Abstract
E.B. Ford’s 1964 book Ecological Genetics was a call for biologists to engage in multidisciplinary work in order to elucidate the link between genotype, phenotype, and fitness for ecologically relevant traits. In this review, we argue that the integration of an ecological genomics framework in studies of phenotypic plasticity is a promising approach to elucidate the causal links between genes and the environment, particularly during colonization of novel environments, environmental change, and speciation. This review highlights some of the questions and hypotheses generated from a mechanistic, evolutionary, and ecological perspective, in order to direct the continued and future use of genomic tools in the study of phenotypic plasticity.
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Acknowledgments
MM held a Vanier Canada Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada (NSERC), as well as a research allowance from Alberta Innovates Technology Futures (AITF). SMR is funded by an NSERC Discovery Grant and an AITF New Faculty Award. The authors wish to thank two reviewers for their insightful suggestions.
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Glossary: Some Definitions of Important Terms
- Adaptive plasticity
-
The production of alternative phenotypes (continuous or discrete) by the same genotype across some environmental variable, such that there is a better match between the organism and its environment (Beldade et al. 2011). Alleles that confer plasticity are more likely to spread through a population relative to competing alleles that do not confer plasticity.
- Behavioural plasticity
-
Environmentally-induced alternative behaviors displayed by a single genotype. Behavioral plasticity is difficult to define. Does an organism display behavioral plasticity if it switches from grazing when there are no predators to predator avoidance when predators are present? Or should behavioral plasticity be restricted to a single behavior type (i.e., different foraging tactics for different foods, or different predator avoidance strategies for different predators)? Or is behavior only plastic if one particular behavioral trait is expressed differently when the same environmental variable in manipulated, such as different foraging strategies for a single food under different light conditions, or different predator avoidance strategies for a single predator under different conspecific densities? One’s definition will determine the magnitude of the relationship one finds between behavioral plasticity and other reaction norms.
- Canalization
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See Robustness.
- Community genetics
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The study of how genes within a community shape the phenotypes and evolution of other members of the community, and the identification of genes that contribute to heritable community traits.
- Cryptic genetic variation
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The subset of standing genetic variation that exists in a population but does not affect the phenotype or performance under normal environmental conditions. Upon exposure to a novel environment, this genetic variation produces novel phenotypic variation, and may facilitate adaptation.
- Developmental noise
-
The production of alternative phenotypes by a single genotype under identical environmental conditions (Raser and O’Shea 2005) due to molecular stochasticity in the birth and death rates of transcripts, the effects of low-abundance regulatory proteins, the stickiness of proteins, and random fluctuations in promoter behavior (Raser and O’Shea 2005; Brettner and Masel 2012; Singh et al. 2012).
- Dominant plasticity
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In niche complementarity, occurs when a superior competitor with high resource use plasticity alters the resources it uses depending on the competitive environment.
- Ecological speciation
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A theory of speciation in which adaptive phenotypic and genetic divergence, contributing to reproductive isolation, is due to divergent selection (Nosil 2012).
- Environmental robustness (environmental
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canalization) The production of a stable reaction norm despite environmental perturbations. Non-plastic reaction norms are canalized against at least one environmental variable. A plastic reaction norm can be environmentally canalized if: (1) the reaction norm does not exhibit discontinuous change under extreme environments, or (2) the reaction norm maintains its height and slope in the presence of a second environmental variable.
- Epigenetics
-
The study of environmentally-induced, sometimes heritable modifications to the phenotype, caused by mechanisms other than changes to the underlying DNA sequence (i.e., DNA methylation, histone modification, etc.).
- Epigenome
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The entire suite of epigenetic modifications that have occurred in a particular cell, tissue, developmental stage, or organism, including the number and placement of methylated sites, the number and nature of histone modifications, etc.
- Flexible stem
-
A model of adaptive phenotypic divergence whereby an initially plastic ancestral population diverges into two populations residing in distinct environments, such that each population expresses opposing ends of a reaction norm. These phenotypes become genetically assimilated, such that plasticity is lost and phenotypic divergence is maintained (West-Eberhard 2003; Wund et al. 2008).
- Gene expression
-
The context-dependent production of gene product, including pre-mRNA, mRNA, microRNA, and protein. Context can include cell type, tissue type, genotype, developmental stage, time, and environment.
- Genetic assimilation
-
The evolved loss of adaptive phenotypic plasticity, such that environmental induction is no longer necessary for the production of the phenotype (Waddington 1953a, b).
- Genetic compensation
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The evolved loss of maladaptive phenotypic plasticity, resulting in phenotypic similarity (cryptic evolution) between populations living in regular and novel environments (Grether 2005).
- Genetic robustness (genetic robustness)
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The production of a stable reaction norm despite different genetic backgrounds (Gibson and Wagner 2000). Genotypically distinct individuals that display the same plastic or non-plastic reaction norm are genetically canalized against the alleles that differentiate them. A lack of genetic robustness can be evidenced by changes to the slope or height of the reaction norm.
