Why phenotypic plasticity is important

View 1 excerpt, cites background. The consequences of phenotypic plasticity on postglacial fishes. Ecological factors shaping immune response and related. Variation in biotic and abiotic ecological factors unavoidably shapes the life history of living organisms.

The ability to integrate environmental cues and respond adequately can mark the difference … Expand. Adaptive phenotypic plasticity for life-history and less fitness-related traits. View 3 excerpts, cites background. Phenotypic plasticity with instantaneous but delayed switches.

Introduction to the symposium-uniting evolutionary and physiological approaches to understanding phenotypic plasticity. Quantitative trait loci mapping of phenotypic plasticity and genotype—environment interactions in plant and insect performance.

The evolutionary consequences of ecological interactions mediated through phenotypic plasticity. Highly Influential. View 4 excerpts, references background. Ecological consequences of phenotypic plasticity. View 1 excerpt, references background. Constraints on the evolution of adaptive phenotypic plasticity in plants. Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes.

View 5 excerpts, references background. Four features are necessary to reveal the importance of plasticity for the evolution of a given trait. First, comparative phylogenetic studies must show that plasticity indeed coincides with a novel trait. Second, molecular mechanisms must provide insight into how environmental information is perceived and how switch genes regulate alternative phenotypes.

Third, the role of selection driving the adaptation of plastic traits has to be investigated in a phylogenetic context, resulting in genetic accommodation and assimilation. However, the true challenge for the decade to come will be to show the molecular mechanisms of genetic assimilation and, thus, how environmental information becomes genetically encoded during character canalization. I thank M.

Dardiry, T. Renahan, and Dr. Werner for critically reading this manuscript; M. Voetsch for the artwork; and members of my laboratory, and the many international colleagues and friends, for stimulating discussions about phenotypic plasticity and its role in evolution over the years. The author also wants to apologize to important contributions in the field that could not be cited because of space restrictions. National Center for Biotechnology Information , U.

Journal List Genetics v. Published online Mar Ralf J. Sommer 1. Author information Article notes Copyright and License information Disclaimer. E-mail: ed. Received Nov 29; Accepted Mar 9. Available freely online through the author-supported open access option. This article has been cited by other articles in PMC.

Abstract Phenotypic plasticity is defined as the property of organisms to produce distinct phenotypes in response to environmental variation. Keywords: phenotypic plasticity, polyphenisms, switch genes, plasticity first evolution, canalization, genetic assimilation, genetic accommodation, Pristionchus , Spea , Ontophagus , Manduca. Box 1. A: Historical skepticism against phenotypic plasticity and its significance for evolution 1. Empirical evidence for plasticity?

Can environmental responsiveness promote evolution? Molecular mechanisms of environmental influence? How should environmental effects be targeted by selection? B: Developmental plasticity and evolution - West-Eberhard and four unique contributions for plasticity as a mechanism of evolution A giant collection of alternative phenotypes Alternative phenotypes as functionally independent targets of selection A general critique of Neo-Darwinism and its inconsistencies and gaps Plasticity as a facilitator of novelty The facilitator hypothesis C: Three predictions for contemporary research to test the facilitator hypothesis The origin of novelty starts with environmentally responsive and developmentally plastic organisms Environmental responsiveness requires developmental switch genes to allow developmental reprograming Molecular mechanisms of environmental influence?

Three Independent, Conceptual Features of Phenotypic Plasticity Three conceptual features of plasticity are important to properly evaluate the significance of plasticity for evolution. The History of a Concept From Baldwin to Bradshaw Some of the controversy and contention around phenotypic plasticity has a historic basis. He wrote: Polyphenism is discontinuous when definite castes are present or definite stages in the life cycle or definite seasonal forms.

Three Predictions for the Role of Plasticity in Evolution Three predictions have to be fulfilled to support the role of plasticity as facilitator for evolutionary novelty and diversity Box 1C. Prediction 1: novelty relies on plasticity West-Eberhard proposed that the origin of novelty often starts with environmentally responsive and developmentally plastic traits West-Eberhard Open in a separate window.

