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Evidence for ecology's role in speciation

Abstract

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.

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Acknowledgements

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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The authors declare that they have no competing financial interests.

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). https://doi.org/10.1038/nature02556

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