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Decomposing phenotypic skew and its effects on the predicted response to strong selection

Abstract

The major frameworks for predicting evolutionary change assume that a phenotype’s underlying genetic and environmental components are normally distributed. However, the predictions of these frameworks may no longer hold if distributions are skewed. Despite this, phenotypic skew has never been decomposed, meaning the fundamental assumptions of quantitative genetics remain untested. Here we demonstrate that the substantial phenotypic skew in the body size of juvenile blue tits (Cyanistes caeruleus) is driven by environmental factors. Although skew had little impact on our predictions of selection response in this case, our results highlight the impact of skew on the estimation of inheritance and selection. Specifically, the nonlinear parent–offspring regressions induced by skew, alongside selective disappearance, can strongly bias estimates of heritability. The ubiquity of skew and strong directional selection on juvenile body size imply that heritability is commonly overestimated, which may in part explain the discrepancy between predicted and observed trait evolution.

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Fig. 1: The effects of different distributions of breeding values (G) and environmental values (E) on the distribution of phenotypes (P) and the shape of the PO-regression.
Fig. 2: Skew in the distribution of avian tarsus lengths across different species, measured as the coefficient of skew.
Fig. 3: Decomposition of variance and skew in juvenile body size traits in blue tits.
Fig. 4: Fitness functions and selection gradients for juvenile body size traits based on survival from day 15 to recruitment.
Fig. 5: PO-regressions for four body size traits.

Data and code availability

All data and code can be found at https://doi.org/10.5281/zenodo.6323689.

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Acknowledgements

We thank our many field assistants for help with data collection; S. Nakagawa, A. Moller, D. Santiago-Alarcon, R. Jovani, S. Sales and N. Rodriguez for providing raw data; and E. McFarlane, J. Gauzere and E. Ivimey-Cook for helpful discussions. This work was funded by the Natural Environment Research Council (NE/P000924/1) and a Royal Society Fellowship to J.D.H., and supported by Lord Rosebery and the Dalmeny estate.

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J.L.P. and J.D.H. conceived and designed the project. J.L.P., H.E.L., C.E.T. and J.D.H. generated the data. J.L.P. and J.D.H. analysed the data and wrote the paper. All authors read and approved the paper.

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Correspondence to Joel L. Pick.

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Pick, J.L., Lemon, H.E., Thomson, C.E. et al. Decomposing phenotypic skew and its effects on the predicted response to strong selection. Nat Ecol Evol 6, 774–785 (2022). https://doi.org/10.1038/s41559-022-01694-2

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