Ecology shapes epistasis in a genotype–phenotype–fitness map for stick insect colour

Abstract

Genetic interactions such as epistasis are widespread in nature and can shape evolutionary dynamics. Epistasis occurs due to nonlinearity in biological systems, which can arise via cellular processes that convert genotype to phenotype and via selective processes that connect phenotype to fitness. Few studies in nature have connected genotype to phenotype to fitness for multiple potentially interacting genetic variants. Thus, the causes of epistasis in the wild remain poorly understood. Here, we show that epistasis for fitness is an emergent and predictable property of nonlinear selective processes. We do so by measuring the genetic basis of cryptic colouration and survival in a field experiment with stick insects. We find that colouration shows a largely additive genetic basis but with some effects of epistasis that enhance differentiation between colour morphs. In terms of fitness, different combinations of loci affecting colouration confer high survival in one host-plant treatment. Specifically, nonlinear correlational selection for specific combinations of colour traits in this treatment drives the emergence of pairwise and higher-order epistasis for fitness at loci underlying colour. In turn, this results in a rugged fitness landscape for genotypes. In contrast, fitness epistasis was dampened in another treatment, where selection was weaker. Patterns of epistasis that are shaped by ecologically based selection could be common and central to understanding fitness landscapes, the dynamics of evolution and potentially other complex systems.

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Fig. 1: Schematic of the hypotheses examined.
Fig. 2: Objectively quantifying colour variation from digital photographs.
Fig. 3: Genetics of cryptic colouration in T. chumash.
Fig. 4: Phenotypic selection on colouration in a field experiment.
Fig. 5: Evidence of epistasis for fitness and the fitness landscape.

Data availability

DNA sequences have been deposited in the NCBI SRA (BioProject PRJNA656892). Other data, including colour measurements and results from the experiment, have been archived in Dryad Digital Repository (https://doi.org/10.5061/dryad.2z34tmpjr). Correspondence and requests for materials should be sent to P.N.

Code availability

Core scripts have been archived in Dryad Digital Repository (https://doi.org/10.5061/dryad.2z34tmpjr).

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Acknowledgements

We thank T. Reimchen, M. Joron, L.-M. Chevin and D. Ayala for discussion and comments on previous versions of the manuscript, M. Muschick for help with photography and reflectance measurements and T. Oakley for laboratory space. The support and resources from the Center for High Performance Computing at the University of Utah are gratefully acknowledged, as well as access to the High Performance Computing Facilities, particularly to the Iceberg and ShARC HPC clusters, from the Corporate Information and Computing Services at the University of Sheffield. The work was funded by a grant from the European Research Council (grant no. EE-Dynamics 770826, https://erc.europa.eu/) and a grant from the National Science Foundation of the United States (grant no. NSF DEB 1638768). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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All authors conceived the project and contributed to writing. R.V., C.F.C., T.L.P. and P.N. collected data. Z.G. led data analysis, aided by all authors.

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Correspondence to Patrik Nosil.

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Nosil, P., Villoutreix, R., de Carvalho, C.F. et al. Ecology shapes epistasis in a genotype–phenotype–fitness map for stick insect colour. Nat Ecol Evol (2020). https://doi.org/10.1038/s41559-020-01305-y

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