- Hierarchy of plasticities
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The production of a plastic or non-plastic macrophenotype due to interactions between numerous underlying reaction norms (Bradshaw 1965).
- Macrophenotype
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The visible manifestation of numerous underlying phenotypes, sometimes referred to as the “end phenotype” (Beldade et al. 2011).
- Maladaptive plasticity
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The production of alternative phenotypes (continuous or discrete) by the same genotype across some environmental variable, such that the match between organism and environment is reduced (Ghalambor et al. 2007).
- Model organism
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Any non-human species that has been readily cultured or raised over many generations in a laboratory setting, for which genomic tools have been developed and applied, and that is used to answer biological questions that can be applied to other species. Examples: Arabidopsis, Drosophila, Daphnia, Mus. The ideal model species for ecological genomics has locally adapted populations, characterized phenotypic and genetic variation, a sequenced genome, a known phylogeny, and is studied by a large community of researchers (Feder and Mitchell-Olds 2003).
- Molecular phenotype
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Measures of context-specific gene expression or protein behavior (Ranz and Machado 2006; Pavey et al. 2010).
- Molecular plasticity
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A form of phenotypic plasticity that focuses on environmentally-sensitive gene expression or protein behavior (plasticity in the molecular phenotype).
- Neutral plasticity
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The production of alternative phenotypes (continuous or discrete) by the same genotype across some environmental variable, that does not contribute positively or negatively to fitness.
- Non-model organism
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Any species that has not been readily incorporated into biological research in the last several decades. Basic biological information, including genomic information, is often lacking for these organisms, although genomic tools may be developed and used.
- Non-plasticity
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A reaction norm with a slope of zero. Sometimes referred to as environmental robustness (Gibson and Wagner 2000). Non-plasticity may be adaptive, maladaptive, or neutral, relative to competing alleles that confer plasticity.
- Phenotypic accommodation
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A source of adaptive phenotypic novelty, in which a genetically- or environmentally-induced change to a phenotype during development is accommodated through plastic changes in other phenotypes (West-Eberhard 2005).
- Phenotypic capacitor
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Any phenotype that can suppress phenotypic variation that would otherwise be expressed via developmental noise, microenvironmental variation, and genotypic variation (Queitsch et al. 2002; Levy and Siegal 2008).
- Phenotypic plasticity
-
The environmentally sensitive production of alternative phenotypes by a single genotype (DeWitt and Scheiner2003).
- Plastic compensation
-
The production of phenotypic similarity between populations living in regular and novel environments, due to plasticity in some compensating phenotype. Without plasticity in the compensating phenotype, maladaptive plasticity would generate phenotypic divergence between populations. Usually comes with a cost to some other phenotype and may mask the existence of maladaptive plasticity (Morris and Rogers 2013).
- Plasticity-mediated population extinction
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(PMPE) The unsuccessful colonization of a new environment due to phenotypic plasticity induced by the new environment (Morris and Rogers 2013).
- Plasticity-mediated population persistence
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(PMPP) The successful colonization of a new environment due to phenotypic plasticity induced by the new environment (Baldwin 1896; Pavey et al. 2010).
- Proteome
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The full complement of proteins present within a particular context (see gene expression).
- Proteomic plasticity
-
A form of molecular plasticity that focuses on environmentally-sensitive protein abundance.
- Reaction norm
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A function of all possible phenotypic states across some environmental gradient.
- Robustness (Canalization)
-
The production of a stable reaction norm despite genetic, environmental, or stochastic perturbations. Both plastic and non-plastic reaction norms can display robustness (Waddington 1953a, b).
- Symmorphosis
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The theory that biological structures match their functional requirements, without unnecessarily exceeding those requirements. This includes the idea that the components of a system will not exceed in possible performance their weakest unit.
- Standing genetic variation (SGV)
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Genetic variation that exists at a single locus in natural populations (Barrett and Schluter 2008). One form of SGV, cryptic genetic variation (CGV), is not apparent until exposed by novel environments (Schlichting 2008).
- Stochastic robustness (Stochastic robustness)
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The production of a stable reaction norm despite stochasticity (developmental noise) in transcript abundance, protein activity, etc.
- Transcriptional plasticity
-
A form of molecular plasticity that focuses on environmentally-sensitive mRNA transcript abundance.
- Transcriptome
-
The full complement of mRNA present within a particular context (see gene expression).
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Morris, M., Rogers, S.M. (2014). Integrating Phenotypic Plasticity Within an Ecological Genomics Framework: Recent Insights from the Genomics, Evolution, Ecology, and Fitness of Plasticity. In: Landry, C., Aubin-Horth, N. (eds) Ecological Genomics. Advances in Experimental Medicine and Biology, vol 781. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7347-9_5
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