Ecologists and evolutionary biologists are well aware that natural and sexual selection do not operate on traits in isolation, but instead act on combinations of traits. This long-recognized and pervasive phenomenon is known as multivariate selection, or—in the particular case where it favours correlations between interacting traits—correlational selection. Despite broad acknowledgement of correlational selection, the relevant theory has often been overlooked in genomic research. Here, we discuss theory and empirical findings from ecological, quantitative genetic and genomic research, linking key insights from different fields. Correlational selection can operate on both discrete trait combinations and quantitative characters, with profound implications for genomic architecture, linkage, pleiotropy, evolvability, modularity, phenotypic integration and phenotypic plasticity. We synthesize current knowledge and discuss promising research approaches that will enable us to understand how correlational selection shapes genomic architecture, thereby linking quantitative genetic approaches with emerging genomic methods. We suggest that research on correlational selection has great potential to integrate multiple fields in evolutionary biology, including developmental and functional biology, ecology, quantitative genetics, phenotypic polymorphisms, hybrid zones and speciation processes.
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We are grateful to D. Goedert for comments on the first draft of this manuscript. E.I.S. and A.R. were funded by grants from the Swedish Research Council (VR; grant numbers 2016-03356 and 2018-04537, respectively). D.A.M. was supported by the Swiss National Science Foundation (grant no. 31003A_163338 to O. Seehausen, L. Excoffier and R. Bruggmann). J.D. acknowledges support by NSF 13-510 Systems & Synthetic Biology, award no. 1714550. J.M.H. is supported by the German Federal Ministry of Education and Research (BMBF). K.C. was supported by a Swiss National Science Foundation grant (CRSK-3_190288). K.M. was funded by the Australian Research Council (DP190101661). M.N.S. was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP), projects 2015/19556-4 and 2016/22159-0. We also wish to thank B. Brodie for kindly providing us with the photograph of the garter snakes in Fig. 2a and the original figure of his classic fitness surface in Box 1.
The authors declare no competing interests.
Peer review information Nature Ecology & Evolution thanks Alison Bell, Frederic Guillaume and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
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Svensson, E.I., Arnold, S.J., Bürger, R. et al. Correlational selection in the age of genomics. Nat Ecol Evol 5, 562–573 (2021). https://doi.org/10.1038/s41559-021-01413-3