Figure 1. Prediction 2: developmental switch genes and the molecular basis of plasticity Nonplastic developmental processes are hardwired against environmental fluctuations, whereas plastic processes are characterized by being able to sense and respond to environmental information. Prediction 3: regimes of canalization, from genetic accommodation to assimilation Important challenges remain to prove the full significance of plasticity as a major mechanism of evolution. Challenges and Opportunities for Current and Future Research The identification of environmentally induced developmental switches and the indication that plastic traits are indeed subject to selection leave one major challenge unanswered: what are the mechanisms that will result in the genetic assimilation of a trait in the final step of plasticity evolution?

A Four-Step Model for the Role of Plasticity and the Origin of Novelty Plasticity first evolution in spadefoot toad tadpoles, environmentally induced developmental switch genes in predatory nematodes, and genetic accommodation and assimilation in dung beetles and tobacco hornworms not only confirm the major predictions of the facilitator hypothesis, but they also represent the different phases of phenotypic plasticity.

Figure 2. Conclusions Phenotypic plasticity was, for a long time, an underappreciated and in large parts neglected mechanism and concept of evolution. Acknowledgments I thank M. Footnotes Communicating editor: A. Literature Cited Abouheif E. Eco-evo-devo: the time has come. A functional perspective on phenotypic heterogeneity in microorganisms.

Cambridge University Press, Cambridge: The C. Cell : 88— A new factor in evolution. The piRNA pathway responds to environmental signals to establish intergenerational adaptation to stress. BMC Biol. Co-option of the hormone-signalling module dafachronic acid-DAF in nematode evolution.

Nature : — Evolutionary significance of phenotypic plasticity in plants. Development, plasticity and evolution of butterfly eyespot patterns. The right tools for the job: regulating polyphenic morph development in insects. Insect Sci. Multiple plasticity regulators reveal targets specifying an induced predatory form in nematodes. Phenotypic plasticity and the semantics of polyphenism: a historial review and current perspectives , pp.

Science Publishers, Jersey: A neo-Darwinian commentary on macroevolution. Evolution 36 : — Argonautes promote male fertility and provide a paternal memory of germline gene expression in C. Cell : — The Regulatory Genome. Academic Press, San Diego. Bet hedging or not? A guide to proper classification of microbial survival strategies. Bioessays 33 : — Phenotypic Plasticity.

Oxford University Press, Oxford. Bistability in bacteria. The evolutionary genetics of canalization. The Quaternary Review of Biology 80 : — H3K27me and PRC2 transmit a memory of repression across generations and during development. Science : — Adaptive vs. Non-adaptive plasticity potentiates rapid adaptive evolution of gene expression in nature.

Nature : — [corrigenda: Nature ]. Morphological variation and its significance in a polymorphic rotifer: environmental, endogenous and genetic controls. Bioscience 68 : — The flexible stem hypothesis: evidence from genetic data. Genes Evol. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Cell 63 : — The Comparative Method in Evolutionary Biology. Transgenerational epigenetic inheritance: myths and mechanisms.

Cell : 95— Transgenerational effects of early life starvation on growth, reproduction, and stress resistance in Caenorhabditis elegans. Genetics : — Genetic accommodation and the role of ancestral plasticity in the evolution of insect eusociality.

Determining the evolutionary forces shaping GxE. New Phytol. Mechanisms, timescales and principles of trans-generational epigenetic inheritance in animals. Transgenerational transmission of environmental information in C. Genomics of developmental plasticity in animals. Does evolutionary theory need a rethink?

The extended evolutionary synthesis: its structure, assumptions and predictions. Evolution of phenotypic plasticity and environmental tolerance of a labile quantitative character in a fluctuating environment. Plasticity-led evolution: evaluating the key prediction of frequency-dependent adaptation.

Morphological novelty emerges from pre-existing phenotypic plasticity. Bridging the transgenerational gap with epigenetic memory. Trends Genet. Contesting the evidence for non-adaptive plasticity. Nature : E21—E Animal Species and Evolution. Harvard University Press, Cambridge: Developmental mechanisms of threshold evolution in a polyphenic beetle.

Rapid evolution of a polyphenic threshold. The role of developmental plasticity in evolutionary innovation. The significance and scope of evolutionary developmental biology: a vision for the 21st century. Origin of termite eusociality: trophallaxis integrates the social, Nutritional, and microbial environments. Phenotypic plasticity: from microevolution to macroevolution , pp. Springer, Heidelberg. A developmental-physiological perspective on the development and evolution of phenotypic plasticity , pp.

