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Personal and transgenerational cues are nonadditive at the phenotypic and molecular level


Organisms can gain information about their environment from their ancestors, their parents or their own personal experience. ‘Cue integration’ models often start with the simplifying assumption that information from different sources is additive. Here, we test key assumptions and predictions of cue integration theory at both the phenotypic and molecular level in threespined sticklebacks (Gasterosteus aculeatus). We show that regardless of whether cues about predation risk were provided by their father or acquired through personal experience, sticklebacks produced the same set of predator-adapted phenotypes. Moreover, there were nonadditive effects of personal and paternal experience: animals that received cues from both sources resembled animals that received cues from a single source. A similar pattern was detected at the molecular level: there was a core set of genes that were differentially expressed in the brains of offspring regardless of whether risk was experienced by their father, themselves or both. These results provide strong support for cue integration theory because they show that cues provided by parents and personal experience are comparable at both the phenotypic and molecular level, and draw attention to the importance of nonadditive responses to multiple cues.

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Fig. 1: Experimental design.
Fig. 2: The effect of personal and paternal experience with predation risk on offspring phenotypes was nonadditive.
Fig. 3: Brain gene expression responses to personal experience with risk and paternal experience with risk.


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We are grateful to E. Murdoch for help with RNA extraction and building libraries for RNA-seq, and M. Bensky for the stickleback and sculpin illustrations. We also thank A. Sih, J. Stamps, G. Robinson, K. Hoke and S. English for valuable comments on the manuscript. This material is based upon work supported by the National Science Foundation under grant no. IOS 1210696 and a National Science Foundation Graduate Research Fellowship to L.R.S. Research reported in this publication was supported by National Institute of General Medical Sciences of the National Institutes of Health under award no. R01 GM082937. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Authors and Affiliations



L.R.S. and A.M.B. conceived and designed the project. L.R.S. carried out the experiment and performed data collection. L.R.S., S.A.B. and A.M.B. analysed the data. L.R.S., S.A.B. and A.M.B. wrote the manuscript.

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Correspondence to Laura R. Stein.

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The authors declare no competing interests.

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Supplementary Information

Supplementary Information

Supplementary Table 1; Supplementary Figures 1–3; Supplementary Reference

Reporting Summary

Supplementary Table 2

Alignment and percent reads mapped to stickleback genome

Supplementary Table 3

Differentially expressed gene lists for paternal experience, personal experience, and both cue treatments

Supplementary Table 4

GO and functional enrichments for all treatments

Supplementary Table 5

Phenotypic data of offspring

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Stein, L.R., Bukhari, S.A. & Bell, A.M. Personal and transgenerational cues are nonadditive at the phenotypic and molecular level. Nat Ecol Evol 2, 1306–1311 (2018).

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