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Indirect genetic effects are shaped by demographic history and ecology in Arabidopsis thaliana

Nature Ecology & Evolution volume 7, pages 1878–1891 (2023)Cite this article

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Abstract

The phenotype of an individual can be affected by the genes of its conspecifics through indirect genetic effects (IGEs). IGEs have been studied across different organisms including wild and domesticated animals and plants, but little is known about their genetic architecture. Here, in a large-scale intraspecific interaction experiment, we show that the contribution of IGEs to the biomass variation of Arabidopsis thaliana is comparable to values classically reported in animals. Moreover, we identify 11 loci explaining 85.1% of the variability in IGEs. We find that positive IGE alleles (that is, those with positive effects on neighbour biomass) occur both in relict accessions from southern Eurasia and in post-glacial colonizers from northern Scandinavia, and that they are likely to have two divergent origins: for nine loci, they evolved in the post-glacial colonizers independently from the relicts, while the two others were introgressed in the post-glacial colonizer from the relicts. Finally, we find that variation in IGEs probably reflects divergent adaptations to the contrasting environments of the edges and the centre of the native range of the species. These findings reveal a surprisingly tractable genetic basis of IGEs in A. thaliana that is shaped by the ecology and the demographic history of the species.

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Fig. 1: Overview of the experimental design and quantification of IGEs.
Fig. 2: GWAS of IGEs on plant biomass.
Fig. 3: Geographic distribution of IGE variants.
Fig. 4: Admixture between non-relicts from north Sweden and relicts at IGE loci.
Fig. 5: Association between IGE loci and environmental variables.
Fig. 6: Association between IGE loci and plant growth.

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Data availability

The data analysed in this study are available in Zenodo: https://doi.org/10.5281/zenodo.7944154

Code availability

All the code used for statistical analysis is available in Zenodo: https://doi.org/10.5281/zenodo.7944154

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Acknowledgements

We thank C. Fankhauser, T. Kay and Q. Pan for their helpful comments on the manuscript and A. Estarague, F. Vasseur and C. Violle for insightful discussions. This work was supported by the University of Lausanne, the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement SOCLE (no. 101030712) to G.M. S.E.W. acknowledges funding from the Swiss National Science Foundation, project no. 310030_192537.

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Author notes

  1. Laurent Keller

    Present address: Social Evolution Unit, Chesières, Switzerland

Authors and Affiliations

  1. Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

    Germain Montazeaud, Quentin Helleu & Laurent Keller

  2. Structure et Instabilité des Génomes, Muséum National d’Histoire Naturelle, CNRS UMR7196, INSERM U1154, Paris, France

    Quentin Helleu

  3. Group Breeding Research, Division Plant Breeding, Agroscope, Wädenswil, Switzerland

    Samuel E. Wuest

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Contributions

G.M. and S.E.W conceptualized the study based on data previously collected by S.E.W. G.M. conducted the quantification of IGEs, the GWAS and the GEAs. G.M. and Q.H. performed introgression tests and investigated candidate genes. G.M. wrote the manuscript with L.K. All the authors commented on the manuscript. L.K. advised and oversaw the project.

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Correspondence to Germain Montazeaud or Laurent Keller.

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Nature Ecology & Evolution thanks Amelie Baud, Julin Maloof and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Supplementary Data 1

List of genes with at least one non-synonymous or frameshift mutation that is in proximity and in high linkage with an SNP significantly associated with IGE.

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Montazeaud, G., Helleu, Q., Wuest, S.E. et al. Indirect genetic effects are shaped by demographic history and ecology in Arabidopsis thaliana. Nat Ecol Evol 7, 1878–1891 (2023). https://doi.org/10.1038/s41559-023-02189-4

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