Springer-Verlag, Heidelberg. To plasticity and back again. Elife 4 : e Interface Focus 7: Oettler J. Interruption points in the wing gene regulatory network underlying wing polyphenism evolved independently in male and female morphs in Cardiocondyla ants.

B Mol. Five heads are better than one. Johns Hopkins University Press, Baltimore. Decoding the architecture and origins of mechanisms for developmental polyphenism. A Genetic Switch. A developmental switch coupled to the evolution of plasticity acts through a sulfatase.

Principles of transgenerational small RNA inheritance in Caenorhabditis elegans. Transgenerational inheritance of an acquired small RNA-based antiviral response in C. Starvation-induced transgenerational inheritance of small RNAs in C. Evolving plastic responses to external and genetic environments. New gene origin and deep taxon phylogenomics: opportunities and challenges.

How a growing organismal perspective is adding new depth to integrative studies of morphological evolution. Phenotypic Evolution. Sinauer Associates, Sunderland. University of Chicago Press, Chicago. How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations. Developmental systems of plasticity and trans-generational epigenetic inheritance in nematodes. Chromatin remodelling and antisense-mediated up-regulation of the developmental switch gene eud-1 control predatory feeding plasticity.

Cell 27 : — Cell : 65— Developmental plasticity and robustness of a nematode mouth-form polyphenism. A developmental switch generating phenotypic plasticity is part of a conserved multi-gene locus. Cell Rep. Conserved hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell.

PLoS Genet. Improved phylogenomic sampling of free-living nematodes enhances resolution of higher-level nematode phylogeny.

BMC Evol. Pristionchus pacificus — a nematode model for comparative and evolutionary biology. Leiden; Boston: Brill; Stochastic and conditional regulation of nematode mouth-form dimorphisms. Rapid diversification associated with a macroevolutionary pulse of developmental plasticity. Evolution of a polyphenism by genetic accommodation. Phenotypic plasticity and developmental innovations in nematodes. Log 2 fold changes were calculated in edgeR, and those involving family as main effect or in interaction with another factor were calculated using all six mutually orthogonal contrasts between the seven families, and averaged across contrasts.

Using maximum log 2 fold change across contrasts rather than mean yielded similar results. First, we used the angsd doSaf and realSFS commands to calculate genotype likelihoods and the folded site frequency spectrum from the bam files. Second, we used this site frequency spectrum as prior to calculate diversity measures e. This yielded diversity measures for 14, transcripts that were also expressed in the abdomen.

In order to identify B. Of the 15, B. Briefly, adult P. DNA was extracted from thorax material using a modified version of a salt-extraction protocol. Fastq data were quality-filtered to a minimum PHRED score of Q10, with ends trimmed of adapters and low-quality bases, and screened for common contaminants using bbduk2 BBMap v The Pool-seq data were mapped to the genome using Next-Gen Mapper v0.

SAMtools v1. Using Popoolation v1. Annotation using the B. The resulting gff file was converted to gtf using an in-house script. All statistical analyses were performed in R v. Script is available at Figshare doi: The transcriptome assembly, expression raw count data, and R script are available at Figshare doi: Any other scripts are available from the authors upon request. Piersma, T. Moran, N. The evolutionary maintenance of alternative phenotypes.

Article Google Scholar. Price, T. The role of phenotypic plasticity in driving genetic evolution. B: Biol. Schlichting, C. Via, S. Adaptive phenotypic plasticity: consensus and controversy. Trends Ecol. West-Eberhard, M. Parmesan, C. Ecological and evolutionary responses to recent climate change.

Chevin, L. Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol. What can plasticity contribute to insect responses to climate change? Article PubMed Google Scholar. Urban, M. Improving the forecast for biodiversity under climate change.

Genotype-environment interaction and the evolution of phenotypic plasticity. Evolution 39 , — Lande, R. Adaptation to an extraordinary environment by evolution of phenotypic plasticity and genetic assimilation.

Charmantier, A. Climate change and timing of avian breeding and migration: evolutionary versus plastic changes. Nussey, D. Selection on heritable phenotypic plasticity in a wild bird population. Science , — Kvist, J. Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits. Leder, E. The evolution and adaptive potential of transcriptional variation in sticklebacks—signatures of selection and widespread heritability.

