Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature

  • An Erratum to this article was published on 29 March 2018

Abstract

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.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Rapid evolutionary divergence in gene expression as measured in second-generation laboratory-born guppies derived from the wild.
Figure 2: Rapid evolutionary divergence is highly correlated with non-adaptive plasticity.
Figure 3: Rapid evolution of reduced plasticity.

Accession codes

Primary accessions

Sequence Read Archive

Data deposits

The sequence data are available at the Sequence Reads Archive (SRA) under accession number SRP062364.

Change history

  • 28 March 2018

    Please see accompanying Erratum (http://doi.org/10.1038/nature25499). The SRA accession should have been ‘SRP062364’ rather than ‘SRP06234’. In addition, owing to an error in the code used to produce some of the simulations, there were several other errors in this Letter, affecting the Methods, Figs 2, 3, Extended Data Table 1, Extended Data Fig. 4, and Supplementary Tables 1 and 2. Please see the Erratum and its accompanying Supplementary Information for further details. The Letter has not been corrected online.

References

  1. 1

    West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, 2003)

    Google Scholar 

  2. 2

    Schmalhausen, I. I. Factors of Evolution: the Theory of Stabilizing Selection (Blakiston, 1949)

    Google Scholar 

  3. 3

    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)

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  4. 4

    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)

    Article  Google Scholar 

  5. 5

    Baldwin, J. M. Development and Evolution (Macmillan Company, 1902)

    Google Scholar 

  6. 6

    Ancel, L. W. Undermining the Baldwin expediting effect: does phenotypic plasticity accelerate evolution? Theor. Popul. Biol. 58, 307–319 (2000)

    CAS  PubMed  MATH  Article  PubMed Central  Google Scholar 

  7. 7

    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)

    Article  Google Scholar 

  8. 8

    Paenke, I., Sendhoff, B. & Kawecki, T. J. Influence of plasticity and learning on evolution under directional selection. Am. Nat. 170, E47–E58 (2007)

    PubMed  Article  PubMed Central  Google Scholar 

  9. 9

    Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation. J. Evol. Biol. 22, 1435–1446 (2009)

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  10. 10

    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)

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  11. 11

    Grether, G. F. Environmental change, phenotypic plasticity, and genetic compensation. Am. Nat. 166, E115–E123 (2005)

    PubMed  Article  PubMed Central  Google Scholar 

  12. 12

    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)

    ADS  PubMed  Article  PubMed Central  Google Scholar 

  13. 13

    Wright, S. Evolution in Medelian populations. Genetics 16, 97–159 (1931)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. 14

    Waddington, C. H. Genetic assimilation. Adv. Genet. 10, 257–293 (1961)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  15. 15

    Suzuki, Y. & Nijhout, H. F. Evolution of a polyphenism by genetic accommodation. Science 311, 650–652 (2006)

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  16. 16

    Schaum, C. E. & Collins, S. Plasticity predicts evolution in marine algae. Proc. R. Soc. Lond. B 281, 20141486 (2014)

    Article  Google Scholar 

  17. 17

    Losos, J. B. et al. Evolutionary implications of phenotypic plasticity in the hindlimb of the lizard Anolis sagrei. Evolution 54, 301–305 (2000)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. 18

    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)

    PubMed  Article  Google Scholar 

  19. 19

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  20. 20

    Scoville, A. G. & Pfrender, M. E. Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci. USA 107, 4260–4263 (2010)

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. 21

    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)

    PubMed  Article  PubMed Central  Google Scholar 

  22. 22

    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)

    PubMed  Article  PubMed Central  Google Scholar 

  23. 23

    Gibson, G. & Weir, B. The quantitative genetics of transcription. Trends Genet. 21, 616–623 (2005)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. 24

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  25. 25

    Reznick, D. A., Bryga, H. & Endler, J. A. Experimentally induced life-history evolution in a natural population. Nature 346, 357–359 (1990)

    ADS  Article  Google Scholar 

  26. 26

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  27. 27

    Charmantier, A. et al. Adaptive phenotypic plasticity in response to climate change in a wild bird population. Science 320, 800–803 (2008)

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  28. 28

    Gomulkiewicz, R. & Holt, R. D. When does evolution by natural selection prevent extinction? Evolution 49, 201–207 (1995)

    PubMed  Article  PubMed Central  Google Scholar 

  29. 29

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30

    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)

    CAS  Article  Google Scholar 

  31. 31

    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)

    Article  Google Scholar 

  32. 32

    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)

    PubMed  Article  PubMed Central  Google Scholar 

  33. 33

    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)

    CAS  Article  Google Scholar 

  34. 34

    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)

    PubMed  Article  PubMed Central  Google Scholar 

  35. 35

    Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, R25 (2010)

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. 36

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. 37

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  38. 38

    Gingerich, P. D. Rates of evolution on the time scale of the evolutionary process. Genetica 112–113, 127–144 (2001)

    PubMed  Article  PubMed Central  Google Scholar 

  39. 39

    Jackson, D. A. & Somers, K. M. The spectre of “spurious” correlations. Oecologia 86, 147–151 (1991)

    ADS  CAS  PubMed  Article  PubMed Central  Google Scholar 

  40. 40

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  41. 41

    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)

    CAS  PubMed  Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

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

Author information

Affiliations

Authors

Contributions

C.K.G., K.L.H. and K.A.H. planned and executed the study, E.W.R. reared the fish, E.K.F. collected the tissues K.A.H. analysed the gene expression data, D.N.R. planned and oversaw the field introduction experiments, and C.K.G. oversaw the laboratory experiments. All authors participated in writing the manuscript.

Corresponding authors

Correspondence to Cameron K. Ghalambor or Kimberly A. Hughes.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Map of Trinidad where the experimental transplants took place.

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.

Extended Data Table 1 Comparison of gene expression divergence (PST) with divergence of putatively neutral microsatellite loci (FST)

Supplementary information

Supplementary Table 1

This table contains a list of all significantly evolved genes. (XLSX 402 kb)

Supplementary Table 2

This table contains a list of all significantly plastic genes. (XLSX 436 kb)

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

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

Download citation

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.