Phenotypic plasticity is the capacity for an individual genotype to produce different phenotypes in response to environmental variation1. Most traits are plastic, but the degree to which plasticity is adaptive or non-adaptive depends on whether environmentally induced phenotypes are closer or further away from the local optimum2,3,4. Existing theories make conflicting predictions about whether plasticity constrains or facilitates adaptive evolution4,5,6,7,8,9,10,11,12. Debate persists because few empirical studies have tested the relationship between initial plasticity and subsequent adaptive evolution in natural populations. Here we show that the direction of plasticity in gene expression is generally opposite to the direction of adaptive evolution. We experimentally transplanted Trinidadian guppies (Poecilia reticulata) adapted to living with cichlid predators to cichlid-free streams, and tested for evolutionary divergence in brain gene expression patterns after three to four generations. We find 135 transcripts that evolved parallel changes in expression within the replicated introduction populations. These changes are in the same direction exhibited in a native cichlid-free population, suggesting rapid adaptive evolution. We find 89% of these transcripts exhibited non-adaptive plastic changes in expression when the source population was reared in the absence of predators, as they are in the opposite direction to the evolved changes. By contrast, the remaining transcripts exhibiting adaptive plasticity show reduced population divergence. Furthermore, the most plastic transcripts in the source population evolved reduced plasticity in the introduction populations, suggesting strong selection against non-adaptive plasticity. These results support models predicting that adaptive plasticity constrains evolution6,7,8, whereas non-adaptive plasticity potentiates evolution by increasing the strength of directional selection11,12. The role of non-adaptive plasticity in evolution has received relatively little attention; however, our results suggest that it may be an important mechanism that predicts evolutionary responses to new environments.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)
Schmalhausen, I. I. Factors of Evolution: the Theory of Stabilizing Selection (Blakiston, 1949)
López-Maury, L., Marguerat, S. & Bahler, J. Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nature Rev. Genet. 9, 583–593 (2008)
Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznick, D. N. Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394–407 (2007)
Baldwin, J. M. Development and Evolution (Macmillan Company, 1902)
Ancel, L. W. Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58, 307–319 (2000)
Price, T. D., Qvarnström, A. & Irwin, D. E. The role of phenotypic plasticity in driving genetic evolution. Proc. R. Soc. Lond. B 270, 1433–1440 (2003)
Paenke, I., Sendhoff, B. & Kawecki, T. J. Influence of plasticity and learning on evolution under directional selection. Am. Nat. 170, E47–E58 (2007)
Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435–1446 (2009)
Chevin, L.-M., Lande, R. & Mace, G. M. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. 8, e1000357 (2010)
Grether, G. F. Environmental change, phenotypic plasticity, and genetic compensation. Am. Nat. 166, E115–E123 (2005)
Conover, D. O., Duffy, T. A. & Hice, L. A. The covariance between genetic and environmental influences across ecological gradients: reassessing the evolutionary significance of countergradient and cogradient variation. Ann. NY Acad. Sci. 1168, 100–129 (2009)
Wright, S. Evolution in Medelian populations. Genetics 16, 97–159 (1931)
Waddington, C. H. Genetic assimilation. Adv. Genet. 10, 257–293 (1961)
Suzuki, Y. & Nijhout, H. F. Evolution of a polyphenism by genetic accommodation. Science 311, 650–652 (2006)
Schaum, C. E. & Collins, S. Plasticity predicts evolution in marine algae. Proc. R. Soc. Lond. B 281, 20141486 (2014)
Losos, J. B. et al. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54, 301–305 (2000)
Wund, M. A., Baker, J. A., Clancy, B., Golub, J. L. & Foster, S. A. A test of the “flexible stem” model of evolution: ancestral plasticity, genetic accommodation, and morphological divergence in the threespine stickleback radiation. Am. Nat. 172, 449–462 (2008)
McCairns, R. J. & Bernatchez, L. Adaptive divergence between freshwater and marine sticklebacks: insights into the role of phenotypic plasticity from an integrated analysis of candidate gene expression. Evolution 64, 1029–1047 (2010)
Scoville, A. G. & Pfrender, M. E. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci. USA 107, 4260–4263 (2010)
Willing, E.-M. et al. Genome wide single nucleotide polymorphisms reveal population history and adaptive divergence in wild guppies. Mol. Ecol. 19, 968–984 (2010)
Handelsman, C. A. et al. Predator-induced phenotypic plasticity in metabolism and rate of growth: rapid adaptation to a novel environment. Integr. Comp. Biol. 53, 975–988 (2013)
Gibson, G. & Weir, B. The quantitative genetics of transcription. Trends Genet. 21, 616–623 (2005)
Leder, E. H. et al. The evolution and adaptive potential of transcriptional variation in sticklebacks-Signatures of selection and widespread heritability. Mol. Biol. Evol. 32, 674–689 (2015)
Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990)
