Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations

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Abstract

Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change—heritability and selection—are both affected by the same environmental variable. To determine how general such an environmentally induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible, open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.

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Fig. 1: Heritability as a function of the standardized selection gradient.
Fig. 2: Meta-analysis on the heritability–selection correlation coefficients.
Fig. 3: No effect of a correlation between heritability and selection on differences in selection response.

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Acknowledgements

We are grateful to all the original data owners who found time in their tight schedules to reply to our e-mails, or who otherwise contributed to the discussion (including people whose data we did not end up using for our analyses). Specifically, we thank—in no particular order—B. Sheldon, A. Husby, E. Postma, B. Schloegl, K. Foerster, J. Fargallo, J. Brommer, B. Class, A. Møller, G. Ljüngstrom, S. Blanchet, N. Wheelwright, M. Nicolaus, N. Dingemanse, S. Sakaluk, A. Wilson, J. Hadfield, J. Hubbard, J. Reid, P. Arcese, E. Huchard, T. Clutton-Brock, J. Pemberton, S. Johnston, T. Bonnet and B. Delahaie. S. Nakagawa kindly advised us on the meta-analysis. T. Reed and A. Husby provided useful comments on the manuscript. This work was funded in part by NIOO Strategic funds (SM1521) and an ERC Advanced Grant (339092 - E-Response) to M.E.V.

Author information

All authors contributed to the design of the study. A.C. and J.J.C.R. retrieved the datasets. J.J.C.R. and P.G. designed the analysis protocol, with assistance from A.C. in the meta-analysis. J.J.C.R. screened the retrieved datasets, contacted the original authors, conducted the analyses and drafted the paper. All authors commented on the manuscript.

Correspondence to Jip J. C. Ramakers.

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Supplementary information

Supplementary Information

Supplementary Methods, Supplementary Figures 1–3

Reporting Summary

Supplementary Data

Supplementary Table 1.1 (All datasets initially retrieved and considered for analysis); Supplementary Table 1.2 (Repositories associated with each dataset in Supplementary Table 1.1); Supplementary Table 2 (Data necessary to reproduce the heritability — selection regressions in Fig 1 and to calculate expected response to selection); Supplementary Table 3 (Data necessary to replicate the meta-analysis on the correlation coefficient of the relationship between heritability and selection).

Supplementary Code

R code examples for each analysis.

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Ramakers, J.J.C., Culina, A., Visser, M.E. et al. Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations. Nat Ecol Evol 2, 1093–1103 (2018) doi:10.1038/s41559-018-0577-4

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