie, R. H. Variation in species diversity and shell shape in Hawaiian land snails: in situ speciation and ecological relationships. Evolution 49, 1191–1202 (1995)

    Article  Google Scholar 

  29. 29

    Fukami, T., Bezemer, T. M., Mortimer, S. R. & Van der Putten, W. H. Species divergence and trait convergence in experimental plant community assembly. Ecol. Lett. 8, 1283–1290 (2005)

    Article  Google Scholar 

  30. 30

    Rainey, P. B. Adaptation of Pseudomonas fluorescens to the plant rhizosphere. Environ. Microbiol. 1, 243–257 (1999)

    CAS  Article  Google Scholar 

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Acknowledgements

We thank P. Meintjes for assistance, and B. Emerson, R. Kassen and the members of the Rainey laboratory for comments. This work was supported by the Marsden Fund Council from government funding administered by the Royal Society of New Zealand, and by the Japan Society for the Promotion of Science.

Author Contributions T.F. developed the concepts, designed the main experiment with P.B.R., collected and analysed the primary data, and wrote the manuscript in conjunction with P.B.R. and H.J.E.B. H.J.E.B. and P.B.R. conceptualized the SMmsc genotype, which was constructed and validated by H.J.E.B. X.-X.Z. designed, constructed and validated lacZ-marked SBW25. H.J.E.B. and T.F. performed selection experiments.

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Correspondence to Tadashi Fukami.

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Supplementary Information

This file contains Supplementary Discussion 1 and 2 and Supplementary Figures 1-2. Supplementary Discussion 1 explains why the boom-and-bust dynamics have parallels with similar dynamics observed in macro-organisms. Supplementary Discussion 2 provides further detail on the results of the experiments that used SMmsc. Supplementary Figure 1 shows the relationship between relative immigration timing and population size and initial population growth rate. Supplementary Figure 2 shows detection of SMmsc-derived WS genotypes in microcosms in which diversification was suppressed by early introduction of small-WS. (PDF 315 kb)

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Fukami, T., Beaumont, H., Zhang, X. et al. Immigration history controls diversification in experimental adaptive radiation. Nature 446, 436–439 (2007). https://doi.org/10.1038/nature05629

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