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.
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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.
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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
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