Contrasting effects of environment and genetics generate a continuum of parallel evolution

Abstract

Parallel evolution of similar traits by independent populations in similar environments is considered strong evidence for adaptation by natural selection. Often, however, replicate populations in similar environments do not all evolve in the same way, thus deviating from any single, predominant outcome of evolution. This variation might arise from non-adaptive, population-specific effects of genetic drift, gene flow or limited genetic variation. Alternatively, these deviations from parallel evolution might also reflect predictable adaptation to cryptic environmental heterogeneity within discrete habitat categories. Here, we show that deviations from parallel evolution are the consequence of environmental variation within habitats combined with variation in gene flow. Threespine stickleback (Gasterosteus aculeatus) in adjoining lake and stream habitats (a lake–stream ‘pair’) diverge phenotypically, yet the direction and magnitude of this divergence is not always fully parallel among 16 replicate pairs. We found that the multivariate direction of lake–stream morphological divergence was less parallel between pairs whose environmental differences were less parallel. Thus, environmental heterogeneity among lake–stream pairs contributes to deviations from parallel evolution. Additionally, likely genomic targets of selection were more parallel between environmentally more similar pairs. In contrast, variation in the magnitude of lake–stream divergence (independent of direction) was better explained by differences in lake–stream gene flow; pairs with greater lake–stream gene flow were less morphologically diverged. Thus, both adaptive and non-adaptive processes work concurrently to generate a continuum of parallel evolution across lake–stream stickleback population pairs.

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Figure 1: Variation in the extent of parallel evolution among individual phenotypic traits, each tested separately.
Figure 2: Calculation of L, ΔL and θ.
Figure 3: Replicate lake–stream pairs exhibit variation in extent of parallel divergence.
Figure 4: Comparisons among 16 pairs reveal that deviations from parallel phenotypic divergence are correlated with both environmental (first column) and genetic (second column) deviations from parallel.

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Acknowledgements

We thank B. Anholt, O. Banjoko, M. Dubin, L. Duncan, S. Halbrook, T. Ingram, A. Kamath, E. Delaney, C. LeBlond, J. Losos, K. Oke, S. Pakula, R. Rangel, S. Rogers, G. Rolshausen, S. Rudman, O. Schmidt, W. Shim, C. Tanner, L. Tanter, the Schluter Lab, the Bamfield Marine Sciences Centre, the Genome Sequencing and Analysis Facility at UT Austin and the Texas Advance Computing Center at UT Austin for their help, advice and comments throughout the research and writing. The British Columbia Ministry of the Environment provided essential permits. The research was supported by National Science Foundation grants DEB-1144773 (D.I.B. and A.P.H.), DEB-1144556 (C.L.P.) and IOS-1145468 (D.I.B.) and conducted in full compliance with ethical regulations according to UT Austin’s Institutional Care and Use Committee (AUP-2012-00065 and AUP-2014-00293).

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Contributions

A.P.H., C.L.P., R.D.H.B., D.H., B.K.L., Y.E.S. and D.I.B. planned the study. All authors executed the study. Y.E.S. oversaw field collections, conducted with D.I.B., C.L.P., A.P.H., R.D.H.B., D.H., B.K.L., T.T., A.D. and R.I. Y.E.S. oversaw morphological and environmental data collections by Y.E.S., D.I.B., C.J.T., T.T., N.A. and R.I. Y.E.S. collected genomic data with help from J.N.W. and D.I.B. Y.E.S., T.V. and D.I.B. analysed the data. M.R. estimated the population genetic parameters. All authors participated in the writing of the manuscript.

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Correspondence to Yoel E. Stuart.

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Supplementary information

Supplementary Information

Descriptions of approximate Bayesian computation analyses, phenotype–environment analyses, Supplementary Tables 1–8, and Supplementary Figures 1–6. (PDF 1758 kb)

Supplementary Dataset

Pair-by-trait, lake–stream t-tests. Each row represents the multidimensional lake–stream divergence vector for a given pair. Each column is the t-statistic from a t-test comparing lake versus adjoined stream for that trait. (CSV 9 kb)

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Stuart, Y., Veen, T., Weber, J. et al. Contrasting effects of environment and genetics generate a continuum of parallel evolution. Nat Ecol Evol 1, 0158 (2017). https://doi.org/10.1038/s41559-017-0158

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