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Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions

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Abstract

There are now thousands of estimates of phenotypic selection in natural populations, resulting in multiple synthetic reviews of these data. Here we consider several major lessons and limitations emerging from these syntheses, and how they may guide future studies of selection in the wild. First, we review past analyses of the patterns of directional selection. We present new meta-analyses that confirm differences in the direction and magnitude of selection for different types of traits and fitness components. Second, we describe patterns of temporal and spatial variation in directional selection, and their implications for cumulative selection and directional evolution. Meta-analyses suggest that sampling error contributes importantly to observed temporal variation in selection, and indicate that evidence for frequent temporal changes in the direction of selection in natural populations is limited. Third, we review the apparent lack of evidence for widespread stabilizing selection, and discuss biological and methodological explanations for this pattern. Finally, we describe how sampling error, statistical biases, choice of traits, fitness measures and selection metrics, environmental covariance and other factors may limit the inferences we can draw from analyses of selection coefficients. Current standardized selection metrics based on simple parametric statistical models may be inadequate for understanding patterns of non-linear selection and complex fitness surfaces. We highlight three promising areas for expanding our understanding of selection in the wild: (1) field studies of stabilizing selection, selection on physiological and behavioral traits, and the ecological causes of selection; (2) new statistical models and methods that connect phenotypic variation to population demography and selection; and (3) availability of the underlying individual-level data sets from past and future selection studies, which will allow comprehensive modeling of selection and fitness variation within and across systems, rather than meta-analyses of standardized selection metrics.

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Acknowledgments

We thank Andrew Hendry, Ryan Martin, Michael Morrissey and two anonymous reviewers for useful suggestions on earlier versions of the manuscript. We thank Jarrod Hadfield for identifying problems and suggesting solutions to an earlier version of the meta-analyses. The Whiteley Center provided an ideal venue for analysis and the initial writing for JGK. Research supported in part by NSF grant IOS-1120500 to JGK.

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Authors and Affiliations

  1. Department of Biology, University of North Carolina, Chapel Hill, NC, 27516, USA

    Joel G. Kingsolver

  2. Department of Biology, North Carolina State University, Raleigh, NC, 27695, USA

    Sarah E. Diamond

  3. Department of Biology, University of San Diego, San Diego, CA, 92110, USA

    Adam M. Siepielski

  4. Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA, 94720, USA

    Stephanie M. Carlson

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  1. Joel G. Kingsolver
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  2. Sarah E. Diamond
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Correspondence to Joel G. Kingsolver.

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Kingsolver, J.G., Diamond, S.E., Siepielski, A.M. et al. Synthetic analyses of phenotypic selection in natural populations: lessons, limitations and future directions. Evol Ecol 26, 1101–1118 (2012). https://doi.org/10.1007/s10682-012-9563-5

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