Nijhout, H. Development and evolution of adaptive polyphenisms. Reed, T. Phenotypic plasticity and population viability: the importance of environmental predictability. Cambridge University Press, Cambridge, Thackeray, S. Phenological sensitivity to climate across taxa and trophic levels. Nature , — Visser, M. Shifts in phenology due to global climate change: the need for a yardstick. Ashander, J. Predicting evolutionary rescue via evolving plasticity in stochastic environments.

Keeping up with a warming world; assessing the rate of adaptation to climate change. Brakefield, P. The African butterfly bicyclus anynana: a model for evolutionary genetics and evolutionary developmental biology. Cold Spring Harb.

Prudic, K. Developmental plasticity in sexual roles of butterfly species drives mutual sexual ornamentation.

Science , 73—75 Beldade, P. Evolution and molecular mechanisms of adaptive developmental plasticity. Oostra, V. Ecdysteroid hormones link the juvenile environment to alternative adult life histories in a seasonal insect. Translating environmental gradients into discontinuous reaction norms via hormone signalling in a polyphenic butterfly. Heuvel, J. The predictive adaptive response: modeling the life-history evolution of the butterfly bicyclus anynana in seasonal environments.

Saastamoinen, M. Wijngaarden, P. Artificial selection on the shape of reaction norms for eyespot size in the butterfly Bicyclus anynana: direct and correlated responses. Hoffmann, A. Heritable variation and evolution under favourable and unfavourable conditions. Holloway, G. The effect of new environment on adapted genetic architecture. Heredity 64 , — Environmental quality and evolutionary potential: lessons from wild populations.

Quantitative genetic analysis of responses to larval food limitation in a polyphenic butterfly indicates environment- and trait-specific effects.

Developmental plasticity and acclimation both contribute to adaptive responses to alternating seasons of plenty and of stress in Bicyclus butterflies. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics , — Carneiro, M. Evidence for widespread positive and purifying selection across the European Rabbit Oryctolagus cuniculus Genome.

Thornton, K. The neutral coalescent process for recent gene duplications and copy-number variants. Ayroles, J. Systems genetics of complex traits in Drosophila melanogaster.

Alvarez, M. Ten years of transcriptomics in wild populations: what have we learned about their ecology and evolution? Mousseau, T. Natural selection and the heritability of fitness components. Heredity 59 , — On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection. Harris, I. Chen, J. Temperature stress mediates decanalization and dominance of gene expression in Drosophila melanogaster.

PLoS Genet. Li, Y. Mapping determinants of gene expression plasticity by genetical genomics in C. Hodgins-Davis, A. Abundant gene-by-environment interactions in gene expression reaction norms to copper within Saccharomyces cerevisiae.

Genome Biol. McCairns, R. The adaptive potential of subtropical rainbowfish in the face of climate change: heritability and heritable plasticity for the expression of candidate genes. Gibbons, T. Gene expression plasticity in response to salinity acclimation in threespine stickleback ecotypes from different salinity habitats.

De Jong, M. Geographic variation in thermal plasticity of life history and wing pattern in Bicyclus anynana. Pijpe, J. Increased life span in a polyphenic butterfly artificially selected for starvation resistance. Zijlstra, W. Simultaneous selection on two fitness-related traits in the butterfly Bicyclus anynana. Evolution 57 , — Fischer, K. Cooler butterflies lay larger eggs: developmental plasticity versus acclimation. Mateus, A. Adaptive developmental plasticity: compartmentalized responses to environmental cues and to corresponding internal signals provide phenotypic flexibility.

BMC Biol. Monteiro, A. Differential expression of ecdysone receptor leads to variation in phenotypic plasticity across serial homologs. Transcriptome-wide differential gene expression in bicyclus anynana butterflies: female vision-related genes are more plastic. Kijimoto, T. The nutritionally responsive transcriptome of the polyphenic beetle Onthophagus taurus and the importance of sexual dimorphism and body region.

Haas, B. De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity.

Suzek, B. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics 31 , — Falda, M. Argot2: a large scale function prediction tool relying on semantic similarity of weighted Gene Ontology terms. BMC Bioinform. Langmead, B.

Fast gapped-read alignment with Bowtie 2. Methods 9 , —