Mutation predicts 40 million years of fly wing evolution

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Abstract

Mutation enables evolution, but the idea that adaptation is also shaped by mutational variation is controversial1,2,3,4. Simple evolutionary hypotheses predict such a relationship if the supply of mutations constrains evolution5,6, but it is not clear that constraints exist, and, even if they do, they may be overcome by long-term natural selection7. Quantification of the relationship between mutation and phenotypic divergence among species will help to resolve these issues. Here we use precise data on over 50,000 Drosophilid fly wings to demonstrate unexpectedly strong positive relationships between variation produced by mutation, standing genetic variation, and the rate of evolution over the last 40 million years. Our results are inconsistent with simple constraint hypotheses because the rate of evolution is very low relative to what both mutational and standing variation could allow. In principle, the constraint hypothesis could be rescued if the vast majority of mutations are so deleterious that they cannot contribute to evolution, but this also requires the implausible assumption that deleterious mutations have the same pattern of effects as potentially advantageous ones. Our evidence for a strong relationship between mutation and divergence in a slowly evolving structure challenges the existing models of mutation in evolution.

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Figure 1: Mean wing shapes of 112 Drosophilid species, plus five outgroup taxa.
Figure 2: Species scores on the two directions in shape phenotype space (canonical variables) that explain the most variance among species means.
Figure 3: Ellipses representing the variation around each landmark.
Figure 4: Relationships between variance in wing shape in M, G and R.

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Acknowledgements

We thank P. Galpern, J. Birdsley, F. S. Hollis, Y. Ng, and L. Carpenter for rearing and imaging Drosophilid species; C. Boake, J. David, G. Gilchrist, J. Hey, A. Hoikalla, L. Reed and J. True for contributing stocks, specimens or images; K. Meyer for assistance with Wombat; S. Steppan for help with r8s and phylogenetic analyses; J. Merilä and M. Kirkpatrick for comments; and to the many students who measured fly wings. This work was supported by US NSF DEB grants 0129219 and 0950002, and NSERC grants to D.H.

Author information

D.H. conceived the project and supervised the gathering of data, K.v.d.L. wrote software and assembled the species dataset, T.F.H., G.H.B. and D.H. derived the major theoretical framework for the analyses, D.H. and G.H.B. analysed the data, and D.H., T.F.H. and G.H.B. wrote the manuscript.

Correspondence to David Houle.

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Reviewer Information Nature thanks J. Cheverud and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Figure 1 Wing landmarks measured and representation of shape changes.

a, Vein model fitted to a D. melanogaster wing. The coordinates of the twelve vein intersections shown are the data for this study. bd, Shape vectors for PC1 of the matrices. b, Mhom matrix. c, G matrix. d, R matrix. Each vector represents a pattern of changes in the locations of landmark intersections, represented by the arrows. The colours represent the pattern of landmark movements as local expansions and contractions that can explain the movements of the landmarks. The scale of local changes is in log2 units, so −1 represents a halving of local area, and +1 a local doubling.

Extended Data Figure 2 Divergence of wing phenotypes as a function of the time since the most common ancestor.

Size divergence (top) is the absolute value of the difference in log-transformed centroid size. Shape divergence (bottom) is measured as Procrustes distance.

Extended Data Figure 3 Relationships between variance in M, G and R in wing size and shape.

a, R and G on Mhom and Mhet. b, R on G. See legend of Fig. 4 for additional explanation.

Extended Data Figure 4 Relationships between conditional variance in M or G and variance at higher levels.

See Legend of Fig. 4 for explanation. Values of the scaling slopes and R2 are given in Extended Data Table 4. a, R and G on Mhom and Mhet for shape. b, R and G on Mhom and Mhet for shape–size. c, R on G for shape. d, R on G for shape–size.

Extended Data Table 1 Taxa included in the species dataset, but not included in ref. 22
Extended Data Table 2 Ratios of evolvabilities of matrix 1 to matrix 2
Extended Data Table 3 Univariate estimates of phylogenetic heritability (H2) for twenty shape traits, plus ln(centroid size)
Extended Data Table 4 Regression of log10 variances in R (per Myr) or G on log10 conditional variances in G or M matrices

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Houle, D., Bolstad, G., van der Linde, K. et al. Mutation predicts 40 million years of fly wing evolution. Nature 548, 447–450 (2017) doi:10.1038/nature23473

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