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

Nature Ecology & Evolution volume 1, Article number: 0158 (2017) Cite this article

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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.

Parallel evolution occurs when phenotypes evolve in the same way in replicate populations adapting to similar habitats1,2 and is strong evidence for the importance of natural selection in adaptive evolution2–7. As an exemplar, marine Threespine stickleback (Gasterosteus aculeatus) have independently colonized many freshwater habitats8–12 in which they repeatedly evolved reduced armour1, probably in response to differences in predator regimes and salinity. However, even such iconic examples of parallel evolution often present many exceptions13–16; that is, replicate populations vary in the magnitude or even in the direction of trait evolution (for example, for stickleback armour, see refs 16–19).

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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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Author notes

  1. Thor Veen, Jesse N. Weber & Catherine L. Peichel

    Present address: †Present addresses: Life Sciences, Quest University,Squamish,British Columbia V8B 0N8,Canada (T.V.); Division of Biological Sciences, University of Montana, Missoula, Montana 59812, USA (J.N.W.); Institute of Ecology and Evolution, University of Bern, Bern 3012, Switzerland (C.L.P.).,

Authors and Affiliations

  1. Department of Integrative Biology, University of Texas at Austin, Austin, Texas 78712, USA

    Yoel E. Stuart, Thor Veen, Jesse N. Weber, Brian K. Lohman, Cole J. Thompson, Rebecca Izen, Newaz Ahmed & Daniel I. Bolnick

  2. Redpath Museum, McGill University, Montreal, Quebec H3A 2K6, Canada

    Dieta Hanson, Rowan D. H. Barrett & Andrew P. Hendry

  3. Department of Biosciences, University of Oslo, Oslo 0316, Norway

    Mark Ravinet

  4. Austin Independent School District, Austin, Texas 78703, USA

    Tania Tasneem & Andrew Doggett

  5. Divisions of Basic Sciences and Human Biology, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA

    Catherine L. Peichel

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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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The authors declare no competing financial interests.

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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