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Evidence for ecology's role in speciation


A principal challenge in testing the role of natural selection in speciation is to connect the build-up of reproductive isolation between populations to divergence of ecologically important traits1,2. Demonstrations of ‘parallel speciation’, or assortative mating by selective environment, link ecology and isolation3,4,5, but the phenotypic traits mediating isolation have not been confirmed. Here we show that the parallel build-up of mating incompatibilities between stickleback populations can be largely accounted for by assortative mating based on one trait, body size, which evolves predictably according to environment. In addition to documenting the influence of body size on reproductive isolation for stickleback populations spread across the Northern Hemisphere, we have confirmed its importance through a new experimental manipulation. Together, these results suggest that speciation may arise largely as a by-product of ecological differences and divergent selection on a small number of phenotypic traits.

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Figure 1: Mating compatibility (mean proportion of trials involving a nest inspection) for same (black) and different ecotype (grey) combinations, for within region tests (P = 0.0058, paired one-tailed t-test, n = 7 populations) and between region tests (P = 0.0045, n = 9; when the genetic distance measure δµ2 and ecotype match were analysed together, only ecotype was significant: δµ2, P = 0.083; ecotype match, P = 0.0036, one-tailed t-tests, n = 9).
Figure 2: Regression lines for mating compatibility (arcsine square-root-transformed) on absolute mean standard length difference for each female population (Supplementary Information) tested with allopatric male populations.
Figure 3: Mating compatibility versus absolute mean standard length difference between males and females, with female size manipulated.


  1. Nagel, L. & Schluter, D. Body size, natural selection, and speciation in sticklebacks. Evolution 52, 209–218 (1998)

    Article  Google Scholar 

  2. Greenberg, A. J., Moran, J. R., Coyne, J. A. & Wu, C. I. Ecological adaptation during incipient speciation revealed by precise gene replacement. Science 302, 1754–1757 (2003)

    ADS  CAS  Article  Google Scholar 

  3. Schluter, D. & Nagel, L. M. Parallel speciation by natural selection. Am. Nat. 146, 292–301 (1995)

    Article  Google Scholar 

  4. Rundle, H. D., Nagel, L., Boughman, J. & Schluter, D. Natural selection and parallel speciation in sympatric sticklebacks. Science 287, 306–308 (2000)

    ADS  CAS  Article  Google Scholar 

  5. Nosil, P., Crespi, B. J. & Sandoval, C. P. Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature 417, 440–443 (2002)

    ADS  CAS  Article  Google Scholar 

  6. McPhail, J. D. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 399–437 (Oxford Univ. Press, Oxford, 1994)

    Google Scholar 

  7. McKinnon, J. S. & Rundle, H. Speciation in nature: the threespine stickleback model systems. Trends Ecol. Evol. 17, 480–488 (2002)

    Article  Google Scholar 

  8. Hagen, D. W. Isolating mechanisms in threespine sticklebacks (Gasterosteus). J. Fish. Res. B. Can. 24, 1637–1692 (1967)

    ADS  Article  Google Scholar 

  9. Bell, M. A. & Foster, S. A. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 1–27 (Oxford Univ. Press, Oxford, 1994)

    Google Scholar 

  10. Baker, J. A. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 144–187 (Oxford Univ. Press, Oxford, 1994)

    Google Scholar 

  11. Hendry, A. P., Taylor, E. B. & McPhail, J. D. Adaptive divergence and the balance between selection and gene flow: lake and stream stickleback in the Misty system. Evolution 56, 1199–1216 (2002)

    Article  Google Scholar 

  12. Rundle, H. D., Vamosi, S. M. & Schluter, D. Experimental test of predation's effect on divergent selection during character displacement in sticklebacks. Proc. Natl Acad. Sci. USA 100, 14943–14948 (2003)

    ADS  CAS  Article  Google Scholar 

  13. Snyder, R. J. & Dingle, H. Adaptive, genetically based differences in life history between estuary and freshwater threespine sticklebacks (Gasterosteus aculeatus L.). Can. J. Zool. 67, 2448–2454 (1989)

    Article  Google Scholar 

  14. McPhail, J. D. Inherited interpopulation differences in size at first reproduction in threespine stickleback, Gasterosteus aculeatus L. Heredity 38, 53–60 (1977)

    Article  Google Scholar 

  15. Colosimo, P. F. et al. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2, e109 (2004)

    Article  Google Scholar 

  16. Buth, D. G. & Haglund, T. R. in The Evolutionary Biology of the Threespine Stickleback (eds Bell, M. A. & Foster, S. A.) 61–84 (Oxford Univ. Press, Oxford, 1994)