Reznick, D. N., Shaw, F. H., Rodd, F. H. & Shaw, R. G. Evaluation of the rate of evolution in natural populations of guppies (Poecilia reticulata). Science 275, 1934–1937 (1997)
Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008)
Gomulkiewicz, R. & Holt, R. D. When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995)
Reznick, D., Butler, M. J. IV. & Rodd, H. Life-history evolution in guppies. VII. The comparative ecology of high-and low-predation environments. Am. Nat. 157, 126–140 (2001)
Merlo, L. M., Pepper, J. W., Reid, B. J. & Maley, C. C. Cancer as an evolutionary and ecological process. Nature Rev. Cancer 6, 924–935 (2006)
Kohler, T. J., Heatherly, T. N., II, El-Sabaawi, R. W., Zandonà, E., Marshall, M. C., Flecker, A. S., Pringle, C. M., Reznick, D. N. & Thomas, S. A. Flow, nutrients, and light availability influence Neotropical epilithon biomass and stoichiometry. Freshwater Sci. 31, 1019–1034 (2012)
Torres-Dowdall, J., Handelsman, C. A., Reznick, D. N. & Ghalambor, C. K. Local adaptation and the evolution of phenotypic plasticity in Trinidadian guppies (Poecilia reticulata). Evolution 66, 3432–3443 (2012)
Ruell, E. W. et al. Fear, food and sexual ornamentation: plasticity of colour development in Trinidadian guppies. Proc. R. Soc. Lond. B 280, 20122019 (2013)
Reznick, D. The impact of predation on life history evolution in Trinidadian guppies: genetic basis of observed life history patterns. Evolution 36, 1236–1250 (1982)
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010)
Culhane, A. C., Perriere, G., Considine, E. C., Cotter, T. G. & Higgins, D. G. Between-group analysis of microarray data. Bioinformatics 18, 1600–1608 (2002)
Culhane, A. C., Thioulouse, J., Perrière, G. & Higgins, D. G. MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics 21, 2789–2790 (2005)
Gingerich, P. D. Rates of evolution on the time scale of the evolutionary process. Genetica 112–113, 127–144 (2001)
Jackson, D. A. & Somers, K. M. The spectre of “spurious” correlations. Oecologia 86, 147–151 (1991)
Leinonen, T., Cano, J. M., Mäkinen, H. & Merilä, J. Contrasting patterns of body shape and neutral genetic divergence in marine and lake populations of threespine sticklebacks. J. Evol. Biol. 19, 1803–1812 (2006)
Fitzpatrick, S. W., Gerberich, J. C., Kronenberger, J. A., Angeloni, L. M. & Funk, W. C. Locally adapted traits maintained in the face of high gene flow. Ecol. Lett. 18, 37–47 (2015)
This work was supported by grants from the National Science Foundation (DEB-0846175 to C.K.G., EF-0623632 to D.N.R., and IOS-0934451 and IOS-1354775 to K.A.H.). We thank C. Handelsman, K. Langin, D. Broder, E. Duval, I. Janowitz, E. Lange, A. Shah, J. Havrid, E. Kane and L. Angeloni for helpful comments on the study. Computing for this project was performed on the Spear cluster at the Research Computing Center at the Florida State University
The authors declare no competing financial interests.
Extended data figures and tables
Guppies were moved from a high-predation (HP) locality where they coexist with cichlid predators and introduced into two streams that lacked cichlids and guppies, Intro1 (left photograph) and Intro2 (right photograph). A naturally occurring guppy population without cichlids, low-predation (LP), was sampled to provide a low-predation reference.
Extended Data Figure 2 Frequency histogram of Haldanes for the top 500 transcripts loading on PC2—the axis representing rapid evolutionary divergence between the source and introduction populations.
a, Intro1 (median Haldane = 0.256, range = 0.07–0.74). b, Intro2 (median = 0.226, range = 0.10–1.68).
Extended Data Figure 3 Ancestral plasticity and evolution in patterns of gene expression for a representative gene: uridine phosphorylase 2 (upp2).
Shown is the plastic response of the high-predation source population and the evolved responses in the two experimental introduction populations (Intro1 and Intro2). In this case the plastic response results in a decrease in expression, whereas the evolved response in the introduction populations is to increase expression, thus illustrating non-adaptive plasticity.
Extended Data Figure 4 Scatter plot of ancestral plasticity (change in transcript abundance to the absence of cichlid predator cues) and population divergence.
Shown are the 565 transcripts that exhibited significant differences in expression between the predator and non-predator rearing treatments in the HP source population. We found a similar pattern as was found for the CDE transcripts (Fig. 2): 75% (424 out of 565) of the significantly plastic genes exhibited population divergence in the introduction populations in the opposite direction of plasticity (χ2 = 284.2, d.f. = 1). This result falls in the upper percentile of the 250 permuted χ2 values; median permuted values = 19.1, interquartile range = 6.7–50.8. Only eight transcripts were common to the data sets that were significantly evolved (CDE; Figs 2, 3) and significantly plastic, suggesting that short-term plastic responses and longer-term evolutionary responses involve largely different sets of genes.
About this article
Cite this article
Ghalambor, C., Hoke, K., Ruell, E. et al. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature. Nature 525, 372–375 (2015). https://doi.org/10.1038/nature15256
Molecular Biology and Evolution (2020)
Trends in Ecology & Evolution (2020)
Nature Ecology & Evolution (2020)
Asymmetric Isolation and the Evolution of Behaviors Influencing Dispersal: Rheotaxis of Guppies above Waterfalls