    Google Scholar 

  17. Ortí, G., Bell, M. A., Reimchen, T. E. & Meyer, A. Global survey of mitochondrial DNA sequences in the threespine stickleback: evidence for recent colonizations. Evolution 48, 608–622 (1994)

    Article  Google Scholar 

  18. Bell, M. A. Lateral plate evolution in the threespine stickleback: getting nowhere fast. Genetica 112–113, 445–461 (2001)

    Article  Google Scholar 

  19. Hay, D. E. & McPhail, J. D. Mate selection in three-spine sticklebacks (Gasterosteus). Can. J. Zool. 53, 441–450 (1975)

    Article  Google Scholar 

  20. Ziuganov, V. V. Reproductive isolation among lateral plate phenotypes (low, partial, complete) of the threespine stickleback, Gasterosteus aculeatus, from the White Sea basin and the Kamchatka Peninsula, Russia. Behaviour 132, 1173–1181 (1995)

    Article  Google Scholar 

  21. Rundle, H. D. & Schluter, D. Reinforcement of stickleback mate preferences: sympatry breeds contempt. Evolution 52, 200–208 (1998)

    Article  Google Scholar 

  22. Servedio, M. R. Beyond reinforcement: the evolution of premating isolation by direct selection on preferences and post-mating, prezygotic incompatibilities. Evolution 55, 1909–1920 (2001)

    CAS  Article  Google Scholar 

  23. Boughman, J. W. Divergent sexual selection enhances reproductive isolation in sticklebacks. Nature 411, 944–948 (2001)

    ADS  CAS  Article  Google Scholar 

  24. Ishikawa, M. & Mori, S. Mating success and male courtship behaviors in three populations of the threespine stickleback. Behaviour 137, 1065–1080 (2000)

    Article  Google Scholar 

  25. McKinnon, J. S. Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration. Anim. Behav. 50, 1645–1655 (1995)

    Article  Google Scholar 

  26. Peichel, C. L. et al. The genetic architecture of divergence between threespine stickleback species. Nature 414, 901–905 (2001)

    ADS  CAS  Article  Google Scholar 

  27. Luttberg, B., Towner, M. C., Wandesforde-Smith, A., Mangel, M. & Foster, S. A. State-dependent mate-assessment and mate-selection behavior in female threespine sticklebacks (Gasterosteus aculeatus, Gasterosteiformes: Gasterosteidae). Ethology 107, 545–558 (2001)

    Article  Google Scholar 

  28. Raufaste, N. & Rousset, F. Are partial Mantel tests adequate? Evolution 55, 1703–1705 (2001)

    CAS  Article  Google Scholar 

  29. Mooers, A. Ø., Vamosi, S. M. & Schluter, D. Using phylogenies to test macroevolutionary hypotheses of trait evolution in cranes (Gruinae). Am. Nat. 154, 249–259 (1999)

    Article  Google Scholar 

  30. Hatfield, T. Genetic divergence in adaptive characters between sympatric species of stickleback. Am. Nat. 149, 1009–1029 (1997)

    CAS  Article  Google Scholar 

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We thank L. Bauers, V. Braithwaite, K. Faller, S. Foster, S. Gray, M. Ishikawa, P. Jacobsen, P. Katz, R. King, B. Kristjansson, M. Nemethy, H. Ogawa, W. Paulson, J. Poole, E. Sassman, S. Shell, S. Skulason and R. Snyder for help collecting fish and/or data. M. Blows, H. Rundle and A. Hendry provided useful comments on the manuscript and the University of Queensland hosted J.S.M. during writing. This project was supported by an NSF research grant, REU supplements and a Putnam grant (J.S.M.), the Howard Hughes Medical Institute (D.M.K.) and an NSERC grant (D.S.). Authors' contributions  Stickleback collection was conducted/supervised by J.S.M., S.M. and D.S.; mating trials by J.S.M., J.C. and L.J.; molecular work by B.K.B., L.D. and D.M.K.; and data analyses by J.S.M., D.S. and B.K.B.

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Correspondence to Jeffrey S. McKinnon.

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Supplementary information

Supplementary Information

Includes: 1. supplementary methods, including additional information on collecting, experimental protocols, genetic analyses; 2. supplementary genetic and phylogenetic analyses and associated re-analyses of mating patterns; 3. supplementary tables 1-3 concerning population combinations tested, genetic distances and estimates of divergence times; 4. Supplementary Figure 1, showing unrooted neighbour-joining tree (DOC 108 kb)

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McKinnon, J., Mori, S., Blackman, B. et al. Evidence for ecology's role in speciation. Nature 429, 294–298 (2004).

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